Microalgae Parameters
Microalgae Parameters
Shaikh Abdur Razzak, Khairul Bahar, K.M. Oajedul Islam, Abdul Khaleel Haniffa,
Mohammed Omar Faruque, S.M. Zakir Hossain, Mohammad M. Hossain
PII: S2666-9528(23)00058-4
DOI: https://doi.org/10.1016/j.gce.2023.10.004
Reference: GCE 195
Please cite this article as: S. Abdur Razzak, K. Bahar, K.M.O. Islam, A.K. Haniffa, M.O. Faruque, S.M.Z.
Hossain, M.M. Hossain, Microalgae cultivation in photobioreactors: Sustainable solutions for a greener
future, Green Chemical Engineering (2023), doi: https://doi.org/10.1016/j.gce.2023.10.004.
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© 2023 Institute of Process Engineering, Chinese Academy of Sciences. Publishing services by Elsevier
B.V. on behalf of KeAi Communication Co. Ltd.
GRAPHICAL ABSTRACT
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1 Microalgae Cultivation in Photobioreactors: Sustainable Solutions for
2 a Greener Future
3
4 Shaikh Abdur Razzak1,2*, Khairul Bahar1, K. M. Oajedul Islam1, Abdul Khaleel Haniffa1,
5 Mohammed Omar Faruque1, S. M. Zakir Hossain3, Mohammad M. Hossain1,2
6
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7 Chemical Engineering Department, King Fahd University of Petroleum and Minerals, Dhahran, Saudi
8 Arabia
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9 Center for Refining and Advanced Chemicals, King Fahd University of Petroleum & Minerals, Dhahran,
10 Saudi Arabia
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11 Department of Chemical Engineering, University of Bahrain, Zallaq, Kingdom of Bahrain
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13 Corresponding Author
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20 E-mail: srazzak@kfupm.edu.sa
21 Phone:+966138607460
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23 ABSTRACT
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34 concentrations, and pH on microalgae growth performance, including specific growth and biomass
35 productivity. The study also examines open systems like unstirred ponds, raceway ponds, and circular
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36 ponds and closed systems like horizontal tubular, vertical bubble-column, airlift, flat panel, and
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37 plastic-bag photobioreactors, comparing their pros and cons. To optimize microalgae cultivation, key
38 factors in photobioreactor design, including photosynthetic efficiencies, light-dark (L-D) cycles, CO2
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39 concentrations, mass transfer, hydrodynamics behavior, and pH, are extensively investigated. In
40 addition, the manuscript outlines recent developments in large-scale photobioreactors and highlights
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41 the challenges and opportunities associated with photobioreactor scale-up and design parameter
42 optimization, including genetic engineering and economic feasibility. This article is a vital resource
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43 for researchers, engineers, and industry professionals seeking sustainable bioprocesses and the
44 application of microalgae-based technologies.
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47 Table of Contents
48 Contents
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54 2.2 CO2 Biofixation and Capture ................................................................................................10
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55 2.3 Production of Biofuel & high-value products ......................................................................12
3. Parameters affecting the growth performance ............................................................................. 15
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57 3.1 Effect of light and solar Irradiation ......................................................................................17
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58 3.2 Effect of Temperature ..........................................................................................................19
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64 4.1.1 Unstirred Ponds ................................................................................................................. 32
65 4.1.2 Raceway Pond.................................................................................................................... 32
66 4.1.3 Circular Pond...................................................................................................................... 33
67 4.1.4 Constraints of open-water systems ................................................................................... 34
68 4.2 Closed System ......................................................................................................................34
69 4.2.1 Horizontal Tubular ............................................................................................................. 36
70 4.2.2 Vertical Bubble-column Tubular ........................................................................................ 37
71 4.2.3 Airlift .................................................................................................................................. 38
72 4.2.4 Flat panel ........................................................................................................................... 38
73 4.2.5 Plastic-bag ......................................................................................................................... 39
74 5. Principal factors in photobioreactor design .................................................................................. 39
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75 5.1 Photosynthetic Efficiencies and Light Irradiance .................................................................41
76 5.2 Light-dark (L-D) Cycles .........................................................................................................48
77 5.3 Mass Transfer & Hydrodynamics .........................................................................................50
78 6. Recent Development, Future Aspects, Opportunities, and Challenges ........................................ 53
79 6.1 Recent development of Large-Scale Photobioreactors .......................................................53
80 6.2 Photobioreactor Scale-up and design Parameters Optimization ........................................54
81 6.5 Oher Challenges ...................................................................................................................63
82 7. Conclusions .................................................................................................................................... 69
83 Acknowledgements............................................................................................................................ 70
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84 Nomenclature .................................................................................................................................... 70
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85 References ......................................................................................................................................... 72
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90 1. Introduction
91 Fossil fuels have become a crucial part of modern life, powering energy and electricity production
92 and improving living standards. However, their combustion releases carbon dioxide (CO2) into the
93 atmosphere, causing global climate change [1]. Saudi Arabia is a significant CO2 emitter, with
94 industries, electricity, transportation, and households being the major contributors [2]. Energy alone
95 is responsible for over 90% of Saudi Arabia's national CO2 emissions from fossil fuels [3]. Globally,
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96 power generation from fossil fuels accounts for one-third of all CO2 emissions [3]. Therefore,
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97 scientists worldwide are working to mitigate CO2 emissions and combat global warming [4].
98
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As cities grow and industries expand, the amount of wastewater they generate is increasing rapidly.
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99 Treating this wastewater is essential for protecting the environment, as excessive nutrients like
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100 nitrogen and phosphorus can lead to eutrophication and harm ecosystems [5]. Removing these
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101 nutrients from tertiary wastewater is crucial to reduce oxygen requirements in water bodies, protect
102 aquatic life, and maintain human health. There are several methods available for nutrient removal,
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103 including filtration, membrane technology, precipitation, advanced oxidation, and biological nutrient
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104 removal. However, these methods can be costly and produce hazardous waste sludge [6]. One
105 significant challenge is removing nitrogen and phosphorus simultaneously from tertiary wastewater
106 [7].
107 Microalgae are unicellular organisms that can convert solar energy into chemical energy through
108 photosynthesis, using CO2 as a carbon source [8]. They are more efficient at converting light into
109 energy than other plants. Microalgae can be grown in a photoautotrophic mode, where light is the
110 primary energy source and CO2 is the carbon source [9,10]. They are capable of producing lipids,
111 nitrogen, and phosphorus from media and converting them into valuable food additives and bioactive
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112 compounds [11,12]. Using wastewater as a growth medium can provide additional benefits, such as
113 removing nitrates, phosphates, and heavy metals [13]. It is used in the food industry, pharmaceuticals,
114 cosmetics, and even cancer treatment [14]. Microalgae are used in various industries, including food,
116 In a photosynthesis process, microalgae cultivation with wastewater offers many advantages to lessen
117 the aforesaid problems, including the following: i) the economic value of the tertiary wastewater
118 effluent in terms of water and nutrient recovery ii) nitrogen and phosphorus are removed from
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119 wastewater simultaneously iii) microalgae can grow much faster, about 10-50 times higher than
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120 terrestrial plant resulting in a CO2 conversion efficiency into organic compound iv) generation of
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large volumes of water that are suitable for recycling on-site and off-site or safe to discharge to surface
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122 water bodies v) production of algae biomass that is suitable for bioenergy generation [17–19]. A
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123 photobioreactor is the place where these algal species can be cultivated and harvested with control to
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124 achieve the desired output. Mass transfer, the impact of light, and pH are the three major parameters
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125 that allow controlling eventually desired output. Scaling up the laboratory scale to industrial is very
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126 much necessary to open the door to the microalgal economy. Much effort is necessary to know the
128 Advancements in microalgae engineering signify progress, innovations, and developments in the
129 application of engineering principles and techniques for the manipulation and utilization of
130 microalgae [20]. In simpler terms, it involves the pursuit of more efficient methods to harness the
131 capabilities of these minuscule algae across diverse applications. These strides encompass a spectrum
132 of crucial enhancements. Scientists and researchers are dedicated to breeding microalgae strains
133 characterized by accelerated growth rates, heightened production of valuable compounds such as
134 lipids and proteins, and resilience in the face of varying environmental conditions [21].
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135 Simultaneously, they are refining the design and functionality of cultivation equipment and systems
136 to create optimal growth environments for microalgae, thereby ensuring efficient nutrient utilization
137 and biomass production [22]. This optimization extends to the entire microalgae production process,
138 from cultivation to harvesting and downstream processing, with the aim of maximizing yields while
139 minimizing resource consumption[23]. Genetic engineering techniques are being employed to
140 manipulate the genetic makeup of microalgae, enhancing their capacity to produce biofuels or engage
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142 are developing strategies for recycling and repurposing resources like carbon dioxide and wastewater
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143 within the microalgae cultivation process, a sustainable practice that reduces resource expenditure
146 parameters such as light irradiance, construction material, and temperature, can be directly related to
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147 the design and mode of the photobioreactor. This review discusses different types of photobioreactors
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148 currently used for microalgae (open & closed systems), features, advantages, and disadvantages of
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149 control systems. Design components, construction and materials, growth parameters, and controls of
150 photobioreactors are key parameters that affect microalgae cultivation. Hydrodynamics and mass
151 transfer studies for photobioreactors are also discussed with other key parameters. Finally, a
152 comparison is made to discuss photobioreactors according to the most influencing parameters in
153 operation, issues, and challenges that need to be explored in the future. Laboratory-based analysis is
154 highly important to understand to grow suitable microalgae species in normal to harsh environments.
155 A significant challenge for the outdoor mass cultivation that supports the microalgal economy is the
156 transition from laboratory to industrial scale. To understand the behaviors and upgrade to an industrial
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158 2. Advantages of microalgae cultivation in photobioreactors
159 Microalgae are highly efficient in photosynthesis and have a much faster growth rate than land-based
160 plants. Some species of microalgae can even be harvested twice a day [26], and their annual yield can
161 be several times that of traditional food crops [27]. Microalgae can capture more CO2 from industrial
162 flue gases than conventional crops, making them attractive for reducing greenhouse gas emissions
163 [28,29]. Microalgae can be harvested for biodiesel, food, animal feed, biogas, and fertilizer, providing
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164 additional revenue and attracting investment [20,30]. Microalgae cultivation in photobioreactors
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165 offers numerous advantages that make it a promising and sustainable approach for various
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166 applications. The following are some of the main advantages of microalgae cultivations.
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167 2.1 Nutrient Recycling and Wastewater Treatment
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168 There is an incredible requirement to expand the most consistent knowledge for the treatment of
169 household wastewater in many developing countries. This type of treatment method ought to achieve
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170 numerous conditions, like easy design, utilization of non-modern equipment, good removal
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171 efficiency, and minimum capital expenses. Moreover, the regular growth of the population, the rapid
172 rise in urbanization, the expense, and ease of use of land are pivotal factors when selecting a
173 wastewater treatment system [31]. Appropriate wastewater treatment techniques are generally
174 categorized into three major types—physical, chemical, and biological. These processes might be
175 applied independently or in the arrangement based on the scope and nature of contamination.
176 Phosphorus, nitrogen, and carbon are nutrients that are essential to aquatic life. However, excess of
177 these nutrients in the water body may cause eutrophication and toxicity in water body.
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178 In water treatment process industries, secondary effluent primarily consists of nitrogen and
179 phosphate, which require extensive tertiary treatment. This treatment units are mainly biological
180 treatment types, where nitrate and phosphate are mostly treated. Phytoremediation indicates the
181 bioremediation or elimination of wastes from the environment utilizing microalgae, and it enjoys
182 many returns over other conventional remediation practices that are expensive, absorb enormous
183 energy, and make a substantial quantity of waste. Microalgae cells might be efficiently applied for
184 wastewater treatment as they possess an inherent character of nutrient, metal, and organic components
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185 elimination from the wastewater [32]. The utilization of microalgae for wastewater treatment in
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186 conjunction with energy production is very promising. A variety of non- pathogenic species,
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Chlorella, Scenedesmus, Spirulina, Chlamydomonas, are applied for the goals of Phycoremediation
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188 [33]. Currently, tertiary wastewater treatment using microalgae is fairly recognized [1]. Microalgae
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189 have the ability to eliminate nitrogen and phosphorus from tertiary wastewater simultaneously in both
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190 open and closed photobioreactor systems [34]. Microalgae are considered prokaryotic or eukaryotic
191 photosynthetic microorganisms that can grow up swiftly and reside in insensitive environmental
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192 situations due to their unicellular or straightforward multicellular form. Microalgae can be
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193 autotrophic, heterotrophic, or mixotrophic. Autotrophic algae use photosynthesis to convert water,
194 carbon dioxide, light, and other minerals into oxygen and biomass. All microalgae are obtainable in
195 earth ecosystems, not just water but also terrestrial, presenting a wide range of species residing in
196 various environmental settings. An innovative photobioreactor known as the Sequential Flow Baffled
198 microalgal and bacterial communities. The combination of microalgae and bacteria cultivated in
199 municipal wastewater yielded greater biomass and lipid production compared to their counterparts in
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201 This superior performance was attributed to the presence of trace elements such as iron and copper
202 in the municipal wastewater, which significantly boosted biomass production and consequently led
203 to higher lipid yields. Notably, both microbial cultures in the synthetic and municipal wastewater
204 media exhibited similar total nitrogen removal efficiencies, exceeding 97% [35].The primary
205 objective was to enhance the absorption of nitrogen into microalgal biomass when treating nutrient-
206 rich wastewater. The SFB-AlgalBac photobioreactor exhibited its best performance when operated
207 at an influent flow rate of 5.0 L/d, which corresponds to a hydraulic retention time (HRT) of 20 days.
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208 During this flow rate, we observed the highest rate of microalgal nitrogen assimilation (0.0271 /d)
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209 and the greatest biomass productivity (1350 mg/d) [36].
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210 2.2 CO2 Biofixation and Capture
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211 As a response to the problem of global warming, people all over the globe are searching for viable
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212 solutions. People are attempting to capture carbon dioxide from large point sources in order to prevent
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213 further emissions of the vast quantities of CO2 production [25]. These large CO2 point sources may
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214 include fossil fuel, natural gas combustion, other synthetic fuel plants, and fossil fuel-based hydrogen
215 production plants [37]. A method that has gained attention is the use of photosynthetic CO2
216 biofixation, which is considered environmentally friendly and energy efficient. While traditional
217 terrestrial plants can capture CO2, their slow growth rates limit their effectiveness to only 3-6% of
218 fossil fuel emissions [38,39]. On the other hand, microalgae offer a faster growth rate and can be used
219 for in-situ CO2 bioremediation, making them a promising technique for CO2 capture and storage
220 [18,40]. In fact, microalgae have been found to have the potential to capture up to 1.83 kg of CO2 per
221 kilogram, making them a valuable tool in the fight against global warming.
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222 Microalgae are tiny photosynthetic organisms that live in water and can capture CO2 through
223 photosynthesis. This process converts CO2 and sunlight into carbohydrates and releases oxygen (Fig.
224 1.). Microalgae are especially efficient at this process, which is known as "oxygenic photosynthesis".
225 CO2 is converted into lipids and hydrocarbons, making it a form of "CO2 fixation". Water is used as
226 the electron donor and releases oxygen. The general equation for photosynthesis is::
228
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229 This reaction converts the energy of light to chemical energy (ATP, NADPH). Then, by using this
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230 chemical energy, organic carbon is synthesized from inorganic carbon [41].
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231
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232 Fig. 1. Schematic diagram of the photosynthesis process for microalgae cultivation
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235 The production of biofuels and high-value products from microalgae is one of the key drivers for the
236 growing interest in microalgae cultivation in photobioreactors. Microalgae offer a sustainable and
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237 renewable source for the generation of biofuels and a wide range of valuable compounds with various
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238 industrial applications. Microalgae offer significant potential for biofuel production, encompassing
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239 biodiesel, bioethanol, and biogas [42]. With their high lipid content, microalgae can be efficiently
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240 converted into biodiesel through transesterification, presenting an advantage of increased
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241 productivity and reduced competition with food crops compared to conventional biodiesel sources.
242 Additionally, certain microalgae species produce carbohydrates that can be converted into bioethanol
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243 through fermentation, though further optimization is still underway to enhance its efficiency.
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244 Furthermore, anaerobic digestion of microalgae biomass yields biogas, primarily composed of
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245 methane, which can be harnessed for electricity generation or as a renewable substitute for natural
246 gas, contributing to sustainable energy solutions [43]. Presently, countries such as the USA, Canada,
247 and Brazil produce biofuel from food sources and biomass. But this food-based biofuel is criticized
248 as it is competing with the demands of food for humen. As an alternative, agricultural wastes,
249 municipal wastes, microalgae, and other microbial sources are used as non-food biofuel sources [44].
250 Nowadays, Microalgal-based renewable fuels are gaining increased attention because they have great
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252 Microalgae offer a diverse range of high-value products that hold significant potential for various
253 industries. Certain microalgae species, such as Nannochloropsis and Schizochytrium, are abundant
254 sources of omega-3 fatty acids, including docosahexaenoic acid (DHA) and eicosapentaenoic acid
255 (EPA), which play essential roles in human health and are widely used in dietary supplements and
256 functional foods [45]. Additionally, microalgae produce various pigments like chlorophyll,
257 carotenoids, and phycobiliproteins, finding applications in food coloring, cosmetics, and
258 pharmaceuticals due to their natural and safe characteristics [46]. Microalgae, such as astaxanthin
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259 and spirulina, are rich sources of antioxidants, which have potential health benefits and are commonly
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260 used in dietary supplements and beauty products [47,48]. Furthermore, microalgae-based bioplastics
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262 advantage of biodegradability and reduced environmental impact [49]. Lastly, the rich nutritional
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263 content of microalgae has led to investigations into their potential as nutraceuticals, addressing
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264 various health concerns and promoting overall well-being [50]. These findings underline the
265 significant value of microalgae in the development of innovative and sustainable high-value products,
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266 contributing to various industries and enhancing human health and environmental sustainability.
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267 Bioactive compounds, including carotenoids, phycobilins, polysaccharides, omega-3 fatty acids, and
268 phenolics, have been identified and isolated from microalgae [51].
269 Microalgae cultivation can be integrated with other industries, such as wastewater treatment plants
270 and power stations, where microalgae can utilize CO2 and nutrients from effluents or flue gases,
271 contributing to biofuel and high-value product production while helping in environmental
272 remediation. The integrated CO2 capture and wastewater treatment of microalgae cultures in a
273 photobioreactor are shown in Fig. 2.. And finally, cultivated biomass gives value-added biofuel and
274 non-biofuel high-value products. This system requires three main feeds: (i) CO2 from the flue gas
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275 stream from power plants or other stationary sources, (ii) Culture media (tertiary wastewater reach
276 with nitrate, phosphate, etc.), and (iii) light. The culture mainly progresses in the presence of natural
277 sunlight or other sources. The cultured microalgae can be further processed into the downstream
278 system. In this process, the microalgae are harvested and dried as collected biomass for further
279 products. Microalgae biomass can be used for further applications such as biofuel production,
280 fertilizer, food, etc. Thus, microalgae cultivation provides advantages: CO2 capture, Treatment of
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283
284 Fig. 2. Schematic flow diagram of an integrated system for CO2 capture, biomass separation, and fuel
285 and non-fuel production using the microalgae cultivation inside the photobioreactor by
286 photosynthesis process.
287
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288 3. Parameters affecting the growth performance
289 Microalgae, in general, unicellular phototrophs, are fast-growing microorganisms or, to be more
290 precise, they are fast-duplicating organisms with a great potential to generate biomass at a high rate
291 compared to other higher photosynthetic biomass sources like plants. The major advantage of
292 microalgae cultivation in photobioreactors is their reproduction time (properly duplication time) is
293 short; therefore, their growth rate is high with higher photosynthetic efficiency. But this limited light
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294 cultivation in photobioreactors, biomass growth rate is the function of light and solar irradiation,
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295 temperature, nutrient availabilities, CO2 concentration, and pH in culture media. These parameters
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296 are major components and must be considered in the mass-scale cultivation and design of
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297 photobioreactors. In general, the basic concept of biomass growth calculation is based on the
following equations of specific growth rate and biomass productivity.The specific growth rate, μg,
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299 described as the growth of the dry biomass weight per day, was computed using the following
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𝑋2
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𝑋1
301 𝜇𝑔 = (1)
𝑡2 −𝑡1
302 where, 𝑋1 and 𝑋2 is the dry biomass weight at time 𝑡1 and 𝑡2 , respectively, of the exponential
303 growth phase. The effect of limiting nutrient (nitrate) on the growth of microalgae was described by
𝑆
305 𝜇 = 𝑓(𝑆) = 𝜇̂ [ ] (2)
𝐾𝑆 +𝑆
306 where, 𝜇= specific growth rate, day-1; 𝜇̂ = maximum specific growth rate, day-1; 𝑆= limiting nutrient
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310 Fig. 3. Typical parameters that impact the growth of microalgae during the cultivation inside the
311 photobioreactor.
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313 The biomass productivity (Pb), which is also described as the rate of biomass production, was
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𝑋𝑡 −𝑋0
315 𝑃𝑏 = (3)
𝑡𝑡 −𝑡0
316 where, 𝑋0 and 𝑋𝑡 are the dry biomass weight at the beginning, at the time 𝑡0, and at the end of the
317 cultivation (growth phase), at time 𝑡𝑡, respectively. Fig. 3. listed typical parameters that impact
318 microalgae growth during the cultivation inside photobioreactors. Several microalgae species with
319 different growth metabolisms are used in the experiments. The factors that influence the biomass
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321 3.1 Effect of light and solar Irradiation
322 Light is a fundamental driver of photosynthesis, the process by which microalgae convert light energy
323 into chemical energy, leading to their growth and biomass production. The intensity, duration, and
324 quality of light significantly impact microalgae growth performance. Adequate light exposure
325 promotes photosynthetic activity, while excessive or insufficient light levels can lead to
326 photoinhibition or limited growth, respectively. The amount of photons reaching the culture's surface
327 (µmol photons m-2s-1) enables the determination of incoming light intensity as a function of photon
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328 flux density (PFD). How much PFD can be absorbed by cells is dependent on cell density, cell optical
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329 properties, culture mixing, and light penetration in the reactor; the remaining photons are either
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reflected or transformed to heat. Light-driven growth follows saturation kinetics, in which growth is
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331 accelerated, and maximal efficiency is observed after a threshold of light intensity is exceeded [58].
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332 As the intensity of light increases, saturation is reached, and growth remains constant; further
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333 increases may harm or kill the cells (e.g., photoinhibition) [59].
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334 Increased light intensity can boost microalgae growth, up to a certain point that varies depending on
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335 the species. But excessive light can lead to photo-inhibition. Light is a critical factor for microalgae
336 growth since it serves as their energy source when they grow as phototrophic organisms [60].
337 However, only around 10% of the light is converted to chemical energy while the rest is dissipated
338 as heat. Some studies suggest that the conversion rate may be as low as 2% [61]. Microalgae use light
339 to produce adenosine triphosphate (ATP), which is essential for cell maintenance and synthesis.
340 However, intense light can also impede the photosynthetic process [62].
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341 The kinetics related to light have been analyzed by Schediwy et al. (2019) [63]. All the experiments
342 were done in a small diameter PBR to visualize the effect of light. Light kinetics can be represented
343 as a correlation of light intensity, average specific growth, and photon availability,
344
1 𝐷𝑅
𝑟𝑋,𝑎𝑣 (𝐼ℎ𝑣,0 ) = 𝑟𝑋 ( ∫ 𝐼ℎ𝑣 (𝑙𝑝𝑎𝑡ℎ ). 𝑑𝑙𝑝𝑎𝑡ℎ ) (4)
𝐷𝑅 0
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1 𝐷𝑅
𝑟𝑋,𝑎𝑣,𝜇 (𝐼ℎ𝑣,0 ) = ( ∫ 𝑟𝑋 (𝐼ℎ𝑣 (𝑙𝑝𝑎𝑡ℎ )) . 𝑑𝑙𝑝𝑎𝑡ℎ ) (5)
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𝐷𝑅 0
346
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here, 𝑟𝑋,𝑎𝑣 indicates the average value for the specific growth rate with respect to the mean light
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347 intensity (𝐼ℎ𝑣,0 ). 𝐷𝑅 is the PBR diameter. 𝑙𝑝𝑎𝑡ℎ indicates the distance in the reactor that is crossed by
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348 light.
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349 The following equation can represent the CO2 transfer rate (CTR)
𝑀𝐶𝑂2
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𝐶𝑇𝑅𝑚𝑖𝑛 = .𝑟 .𝑐 .𝑒 (6)
𝑀𝑐 𝑥 𝑥 𝐶,𝑥
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350 here 𝑒𝐶,𝑥 is the carbon content of the cells/nutrients. Here c as a subscription mode indicates carbon.
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352 Monod saturation function was used to correlate the light intensity with the specific growth rate in
𝐼
354 𝜇 = 𝑓(𝐼) = 𝜇̂ [ ] (7)
𝐾𝑆 +𝐼
355 where, 𝜇= specific growth rate, day-1; 𝜇̂ = maximum specific growth rate, day-1; 𝐼 is the light
356 irradiance µmol photons m-2 s-1. ; 𝐾𝑆 = half saturation coefficient, mg/L. Not only the intensity of light
357 but quality also plays an important role in growth rate and microalgae biomass production.
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358 Light-driven growth follows saturation kinetics where growth is accelerated after a threshold of
359 intensity is passed, and maximal efficiency is observed. As light increases its intensity, saturation is
360 achieved, and growth becomes steady; further increases might damage the cells (e.g., photoinhibition)
361 or even kill them [59]. In order to replicate their natural environments, microalgae are typically
362 cultivated in dim light (60 to 400 µmol m−2 s−1) [64]. At a light intensity of 80 µmol m−2 s−1, the
363 highest growth of Chlorella vuygaris was observed [65]. A light intensity of 50 µmol m−2 s−1 of light
364 intensity is insufficient for microalgae growth, while 110 µmol m−2 s−1 of light intensity causes photo-
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365 inhibition [66]. For maximum lipid production, distinct microalgae species and strains require
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366 lighting intensities ranging from 60 to 700 µmol m−2 s−1. Strong light increases the triacylglycerol
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content disproportionately. The light intensity regulates the synthesis of fatty acids, carotenoids,
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368 including -carotene, lutein, and astaxanthin [67].
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369
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370 Temperature plays a crucial role in regulating microalgae growth rates and influencing biochemical
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371 pathways within cells. Different microalgae species have distinct temperature optima for growth, and
372 deviations from these optima can impact physiological processes and alter biomass productivity. The
373 maximum specific growth rate (𝜇̂ ), which appears in the Monod model, depends on temperature and
374 light intensity rather than the limiting nutrient content. Since the amount of light was supposed to be
375 constant, the maximal specific growth rate can only be a function of temperature, and the Arrhenius
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378 Where, 𝐴= constant, day-1; 𝐸= Activation energy, cal/mol; 𝑅= Universal gas constant, cal/K/mol;
379 𝑇= Temperature, K.
380 The growth of microalgae as a function of temperature and limiting nutrient concentration. The
381 specific growth rate in the Mondo model can be written as:
𝑆
382 𝜇 = 𝐴𝑒 −𝐸/𝑅𝑇 [ ] (9)
𝐾𝑆 (𝑇)+𝑆
383 The growth rate of microalgae is significantly influenced by temperature. In order for microalgae to
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384 grow well, the proper temperature must be provided. Extremely low or high temperatures could stunt
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385 the growth of microalgae. Algal growth can be accelerated by raising the temperature until it reaches
386
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the ideal level. The ideal temperature for growing algae is between 25°C and 30°C [68].
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387
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388 The environment has a cooling impact on the culture media in an open system, keeping it below 400
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389 degrees Celsius, which is an advantage of this method of cultivation. The chemical equilibrium, pH
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390 levels, and gas solubility in a system are all affected by temperature. The below-mentioned equation
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391 describes the Cardinal model, which can be used to illustrate the impact of temperature on microalgal
392 growth. The model provides insight into the range of possible values and their optimality for different
(𝑇−𝑇𝑚𝑎𝑥 )(𝑇−𝑇𝑚𝑖𝑛 )2
394 𝜇 (𝑇 ) = (10)
(𝑇𝑜𝑝𝑡 −𝑇𝑚𝑖𝑛 )[(𝑇𝑜𝑝𝑡 −𝑇𝑚𝑖𝑛 )(𝑇−𝑇𝑜𝑝𝑡 )−(𝑇𝑜𝑝𝑡 −𝑇𝑚𝑎𝑥 )(𝑇𝑜𝑝𝑡 +𝑇𝑚𝑖𝑛 −2𝑇)]
395
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396 3.3 Effect of Nitrogen and Phosphorus concentration
397 Microalgae require essential nutrients such as nitrogen and phosphorus for growth and biomass
398 accumulation. Impact of total nitrogen (TN) in the form of N-NO3 – and total phosphorus (TP) in the
399 form of PO43- concentration in the culture medium is very important for microalgae cultivation in
400 photobioreactors. Optimal nutrient concentrations are necessary to avoid nutrient limitation or excess,
401 which can affect cell division rates and overall productivity. These two parameters have a major
402 impact on biomass growth at the same time, the removal of these two substrates re the prime concern
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403 of wastewater treatment. There is an adequate growth model by which experimental behavior can be
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404 predicted. The Monod model is mostly used for measurement purposes in the nutrient media
406 𝜇= (11)
𝐾𝑠 +𝑆
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407 where, the 𝜇𝑚𝑎𝑥 indicates the maximum growth rate of the microalgae/biomass. S is the concentration
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408 of the substrate and 𝐾𝑠 embodies the half-saturation constant of the biomass in respect to the substrate.
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𝜇𝑚𝑎𝑥 .𝑆
411 𝜇= 𝑆2
− 𝜇𝑚 (12)
𝐾1 +𝑆+
𝐾2
412 where, 𝐾1 is the limiting constant, 𝐾2 is the inhibition constant; both have the unit of g/l. here, 𝜇𝑚
414 In batch kinetics experiments, the percentage rate of TN and TP removal was calculated using the
21
𝑆0 −𝑆𝑡
416 % 𝑟𝑒𝑚𝑜𝑣𝑎𝑙 = × 100 (13)
𝑆0
417 where 𝑆0 and 𝑆𝑡 are the substrate concentrations at the beginning, time 𝑡0, and at the end of the
419 Phosphorus also is an important nutrient after nitrogen. It is an essential nutrient component that
420 contains 1% of the cell’s dry weight [70]. The ideal N:P ratio is between 5:1 and 10:1 for microalgae
421 growth. Lipids accumulation is advanced with decreasing N and P concentrations in microalgae [71].
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422 However, biomass growth is reduced by reducing N and P concentrations. Table 1 has reported some
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423 comparison analyses of such species used for nitrogen and phosphorus removal. This table
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424 summarizes the impact of temperature, light irradiance, CO2 concentrations on some reported work
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425 on TN, TP removal, and biomass productivity. It is evident that some values of TN, TP removal, and
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426 maximum biomass production of microalgae species are comparable, higher, or less than those of
427 some reports. The difference can be explained because the strain type, growth conditions (e.g., growth
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428 media, photo period, photo intensity, temperature, pH, culture time, % of CO2, Nitrogen-phosphorus
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429 ratio, initial nitrogen and phosphorus concentrations), photo-reactor type, process type (e.g., batch or
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430 continuous). The nitrogen removal rates determined in all studies under all experimental conditions
431 are higher than those of phosphorus, as expected by the chemical composition of microalgae cell.
432 Due to the phenomenon of higher NP ratio requirement could reasonably associated with causing a
433 high inner PO43- pool. In some cases, Phosphate removal rate is higher due to initial concentration
434 remain same and nitrogen phosphorus ratio is higher. Different nitrogen to phosphorus ratio studies
435 are valid due to the tertiary wastewater and dairy wastewater also varies.
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436 3.4 Effect of CO2 Concentrations
437 CO2 is a critical substrate for photosynthesis, and its availability can directly impact microalgae
438 growth rates. Elevated CO2 levels can enhance photosynthetic efficiency and, consequently, biomass
439 productivity. Determining the total carbon content of microalgae allowed us to calculate the bio-
440 fixation rate of CO2, RCO2. The following equation was used to determine the total quantity of carbon
𝑇𝑂𝐶𝑏𝑖𝑜𝑚𝑎𝑠𝑠
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442 %𝐶 = × 100 (14)
𝑋
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443 where, TOCbiomass is the total organic carbon concentration of microalgal biomass (mg/L), X is the
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444 biomass concentration (mg/L) on a given day, and % C represents the percent carbon content in dry
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445 biomass.
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446 According to De Morais and Costa, the following equation can be used to determine the rate of carbon
𝑀𝑊𝐶𝑂2
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449 where, 𝑃𝐵 is the biomass productivity, 𝑀𝑊𝐶𝑂2 is the molecular weight CO2, and 𝑀𝑊𝐶 is the atomic
451 Gas mixture bubbling by spargers from the bottom of the photobioreactor can facilitate the mass
452 transfer of CO2 from gas to liquid [73,74]. CO2 concentration between 2%-4% gives the maximum
453 biomass productivity, specific growth rate, CO2 uptake for C. vulgaris [73,74]. For mixotrophic
454 growth of Nannochloropsis oculata 2% CO2 concentration gives both high growth of biomass and
455 lipid [75], while 8% CO2 can also provide high growth with good consumption of Nitrogen based
456 nutrients[76]. It depends on the purpose whether to produce lipids or CO2 capture the concentration
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457 of CO2. It should be kept in mind that gas holdup controls overall mass transfer in the photobioreactor.
458 Optimization of the pH is important not only for algal survive but also for reducing production costs.
459 Moraes et al. (2020) deployed a bioprocess methodology to increase biomass productivity and CO2
460 usage efficiencies in N. gaditana cultures under outdoor circumstances by adjusting pH and setting
461 control of this parameter in a tubular PBR . This allowed for lower carbon losses to the atmosphere
462 and overall process costs. In this context, CO2 on-demand pH control, in addition to encouraging pH
463 control, also adds to the carbon supply by the cultures. Under outdoor circumstances, N. gaditana
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464 cultures in tubular photobioreactors had the maximum biomass output (0.16 g L-1 d-1), CO2 usage
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465 efficiency (74.6 percent w/w), and RCO2/biomass (2.42 gCO2 gbiomass1 at pH 8.0.)
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466 3.5 Effect of pH
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467 pH directly influences various physiological and biochemical processes in microalgae. Maintaining
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468 an optimal pH range is essential for cell growth, enzyme activity, and nutrient uptake[78]. pH should
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469 be an appropriate range for the functioning of microalgal growth. A neutral pH range is favorable for
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470 ideal growth of most microalgae species. Also, acidic conditions are suitable for some species. pH
471 can be raised due to higher photosynthetic activity. The supplementation of CO2 can control
472 increasing pH. Neutral pH is beneficial, but pH as high as 10 and as low as 4 are acceptable by some
473 species [79,80]. Besides, pH can play an important role in the biochemical composition of
474 wastewater. For instance, Hodaifa et al. (2009) observed that pH greatly affects the growth and
476 Since CO2 solubility and accessibility are influenced by pH, it is one of the major environmental
477 aspects that affect microalgae's growth and metabolism [76]. The pH is the most important element
478 in determining the relative concentrations of carbonaceous species in water [5]. Fig. 4. illustrates the
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479 different inorganic carbon species with respect to mole fractions at different media pH [5]. Maximum
480 algal growth happens in the area of neutral pH (6.1-10) where CO2 in water could also be in the form
481 of CO2+H2 = H+ + HCO3- [68]. The synergic effect of pH with CO2 is very keen, and several works
482 have been done [82–84]. Higher CO2 concentrations could increase productivity, but pH will be
483 decreased, and physiology will be affected [74] By adjusting the balance, microalgae's uptake of CO2
484 from water reduces carbonate and bicarbonate while the excretion of OH- raises the pH. pH is mainly
485 the result of the equilibrium between highly soluble CO2, bicarbonate, and carbonate equilibrium.
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486 Algal species like to take bicarbonate from water instead of taking direct CO2 from the water. The
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487 cardinal model like the temperature effect also helps in determining the optimal pH value for
488
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microalgae growth. Most microalgae strains prefer to be cultivated in the culture media close to the
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489 neutral pH [85].
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(𝑝𝐻−𝑝𝐻𝑚𝑎𝑥 )(𝑝𝐻−𝑝𝐻𝑚𝑖𝑛 )2
490 𝜇(𝑝𝐻 ) =
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(𝑝𝐻𝑜𝑝𝑡 −𝑝𝐻𝑚𝑖𝑛 )[(𝑝𝐻𝑜𝑝𝑡 −𝑝𝐻𝑚𝑖𝑛 )(𝑝𝐻−𝑝𝐻𝑜𝑝𝑡 )−(𝑝𝐻𝑜𝑝𝑡 −𝑝𝐻𝑚𝑎𝑥 )(𝑝𝐻𝑜𝑝𝑡 +𝑝𝐻𝑚𝑖𝑛 −2𝑝𝐻)]
491 (16)
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492
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493 Fig. 4. Carbon mole fractions of several inorganic substances at varying medium pH.
494
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495 The above-mentioned characteristics affect the specific growth rates or biomass productivities
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496 of various types of microalgae species. The overall effects of temperature, light irradiance,
497 CO2 concentrations, TP removal from the medium, and biomass productivity of certain
498 microalgae species are summarized in Table 1. The table presents a comprehensive overview
499 of various microalgae species cultivated in different types of wastewater media, along with
500 key growth parameters and nutrient removal efficiency. In these studies, researchers
501 investigated the performance of microalgae under varying conditions to explore their
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503 For instance, Nayak et al. (2016) cultivated Scenedesmus sp. in domestic wastewater at a
504 temperature of 25°C, with a 12/12-hour light/day cycle and a light irradiance of 60 μmol m-
505 2 s-1. The microalgae achieved a maximum biomass concentration of 430 mg L-1 and
506 exhibited significant nutrient removal efficiency, with TN (Total Nitrogen) removal reaching
507 61.1% and TP (Total Phosphorus) removal at 81.9% [38]. In another study by Ji et al. (2013),
508 Scenedesmus obliquus was cultivated in tertiary treated wastewater at the same temperature
509 and a higher CO2 concentration of 15%. The cultivation period lasted 7 days, with a light
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irradiance of 45 μmol m-2 s-1. The microalgae achieved a biomass concentration of 310 mg L-
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510
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511 and displayed remarkable nutrient removal efficiency, with TN and TP removal both
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512 reaching 99% [86].
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513 Furthermore, the table includes research on synthetic wastewater and modified media.
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514 Álvarez-Díaz et al. (2017) investigated Chlorella Kessleri's growth in synthetic wastewater,
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515 achieving a maximum biomass concentration of 580 mg L-1 with almost complete nutrient
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516 removal (TN and TP both at 99%) [7]. Xin et al. (2010) explored Scenedesmus sp. growth in
517 wastewater and reported a biomass concentration of 120 mg L-1, with TN removal at 99% and
518 TP removal at 98% [87]. Lastly, two studies by Gao et al. (2019) and Hossain et al. (2022)
519 investigated Chlorella Kessleri's growth in modified BBM media. While Gao et al. (2019) did
520 not report nutrient removal data, Hossain et al. (2022) achieved impressive nutrient removal
521 efficiency, with TN removal ranging from 92% to 99% and TP removal from 19% to 88%
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523 Table 1: Impact of temperature, light Irradiance, CO2 concentrations on TN, TP removal, biomass productivities
Wastewater Microalgae species Temp CO2 Light/Day Light Cultivati Max. Initial Nutrient Reference
f
oo
Domestic 0.03 TN=41 TN=61.1
r
Scenedesmus sp. 25 12/12 60 7 430 [38]
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wastewater (air) TP= 53 TP= 81.9
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Tertiary treated TN=8.7 TN=99
Scenedesmus obliquus 25 15 45 7 310 [86]
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wastewater ur TP= 1.7 TP= 99
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TN=15.5 TN=99
Wastewater Scenedesmus sp. 25 - 55-60 15 120 [90]
TP= 0.5 TP= 98
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Phosphate
rich
f
oo
Modified BBM TN=48 TN=99
r
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Chlorella Kessleri 30 2 12/12 54 9 524 [91]
Media TP= 18 TP= 19
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524
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525 4. Photobioreactor Technologies
526 Photobioreactors are mostly used to produce algal biomass, pigments, and bioactive molecules [1].
527 Photobioreactors also have been designed for life support in outer space, removal of various
528 compounds from water, production of gas vesicles in cyanobacteria, CO2 removal, hydrogen
529 production, and macroalgal production. They are classified as closed or open-system
530 photobioreactors [92]. The photoautotrophic mode of microalgal culture, which uses light sources as
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531 the main source of energy and CO2 as the inorganic carbon source, is the most common cultivation
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532 method [9]. In the scientific literature, microalgae cultivation systems mainly depend on: a) the cost,
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533 b) local environment such as sunlight availability, local temperature, c) the source of nutrients, and
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534 d) the CO2 availability.
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535 In open ponds, high biomass productivity can be achieved with microalgae strains that are resistant
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536 to harsh culture environments, but contamination can be a major drawback [93]. However, open
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537 ponds have a simple technology but may not be economically viable due to the higher cost of
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538 downstream processing [94]. The choice of microalgae cultivation system should consider several
539 parameters such as the biological nature of the microalgae species, the cost of land and energy,
540 availability of nutrients and water for cultivation, local environment and climate conditions, and the
543 One of the most traditional and simple techniques for mass-producing microalgae is open pond
544 cultivation. Open ponds are a common option in the sector due to the costs involved in its
545 construction, maintenance, and operation [95]. Additional benefits of open pond systems include easy
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546 operation and maintenance, minimal energy demand, and scalability. Typically, paddle wheels and
547 baffles are installed in open pond systems to provide enough mixing, just as they would be in raceway
548 ponds. Fig. 6. illustrates examples of an open photobioreactor system (raceway pond) schematically.
549 As for open ponds, they are the cheapest system for microalgae cultivation than closed ones [27], but
550 they have some serious technical issues in addition to economic drawbacks. Open ponds subjected to
551 environmental conditions are difficult to control the light, temperature, and evaporation [96].
552 Although the pond produces big biomass, it needs a big area to grow and culture. Therefore, ponds
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553 will be exposed to contamination. In addition, the low percentage of CO2 in the, approximately 0.03-
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554 0.06% , leads to limitation in mass transfer and thus lowers the microalgae growth [8]. For
555
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commercial production of microalgae, the open systems (ponds) are the most convenient [97], where
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556 the open system is easy to clean after culture and very good for mass culture of algae. In addition, the
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557 culture of an open system has many advantages, as it is cheap to build and has high productivity[12].
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558 Open-air farming systems are commonly used for microalgae biomass production, and they include
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559 natural and synthetic ponds, raceway-type ponds, and inclined outward systems driven by paddle
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560 wheels. These systems are relatively simple to design and operate, but they have certain challenges
561 and drawbacks that have been identified over the past fifty years of study. Some of these challenges
562 and drawbacks include limited success with only a few species of microalgae, presence of predator
563 species, water supply issues due to evaporation loss, inefficient utilization of CO2, large area
564 requirements that can only make use of waste land, lower biomass productivity compared to closed
565 systems, and high cost of microalgae harvesting. Despite these challenges, open culture systems are
566 still being used for microalgae biomass production, and efforts are being made to improve their
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568 4.1.1 Unstirred Ponds
569 An unstirred open pond (Figure 5a) is a simple and commercially used system for cultivating some
570 microalgae species, as it is easy to construct [99]. However, due to the lack of mixing, it may not be
571 suitable for large-scale cultivation. One example of commercial-scale cultivation using this method
572 is with Dunaliella salina [100]. The ponds are typically shallow, around 50 cm in depth, with a
573 plastic film covering at the bottom [101]. The depth is kept less than 1 m to ensure sufficient light
574 penetration. Transparent plastic covering can be used to mitigate contamination issues. In Southeast
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575 Asia, over 30 tons per year of dried microalgae biomass have been harvested from unstirred natural
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576 lakes [102].
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577 4.1.2 Raceway Pond
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578 The "stirred paddle wheel open pond" or "raceway pond" is the most commonly used open culture
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579 system (Fig. 5b.), accounting for almost 95% of global algal production [103]. These ponds are
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580 shallow, usually between 15 to 25 cm in depth, and constructed as a single channel or groups of
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581 channels. Paddlewheels are used for mixing, and the culture is exposed to the open atmosphere to
582 regulate temperature through evaporation. These ponds are suitable for commercial scale production
583 of microalgae biomass and cyanobacteria [104]. The depth of the pond is optimized to provide enough
584 light and prevent evaporation while allowing proper mixing [105]. Raceway ponds are highly
585 productive, with biomass yields ranging from 60-100 mg dry weight L-1d-1, and are primarily used
586 for the culturing of Chlorella sp., Spiriluna platensis, Hematococcus sp. and Dunaliella salina [106].
587 Various commercial designs of raceway ponds have been used over the past three decades,
588 particularly the paddle wheel mixed type. The paddle wheel helps to circulate the cultured media in
589 the raceway pond loop, generating the required water velocity to prevent the settling of cells or the
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590 aggregation of cells via flocculation. A liquid velocity of more than 30 cm/s is commonly maintained
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592
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593 Fig. 5. Open Cultivation Systems: a) Solix Biofuel's open, undisturbed pond for growing chlorella in
594 Colorado, USA; b) Carbon Corporation's paddle wheel racing pond in California, USA. c) Taiwan's Circular
596
598 Circular ponds (Fig. 5c.) have been primarily used for large-scale cultivation in South East Asia for
599 the culture of Chlorella sp. [108]. These are the oldest large-scale algae cultivation open-ponds with
600 a depth of about 30-70 cm. Microalgae are grown in concrete circular ponds up to 45 m in diameter,
601 with agitation by a rotating arm that moves a 20-30 cm thick layer of inorganic nutrient solution with
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602 algae. These systems have limitations such as less control on temperature, high capital and operational
603 costs, and higher contamination risks. Contamination risks are sometimes reduced by covering these
604 ponds with a greenhouse, which also increases biomass yield [109].
606 The challenges associated with open systems for microalgal production are numerous. These include
607 poor light utilization by cells, significant evaporative losses, limited diffusion of CO2 from the
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608 atmosphere, and the need for large land areas [108]. Additionally, open systems are prone to
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609 contamination by unwanted biological agents such as algae, mold, fungi, yeast, and bacteria [110].
610
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Various methods have been proposed to mitigate these issues, including the use of plastic covers or
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611 greenhouses over open ponds to improve biomass productivity and extend the growing period [111].
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612 However, contamination issues still persist, and capital costs, maintenance, and overheating can make
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614 Commercially successful microalgal species that thrive in open ponds are those that can withstand
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615 harsh environments and competition. Examples of such species are Dunaliella, Spirulina, and
616 Chlorella, which can grow in high saline water, alkaline environments, and nutrient-rich water,
617 respectively. Evaporative water loss is a significant challenge that affects the success of open pond
618 systems [113]. However, the main drawback of these systems is the lack of sufficient control
621 Open pond systems have reached their maximum productivity, and it is not economically feasible to
622 enhance their output. Therefore, many researchers have suggested the need for closed reactor systems
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623 for future large-scale biomass production. Over time, the cost of closed reactors is expected to
624 decrease, making them the most popular microalgae culturing systems. Various designs of closed
625 photo-bioreactors have been developed to achieve better growth control and operating parameters.
626 The three most common types for larger-scale cultivation systems are horizontal tubular reactors,
627 vertical column reactors, and flat plate or panel (FP) type photo-bioreactors [114]. Fig. 6. shows the
629 To overcome the limitations of open systems, closed systems were developed. The closed system's
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630 primary objective is to provide an environment for cultivating a monoculture of microalgae with very
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631 low contamination to produce high-value and biochemical metabolites. The basic structure of the
632
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reactor comprises a closed vessel in which the microalgae are cultivated by using artificial
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633 illumination or by using direct sunlight. Due to a high surface area to volume ratio, closed
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634 photobioreactors are multiple times more efficient than the open system, but the process isn’t
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635 economical [115]. The closed-system photobioreactors are classified based on the geometric
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636 configuration, which are discussed in detail below. Though the closed system yields higher biomass
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637 concentration with better quality, it is also expensive. To evaluate, the advantages and disadvantages
639 A closed system has many advantages, such as controlling the microalgae growth, preventing
640 contamination, limiting the transfer of gasses or bacteria between inside and outside, manipulating
641 the system, and optimizing the system [18]. In addition, closed (PBRS) is preferred when the slow-
642 growing is required for microalgae because they allow controlling microalgae species [117]. Close
643 photobioreactor has high efficiency in photosynthesis and very good control [118]. It can be bulk
644 vertical instead of horizontal to reduce the required area and decrease water loss via evaporation [119]
645 and to decrease the water loss via evaporation [120]. However, this type of reactor has many
35
646 drawbacks, such as the high cost of building and operating, oxygen accumulation, difficulty in scaling
647 up, and the cells being subjected to death because of the material structure used in the photo process
648 [118].
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649
650 Fig. 6. Closed Cultivation System: a) Horizontal Tubular b) Bubble column c) Airlift tubular; d) Flat
651 panel, and e) Large-scale plastic-bag photobioreactors.
653 Horizontal tubular photobioreactors are constructed with transparent materials and placed in outdoor
654 facilities under sunlight irradiation (as shown in Fig. 6a.). These cultivation vessel designs have a
655 large surface area per unit volume to maximize exposure of microalgae to sunlight. The tube sizes
36
656 are generally less than 10 centimeters in diameter to ensure sunlight penetration. In a typical tubular
657 microalgae culture system, the medium is circulated through the tubes, which are exposed to sunlight
658 for photosynthesis. The medium is then circulated back to a reservoir with the help of a mechanical
659 or airlift pump, which maintains a highly turbulent flow within the reactor to prevent algal biomass
660 from settling. A fraction of the algae is usually harvested after it circulates through the solar collection
661 tubes, making the system a continuous operation. However, most tubular photobioreactors studied in
662 the presence of artificial light have been developed at a small/laboratory scale (0-20 L capacities),
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663 and there are limited studies reporting data for large-scale closed photobioreactors. James and Al-
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664 Khars (1990) studied the growth and productivity of Chlorella and Nannochloropsis in a translucent
665
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vertical airlift photobioreactor, and they obtained productivities between 109 and 264 g m-3 d -1 for
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666 Nannochlropsis and between 32.5 and 95.3 g m-3 d -1 for the Chlorella strain [121].
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667
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668 Bubble column vertical tubular reactors (Fig. 6b.) are designed with double height to its diameter,
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669 giving high surface-to-volume ratio with optimal heat & mass transfer along the reactor [122].
670 Internal illumination setup is much preferred as it enhances the energy required for photosynthesis.
671 The gas flow rate and the light/dark cycles are crucial factors for biomass yield and efficiency of
672 photosynthesis [123]. A vertical glass tube measuring 5 cm in diameter and 2.3 m in height (4.5 L)
673 was utilized by Miyamoto et al. (1988) [124] . he bubble column unit lets in plenty of light. It is yet
674 unclear how feasible it will be to deploy on a commercial basis. Production rates of 23 g m- 3 d- 1 of
37
676 4.2.3 Airlift
677 Airlift photobioreactors (Fig. 6c.) use a baffle or a draft tube to divide the vessel's fluid volume into
678 two interconnected zones, creating large circulatory currents. While these reactors have advantages
679 such as high mass transfer, good mixing with low shear stress, low energy consumption, and easy
680 operation under sterile conditions, they are difficult to scale up due to their complex flow pattern
681 [125]. Cycling effects occurring between lighter and darker zones in these reactors make them
682 suitable for both pure algae culture and algae wastewater co-cultivation, and they have a high surface
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683 area to volume ratio and cell density. Agitation is achieved through air bubbling or mechanical motor
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684 rotation through the perforated tube, which helps with mixing, optimal nutrient transfer, light
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distribution, and preventing the accumulation of oxygen.
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687 Vertical flat panel photobioreactors (Fig. 6d.) mixed with air bubbling are considered superior to
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688 bubble columns in terms of productivity and ease of operation. They offer a large irradiated surface
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689 area, are suitable for outdoor cultures, and are good for algae immobilization, allowing for good
690 biomass productivity [126]. They are relatively inexpensive and easy to clean. These
691 photobioreactors can be accommodated in 1000-2000 L volume capacity units and have been
692 successfully operated for several days [112]. Closed flat panels with bubbling air can achieve high
693 ground-aerial productivity in volume cultivation. A 500 L unit with 440 L culture volume capacity
694 was able to achieve 0.27 gL-1d-1 using a flat plate glass photobioreactor [127]. However, there are
695 limitations to flat panel bioreactors, such as difficulty in controlling culture temperature, a limited
696 degree of growth at the near-wall region, and the possibility of hydrodynamic stress [126,127].
697 Although they have some limitations, such as difficulty in controlling culture temperature and
38
698 hydrodynamic stress, flat panel bioreactors have minimal risk of oxygen accumulation with high
700 Flat plate photobioreactors are recommended for mass production of microalgae in both indoor and
701 outdoor culture systems due to their high irradiation of plate surface, small accumulation of dissolved
702 oxygen, and convenient modular design for scale-up. Pulzl et al. (1995) optimized a large-scale flat
703 plate photobioreactor module of 6000L, with one layer for the circulation of the culture and the other
704 for the circulation of temperature-controlled water [129]. High productivity was obtained, given the
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705 high surface/volume ratio. However, photo-inhibition and temperature control issues could limit
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706 biomass output.
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707 4.2.5 Plastic-bag
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708 Microalgae can be produced in transparent polyethylene bags (Fig. 6d.) through sunlight irradiation,
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709 with air mixing at the bottom of the bags [130]. These bags can be hung or placed in a cage for
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710 cultivation, and transparent polyethylene sleeves are also commonly used to prevent cell settling.
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711 Turbidostats using 50 liters of polyethylene bag cultures have been successfully operated. However,
712 careful consideration should be given to potential issues with photo-inhibition and cell settling.
714 Photobioreactor design for microalgae cultivation must take into account various parameters,
715 including the surface area to volume ratio, mixing of the culture media, illumination, supply of CO2
716 or air, temperature, and dissolved oxygen. A good photobioreactor should have an effective
717 illumination area, optimal gas-liquid transfer rate, ease of operation, low potential for contamination,
718 low capital and production costs, and minimal land area requirements [61]. The design and selection
39
719 of photobioreactors for microalgae production depend on various factors such as surface area to
720 volume ratio, media mixing, illumination, CO2 or air supply, temperature, and dissolved oxygen.
721 Bioreactors can be open or closed, with closed systems offering better control of operational
722 variables. However, closed photobioreactors are more expensive and complicated to operate
723 compared to open systems, which use direct sunlight but are affected by weather fluctuations.
724 Therefore, open cultivation is recommended only in regions with high solar radiation [131]. Closed
725 photobioreactors are now considered a useful method for algal mass culture, with some research
of
726 suggesting they are the most feasible option for CO2 removal and treatment. Operational difficulties
ro
727 with open ponds make them less preferable, as the production process depends primarily on local
728
-p
climatic conditions. Table 2 compares the production of microalgae in open and closed
re
729 photobioreactors.
lP
730
na
731 Table 2: Comparative study between open and closed photobioreactors system regarding the
Factors
Photobioreactors photobioreactors
40
Energy (power and heat) requirement ±57 MJ m-2 y-1 ±207 MJ m-2 y-1 [134]
of
Contamination Higher None [136]
ro
Quality of biomass Variable Reproducible [136]
734 Photosynthetic efficiency refers to the amount of light energy that can convert atmospheric carbon
735 dioxide by microalgae into chemical energy through photosynthesis. Higher light irradiance has a
736 higher chance of accumulating more carbohydrates, lipids, and biomass productivities. In addition
737 to light intensity, it is also essential to understand that the irradiance is not homogenous, especially
738 in the dense culture where the light penetration is relatively low[137]. Furthermore, CO2
739 concentration should also be considered as it is a major source of carbon in most the reactor set-up,
41
740 and additionally, it helps in maintaining the optimal pH for the medium. The below model shows the
741 effect of growth considering the light intensity and CO2 concentration. In some cases, CO2 may also
𝐼𝑎𝑣
𝐼𝑎𝑣 (1− ) 𝑝𝐶𝑂2
𝐼𝑜𝑝𝑡
743 𝜇 = 𝜇𝑚𝑎𝑥 ∗ ∗𝑒 ∗( 𝑝𝐶𝑂2 ) (17)
𝐼𝑜𝑝𝑡 𝐾𝑆 +𝑝𝐶𝑂2 +
𝐾𝐼
744 where 𝜇𝑚𝑎𝑥 - maximum specific growth rate, 𝐼𝑎𝑣 – intensity of light, 𝐼𝑜𝑝𝑡 – intensity of light when
of
745 𝜇 = 𝜇𝑚𝑎𝑥 , 𝑝𝐶𝑂2 – partial pressure of CO2, 𝐾𝑆 – Saturation constant of substrate and 𝐾𝐼 – constant
ro
746 for inhibition. The parameter that characterizes the radiation of light absorbed by the microalgae
747
-p
during production is known as the light regime. Appropriate light intensity, wavelength, and duration
re
748 are essential for optimal growth rate. As discussed earlier, the photosynthesis mechanism is triggered
lP
749 by the light photons acting as the energy source. The light which passes through the photobioreactor
na
750 is used for producing chemical energy, and the Lambert-Beer law is used for describing the light
753 where z is the flat plat depth in the photobioreactor, α is the absorption coefficient, Io is the irradiance
754 of light source and I(z) is the irradiance at the length z. It is important that the microalgae get imposed
755 with sufficient light to saturate the active sites during the passage of photons, and simultaneously
756 photoinhibition need to be prevented. Having said that, the irradiance at a particular depth is difficult
757 to find out, in order to overcome this problem, the average radiation intensity shall be considered
758 [140].
I0
759 Iav = (1 − 𝑒 −𝛼𝑋𝑧 ) (19)
𝛼𝑋𝑧
42
760 This model is relatively simple as it considers only light transfer to the photobioreactor, and the light
of
ro
-p
re
lP
na
762
ur
763 Fig. 7.: Photobioreactor Illumination Zones. The growth rate is maximum near the illuminated wall,
Jo
764 known as the light saturation zone (or, alternatively, photoinhibition). Illuminance between Is and Im:
765 μ is linear on I. I < Im: the culture declines.
766 Fig. 7. presents the Illuminance profile as it decreases exponentially from the illuminated face of the
767 reactor. To keep it simple, one-dimensional geometry has been considered. The space coordinate here
768 is z, which denotes the distance from the light source. This figure further illustrates the specific
769 growth rate (μ) of these microalgae. There are three different illumination zones in the
770 photobioreactor, which represent different growth regimes. The first zone is the light-saturated zone
771 where the growth rate is maximum which spreads from the illuminated wall to the point where the
772 illuminance reaches Is. Any value of I more than Is will not increase the biomass growth rate rather it
43
773 may result in a decrease in the growth rate if photoinhibition occurs. Additionally, in the zone which
774 spreads between Is and Im, there is a linear relationship between growth rate and irradiance. Irradiance
775 represented by Im does not result in any distinct photosynthetic growth, but it is just for maintenance
776 in which the biomass is continuously consumed. For I < Im, the concentration of biomass may
777 decrease as the growth rate is below the rate of consumption by maintenance. By considering a
778 photobioreactor where the distance from the light source to every biomass cell remains constant, the
779 integration of the rates over the whole volume of the photobioreactor for a steady-state situation shall
of
780 results in the average biomass growth rate:
ro
1
781 𝜇𝑎𝑣 = ∫ 𝜇(I(𝑧))𝑑𝑧 (20)
-p
𝑧𝑓 re
782 where 𝑧 is the distance from the light source, I is the illuminance local value, 𝑧𝑓 is the reference
lP
783 distance, and I is related to z via the optical decay equation appropriate to the system, I(𝑧) [141].
na
784 Optimum illumination is an important parameter to produce microalgae. The amount of light varies
ur
785 from species to species. Various light/dark ratio gives different production rate. Many literatures
Jo
786 cared about different light/ dark cycles to experience the best biomass production rate.
787 Table 3 shows the photosynthetic efficiency, biomass productivity and light intensity of various algal
788 cultivation systems. For example, a new ultra-flat panel developed by Gifuni et al. (2018) with a
789 thickness of 3 mm was fabricated to increase biomass productivity. Cell growth, biochemical
790 composition, and photosynthesis rate were investigated in different light irradiance ranges of 50-1000
791 µmol m-2 s-1 of Chlorella sorokiniana [142]. Reports the effect of light irradiance in the following
792 range 0-1000 µmol m-2 s-1 upon the growth rate, biomass concentration, and productivity. It is found
793 from their study that high irradiance results in higher superficial productivity (3.45 g/m2.h) and
794 maximum biomass concentration (24 g/L). For the growth rate, the scenario is a little bit different.
44
795 The maximum growth rate was found at 0.17 h-1 with 300 µmol m-2 s-1. Some biological or physical
of
ro
-p
re
lP
na
ur
Jo
45
797 Table 3. Photosynthetic efficiency, biomass productivity and light intensity of various algal cultivation systems.
Photobioreactor Volm Location light Biomass PE Microalgae Illuminated Light Light intensity References
f
oo
LED
Chlorella
Ultra Flat Pannel 0.3 Indoor - 0.50 3-5 floodlight 50-1000 [142]
r
sorokiniana
-p
lamps
re
2.3– Nannochloropsis
lP
Horizontal tubular 98 Outdoor 4.3 0.51–0.76 – Sunlight 857 [143]
3.5 sp.
na
Tetraselmis
Airlift column 120 Outdoor 40 0.42 9.3 5.3 Sunlight 900 [144]
ur
suecica
Jo
2.4– Nannochloropsis
Vertical tubular 1060 Outdoor 4.6 0.31–0.71 31.0 Sunlight – [145]
4.2 sp.
0.97–
Raceway pond 100 Outdoor 30 0.04 Muriellopsis sp. – Sunlight 1449 [146]
0.69
Nannochloropsis
Raceway pond 7500 Outdoor 15 0.02 1 50 Sunlight 490 [147]
salina
46
Artificial
Vertical Tubular 2 Indoor 5 0.7 7 C. reinhardtii 0.1 200 [148]
light
Thin-layer inclined
2200 Outdoor 0.6 1.9 4 Chlorella spp. 224 Sunlight 540 [149]
cascades
Stichococcus Artificial
Bubble column 1.7 Indoor 4 0.3 7 0.002 300 [150]
bacillaris light
f
oo
Scenedesmus
Flat panel 45 Outdoor 2.1 20 14 2 Sunlight 1656 [151]
r
-p
obliquus
re
Combined
lP
natural
Nannochloropsis
na
Helical tubular 588 Outdoor 9.7 1.8 8 20.8 and 700 [152]
sp.
artificial
ur
light
Jo
798
47
799 5.2 Light-dark (L-D) Cycles
800 Light is one of the most important factors for photosynthesis and affects photosynthesis directly. As
801 a result, PBR should have the capacity to be exposed and transfer as much light as possible. For this
802 reason, PBRs are commonly constructed with highly transparent materials with minimum reflection
803 along with very high surface area to volume ratio. Defining light regimes is very crucial for
804 PBRs.[153]. Light intensity and the light/dark (L/D) cycle is a methods to control light [154]. To
805 control the light intensity lux meter and light: dark period alteration can be used in vertical PBRs for
of
806 better control. Batch and fed-batch cultivation can also be another addition. Rattanapoltee et al.
ro
807 (2021) cultivated Scenedesmus incrassulatus in a vertical tubular photobioreactor under batch/fed-
808 -p
batch modes and concluded fed-batch cultivation has higher biomass and lipid (in it) production.
re
809 Gonçalves et al. (2019) introduced a spiral LED strip in the inner portion of the PVC pipe while the
lP
810 vertical PBR inside of that spiral infrastructure to cultivate Tetradesmus sp.
na
811 The light/dark (L/D) cycle is critical for growth and biomolecule production. The impact of the L/D
ur
812 ratio on the growth and other parameters of C. thermophilla was studied by Sarkar et al. (2021). In
Jo
813 contrast, 4500 lx and 24:0 L/D, 4500 lx and 14:10 L/D, the latter of which includes a dark time, were
814 shown to have the maximum biomass and chlorophyll content. It was discovered that the varying
815 intensity of 0~4500 lx with 14:10 L/D produced the most proteins. Alternatively, under 4500 lx with
816 24:0 L/D, carbohydrate and carotenoid buildup increased. 4500 lx with 14:10 L/D had the highest
817 productivity in all circumstances due to larger cellular accumulation. A number of studies have shown
818 that every parameter that increases microalgal biomass production also increases nutrient absorption
819 (e.g., N and P). For example, in the development of a treatment of WWT with C. vulgaris, Azizi et
820 al. [157] found increasing the light irradiation from 100 to 300 µmol m-2 s-1 and extending the light
48
822 productivity and nutrient assimilation. Furthermore, the highest biomass production and nitrate and
823 phosphate removal were achieved in the 300 µmol m-2 s-1 and 24–0 L/D regimes. As the L/D ratio
824 influence the growth, other factors may be affected by this. For example, in the case of membrane
825 PBR 16:8 L/D gives the fastest fouling of membrane while working with C. vulgaris while 24: 0
827 The introduction of various intensities of lights can be a good procedure to stimulate production in
828 the photobioreactor. For example, Gonçalves et al. worked with different spectral combinations and
of
829 intensities within a 24:00 h light: dark period, which showed the variation in biomass production,
ro
830 carotenoids, and chlorophylls for Ttradesmus sp. The LEDs emitting light with white; red; yellow;
831
-p
green, and blue spectrum were used alone and/or combined, with intensities varying from 13 to 190
re
832 μmolm−2 s−1, and found to have a high growth rate in the highest energy light blue in all cases. A
lP
833 combination of different types of light indicates visible light with green light, giving the highest
na
834 biomass concentration, while the red-green combination provides the highest biopigments in that case
ur
835 [155]. It has also been seen earlier depending on the product of interest, the light regime can affect
Jo
836 differently. As for thermophilic Synechococcus sp. production of thermostable C-phycocyanin (PC)
837 in tubular PBRs was achieved maximum under 16:8 L/D ratio while the constant illumination of red
838 light gives the maximum SGR ( 1.918 d-1) and biomass concentration (5.11 g/L) [159]. N. gaditana
839 metabolome and transcriptome modifications were considerable after exposure to narrow red
840 light.[160] N. gaditana metabolome and transcriptome modifications were considerable after
841 exposure to narrow red light.[160] The light color greatly impacts growth depending on the species.
842 Using white LED in conjunction with a typical fluorescent lamp (12 h:12 h) may effectively replace
49
844 5.3 Mass Transfer & Hydrodynamics
845 Mass transfer and hydrodynamics are crucial factors in the design and operation of photobioreactors
846 for microalgae cultivation, having a substantial effect on system performance and yield. Mass transfer
847 is the exchange of gases (e.g., CO2 and O2) and nutrients (e.g., nitrogen and phosphorus) between the
848 microalgae culture and its surrounding environment. Mass transfer is essential for supplying
849 microalgae cells with adequate nutrients and CO2 and removing waste products such as oxygen from
850 the culture medium. Poor mass transfer can hinder the development of microalgae and reduce biomass
of
851 production. The rate of CO2 supply to the photobioreactor, light intensity influencing the rate of
ro
852 photosynthesis, and the diffusivity and solubility of gases and nutrients in the medium are all factors
853 -p
that influence mass transfer. Hydrodynamics, on the other hand, refers to the fluid flow behavior
re
854 within the photobioreactor, which ensures uniform distribution of microalgae and nutrients, prevents
lP
855 settling, and minimizes detrimental shear stress on delicate microalgae cells. The selection of an
na
856 appropriate flow regime (laminar, transitional, or turbulent), impeller design to influence flow
ur
857 patterns and shear stress, and adequate aeration to maintain dissolved oxygen concentration for
Jo
858 respiration are important factors in hydrodynamics. Achieving a balance between mass transfer and
859 hydrodynamics is essential for optimizing the growth and productivity of microalgae in
860 photobioreactors, facilitating the design of efficient and scalable systems through continuous research
861 and optimization. This facilitates the cultivation of microalgae for applications such as biofuel
863 Turbulent mixing properties and better mass transfer are desired for good biomass production. Gas-
864 liquid two-phase flow serves better in this respect when compared to single-phase flow. This system
865 can also be considered a three-phase system where the concentration of supplied CO2 decreases
866 gradually [162]. However, vigorous mixing has several advantages, including uniform distribution of
50
867 nutrients, good biomass production, taking away generated O2 and heat, keeping pH and temperature
868 uniform, proper light achievement by every microorganism without settling down at the bottom of
869 the reactor, etc. But with high velocity, the microalgae are susceptible to cell wall damage resulting
870 in cell death [163–165]. Experiment and numerical simulation studies have been used extensively
871 over the last decade to validate the features of gas-liquid flow and mass transfer in various types of
872 PBRs [166–168]. Because of the complexity of the integrated system numerical and CFD modeling
873 has the huge potential to resolve this problem. The existence of cells affects the overall volumetric
of
874 mass transfer coefficient, kLa [s−1 or h−1], but the gas-liquid mass transfer rate is closely linked to the
ro
875 growth rate[169].
876
-p
The growth kinetics of the photobioreactor is to evaluate the mass transfer of carbon dioxide entering
re
877 the system and the transfer of oxygen to the culture media as a product gas. The mass transfer aspect
lP
878 can be improved by the use of aeration and a good mixing hydrodynamics behavior. Studying the
na
879 mass transfer aids in assessing the operation hydrodynamic variables such as gas power, agitation,
ur
880 gas flow, and the average bubble diameter. Each of these variables is designed to ensure efficient
Jo
881 mass transfer between the liquid and gas [170]. The equation commonly used to represent the mass
882 transfer phenomena is given below, which gives the expression of NCO2 the mole flux transferred
∗
884 𝑁𝐶𝑂2 = 𝐾𝐿 𝑎(𝐶𝐶𝑂2
− 𝐶𝐶𝑂2 ) (21)
∗
885 𝐶𝐶𝑂2
is the concentration at equilibrium which is 0.1525 g/L according to the Henry’s law at 25 C.
886 The volume of gas in the reactor is estimated by the gas flow and gas hold-up (ε).
𝑉𝑔
887 𝜀= (22)
𝑉𝑔 +𝑉
51
888 The expression that relates the gas hold-up and the gas flow is illustrated below which is characterized
𝑃𝑔 0.97
890 𝜀 = 3.32 × 10−4 ( ) (23)
𝑉
𝑉
891 𝑃𝑔 = 𝜌𝐿 𝐹𝑔 √ (24)
𝐿
892 𝜌𝐿 is the liquid density. To evaluate the mass transfer coefficient, the Hunghmark equation for
of
893 individual bubbles is used for the microalgae production using bubbled photobioreactor and the
ro
894 results are quite accurate when the bubble diameter is more than 2.5mm [171].
-p
re
0.0546 0.116
𝐷𝐶𝑂2 𝜇𝐿 𝑑𝐵 𝑔0.33
895 𝐾𝐿 𝑎 = 28.38 [2 + 0.061(𝑅𝑒𝐵 )0.779 ( ) ( ) ] (25)
𝑑𝐵 𝜌𝐿 𝐷𝐶𝑂2 𝐷𝐶𝑂2 0.66
lP
na
𝑑𝐵 𝑉𝐿 𝜌𝐿
896 𝑅𝑒𝐵 = (26)
𝜇𝐿
ur
897 where, 𝐷𝐶𝑂2 - Diffusivity of Carbon dioxide, 𝑅𝑒𝐵 - Reynolds Number, 𝜇𝐿 - Viscosity of liquid
Jo
898 media, 𝑑𝐵 - Bubble diameter, g- gravity, 𝐾𝐿 - Mass transfer coefficient and 𝑉𝐿 - Velocity of the
899 liquid. The dependence of the bubble diameter is on the area between the phases, whereas the
900 dependence of the mass transfer coefficient shows the opposite trend. The bubble size, the pressure
901 of carbon dioxide, and the gas flow rate need to be considered based on the specific culture.
902 A vertical photobioreactor with good control over the concentration of CO2 was used to investigate
903 the effects of various CO2 concentrations in CO2 bioconversion by the cultivation of microalga
904 Chlorella vulgaris [73]. The vertical PBR having a height of 1 m and 0.105 m in diameter, mixed the
905 filtered air with pure CO2 to control the concentration of CO2 from 2% to 10% to provide the desired
52
906 concentration of CO2. The high efficiency of Vertical PBR of CO2 with additional controlled CO2
907 concentration is a better way to control biomass production. Gas mixture bubbling by spargers from
908 the bottom facilitates the mass transfer of CO2 from gas to liquid [73,74]. Gas holdups increases as
909 the superficial velocity of gas increases or that of liquid decreases [170]. Another way of increasing
910 mass transfer is optimizing the gas distributor. For example, recently, Y. Huang et al. (2017) modified
911 the gas distributor and aeration parameters based on bubble-rising behavior to increase microalgae
912 growth. For Chlorella pyrenoidosa, an improved round gas distributor with holes with an inner
of
913 diameter of 0.5 mm and spacing of 1.5 mm results in a maximum bio-mass concentration of 83.44
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914 percent greater compared to the commercial micro bubbles aerator.
-p
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915 6. Recent Development, Future Aspects, Opportunities, and Challenges
lP
917 Integrated processes for algae production with other processes may have many advantages and can
ur
918 be beneficial for both. For example, Romagnoli and Ievina, (2020) designed a Novel Stacked
Jo
919 Modular Open Raceway Ponds (SMORP) in a corporation with a biogas plant, and a model was built
920 with the help of Beer’s Lamberts law to predict the potential microalgae strains suitable for open
921 raceway ponds. This type of concept resolves the issue of the cost of bioreactor and waste
922 management of biogas plants simultaneously. Literature favors the use of Chlorella vulgris in this
923 case but uses the kinetic model, and intensive studies should be carried out to validate the model
925 As nitrogen is to be eliminated primarily, a mixed population of Scenedesmus and Chlorella sp. has
926 a high potential. This idea has been implemented in another study of a bubble column reactor used
53
927 for microalgae biomass production to use in agriculture with the integration of WWTP as a sidestream
928 process to treat wastewater. This research focuses on integrating a microalgal culturing unit within
929 the conventional scheme of a medium-large wastewater treatment plant [173]. This work gives the
930 advantage to WWT and fertilizer production for agriculture simultaneously, which can reduce the
931 cost and make some money from fertilizer. Domestic, piggery, and slaughterhouse wastewaters, as
of
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934 The scale-up procedure of the photobioreactor is the most challenging part of implementing biomass
935
-p
production technology on an industrial scale. Scaling up depends mainly on the type of the reactor
re
936 and its geometry. The mode of operation also affects the scaling up. The difficulty of optimizing the
lP
937 process of creating a sufficient number of inoculums for big-volume open ponds or photobioreactors
na
938 is one of the main difficulties that need to be solved. Table 4 includes several photobioreactors with
939 scale-up conditions, species names, and production rates. Borowiak et al., (2020) developed an
ur
940 automated station for preparing microalgae inoculation material for inoculating six 90 dm3
Jo
941 photobioreactors [174]. They employed eight 12 dm3 airlift photobioreactors, each with its
942 temperature and pH monitoring system, mixing system, and LED illumination. This approach can
943 enhance the last stage of inoculation, and biomanipulation of critical process parameters, which may
945 Biomass growth and secondary metabolite accumulation in microalgae production depend on various
946 process parameters, such as the time profile of light intensity, culture agitation time profile, aeration
947 rate, nitrogen and carbon dioxide availability, and temperature. To achieve optimal results, these
948 parameters and the culture's physiological condition need to be adjusted over time [175]. Diaz et al.
54
949 (2021a) provide guidelines for optimal design of tubular photobioreactors, which include vertical
950 orientation, reduced mixing time, and turbulent mixing, uniform culture illumination, low dark-to-
951 illuminated culture volume ratio, low O2 partial pressure, and a high illuminated surface-to-volume
952 ratio (St/V) [176]. Using these principles, they scaled up a 1250 L Fibonacci-type photobioreactor
953 that can utilize more solar energy. Maintaining geometrical, kinetic, and dynamic similitude and
954 similar L/D cycles and light intensity is crucial for large-scale industrial applications [177]. The mean
955 integral photon flux density can be employed to convey light-dependent growth kinetics in different
of
956 photobioreactor designs [178]. For instance, comparable growth rates can be achieved when scaling
ro
957 up from flat-plate gas-lift photobioreactors (0.09 m2) to thin-layer cascade photobioreactors (8 m2)
958 [179].
-p
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959 Modeling and optimization can be valuable tools for scaling up and predicting reactor behaviors in
lP
960 alternative situations, reducing the need for extensive laboratory trials and saving on labor and
na
961 resources. Response surface methodology (RSM) has emerged as a promising approach in this regard,
ur
962 exploring relationships between explanatory variables and one or more response variables. RSM is
Jo
963 typically categorized into two types: Central Composite Design (CCD) and Box Behnken Design
964 (BBD), both of which have been extensively discussed in the literature [180–184]. As shown in Fig.
965 8a. below, CCD estimates second-order polynomial equations on a wider range of design space,
966 processing input data to identify interactions between response and process variables. BBD, on the
967 other hand, is a spherical, rotatable, or nearly rotatable second-order design represented as a three-
968 level incomplete factorial design with the center point and middle points along the edges of a cube
969 (Fig. 8b.). It is a more cost-effective and practical tool, requiring fewer experimental runs to generate
55
971 Modeling and optimization have many advantages, like scaleup and predicting behaviors of reactors
972 in alternative situations. Our research group recently reported several articles on modeling and
973 optimization-related microalgae research using both CCD and BBD. The effects of different CO2
974 concentrations on CO2 bioconversion by the culture of microalga Chlorella vulgaris are examined in
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56
976
977 Table 4: Detailed scale up condition, species name, production rate from different literature
production
Species Reactor Culture condition Scale up condition Comments Reference
rate
T range 23-25 0C
Solar radiation: 1752
This inoculated
f
𝜇E/m2s
oo
Airlift Bold’s Basal Medium materials was
Eight glass air-lift
Haematococcus photobiorea (BBM) used for six 90
bioreactors [174]
r
pluvialis ctor made pH= 7.00 dm3
-p
12 dm3 each
with glass 8 days photobioreactor
Tube surface exposed to
.
re
LED light
1:10 times scaling, 4 times
lP
No cooling was
required.
na
Maximum CO2
Initial cell density: 0.3 T range: -5-40 ℃ Biomass
utilization.
g/L Solar radiation: 1752 conc =0.96
ur
avoid excessive
Nitrogen was supplied 𝜇E/m2s g/L
Tubular dissolved O2
Jo
for microalgal growth Reactor surface/ volume Biomass
(Fibonacci- accumulation.
(S/V): 50 /m productivity
type) capture 1.6
Dunaliella salin KSP (potassium nitrate Tube surface exposed to = 0.12 g/L. [176]
times more
+ super phosphate) gave light/volume: 77 /m day
photobiorea solar radiation
the maximum conc. Of Volume= 1250 L (max) Maximum
ctor compared to
biomass spiral surface was specific
horizontal
among the four sets of developed to decrease the growth rate
surface
batch reactor photon flow. = 0.17 /day
can be scaled
up easily
57
As light-
Flat-plate
dependent
gas-lift
Nannochloropsis growth kinetics
photobioreact Thin-layer cascade T range: 25-40 ℃
salina & mean integral
ors photobioreactors Solar radiation: 1260 𝜇E/m2s [179]
Nannochloropsis photon flux
(8 m2) Reactor volume: 8 m2
gaditana density is used
photobioreact
for scaling up.
or
CO2 was injected
in an automated
A cone manner to
f
bottom and maintain the pH
oo
polyethylene as given in the
T= 29.5 ± 2.38 °C
tank was condition.
r
pH was 7.56 ± 0.87
developed Microalgae inoculum was When the
-p
Optimal harvest time was
Tetraselmis chuii with cultured in Yield 1700 L number of the [29]
after 300 h
internally a 20L bubble column lamps were
re
1200 cells/𝜇l/ m2 illuminated
attached and decreased, the
surface area
lP
submersed production rate
fluorescent and biomass
light concentration
na
was decreased as
well.
ur
Total inner dimension Biomass 16.4
Jo
Blue Green -11 broth 100×100×5 cm3 mg/L.day
Operations were
Pilot scale medium was used for Bioreactor controller unit was proteins 10.5
performed in
flat microalgal culture. attached to mg/L.day
Chlorella three different
photobioreact T=28 C control the air supply, pH, carbohydrate [156]
thermophila lighting patterns
or pH=7.4 temperature, dissolved 4.03 mg/L.day
to get
(50 L) filtered air supply rate =35 oxygen. chlorophylls
the effect of light
ml/min Fixed 4500 lux intensity with 0.76 mg/L.day
light /dark ratio = 14:10 carotenoids 0.6
mg/L.day
Inocula were prepared in a Three identical raceway 25.1.g/ m2.day Experiments
Pilot-scale 5L reactors were used to maximum were run
Scenedesmus sp. raceway photobioreactor. under the same nitrogen throughout the
[185]
photobioreact Commercial solid mixture environmental condition. removal rate whole
ors of Operating volume= 11.8 4286.6 year emphasizing
micronutrients were used m3(each reactor) mg/⋅m2⋅day1( the effect of four
58
surface area=80 m2 during seasons.
culture depth =0.135 m summer) Four dilution rate
0.1, 0.2, 0.3 day-
1 were
observed
Three parts:
a tubular PBR, O2 stripping Biomass
Waste water
Algae cell was cultivated system production of
came from food
in 250 mL and dynamic system 1.83-2.10 g/L
Pilot scale processing
conical flasks. length of each tube 2.5 m specific
Chlorella tubular plant was used
It was placed in a light total 56 tubes growth rate of [186]
pyrenoidosa photobioreact for algae
f
incubator and External Tube diameter 94 0.73-1.59 /day
oo
or cultivation
light intensity = mm Lipids content:
waste water was
127𝜇mol/m2.s Internal Tube diameter 90 8.1-15.3% of
r
processed
mm dried weight
-p
re
978
lP
na
ur
Jo
59
of
ro
979
-p
re
980 Fig. 8. The structural difference between CCD (a) and BBD (b) for optimizing three independent
981 variables. Here, factorial/axial points are symbolized as ( ● ), and central points are represented as
( ○ ).
lP
982
na
983 The main response parameters that were calculated as specific growth rate µ (d-1), biomass
984 productivity, P (gL-1d-1), and CO2 biofixation or uptake rate, RCO2 (gL-1d-1), and the reported models
ur
990 RCO2 = 0.1367 – 0.0029x1 + 0.0091x2 + 0.0368x3 - 0.0871x12 -0.0270x22 - 0.0163x32 - 0.0100x1x2 –
60
992 where, x1 , x2 and x3 are the coded values of the temperature, NP ratio, and LD cycle. When
993 comparing the model with experimental data, it gave less than 6% error at an optimized condition
994 where the highest SGR, CO2 biofixation rate, and biomass productivity were determined to be 2.23
995 d–1, 0.065 gL-1d-1, and 0.092 gL-1d-1 at an optimal setting of 3 percent CO2 with 7 days of culture,
996 respectively. Further improvement was made by Kazeem et al. also used CCD to develop a quadratic
997 model for C. vulgaris where the effects of CO2 concentration, NP ratio, and culture temperature were
998 used to find SGR, BP, and CO2 uptake rate. The predicted value matched well with the experimental
of
999 value, while all the optimal sets gave errors of less than 15.6%. S. M. Zakir Hossain et al., (2018)
ro
1000 used BBD approach to model and calculated the effect of temperature, NP ratio, and LD cycle on
1001
-p
SGR, BP, and CO2 uptake rate for C. vulgaris. The optimal set was 30ºC, 3:1 NP ratio, and 16:8 L/D
re
1002 ratio. The maximum SGR, BP, and CO2 biofixation rate for this set are calculated to be 0.66 d-1, 147.6
lP
1003 mgL-1d-1, and 141.7 mgL-1d-1, respectively, which is a good match with the experimental data.
na
1004 Chen et al., (2016) developed a model of CO2 mass transfer for flat-plate airlift photobioreactor and
ur
1005 validated it with experimental data. After investigating four structural parameters of baffle by
Jo
1006 numerical approach, the authors concluded mass transfer in flat-airlift photobioreactor mainly
1007 depends on the downcomer to riser cross-sectional area ratio. The impact of wave number and
1008 amplitude is negligible, while baffle number has an irregular pattern of effects. The key equations for
𝑑𝐶𝑇
1010 = 𝐾𝐿 𝑎(𝐶𝑇∗ − 𝐶𝑇 ) (30)
𝑑𝑡
𝐷𝐿 𝜌𝐿 𝜀 0.25
1011 𝐾𝐿 = 2√ ( ) (31)
𝜋 𝜇𝐿
61
6𝜀𝑔
1012 𝑎= (32)
𝑑𝐵 (1−𝜀𝑔 )
1013 where units of the parameters are as conventional as inorganic carbon concentration, 𝐶𝑇 (mol/m3),
1014 overall mass transfer, 𝐾𝐿 (m/s), specific interfacial area per volume, 𝑎 (m2/m3).
1015 In the context of scaling up and understanding the effect of various vital factors on PBRs, CFD
1016 modeling can be a very useful tool. Like gas-liquid mass transfer, an airlift PBR emphasizes two
important parameters, i.e., CO2 mass transfer and 𝐾𝐿 𝑎). Ndiaye et al. (2018) constructed a CFD
of
1017
ro
1018 model considering the cultivation of C. vulgaris. It is reasonably satisfactory to find 𝐾𝐿 𝑎 from O2
1019
-p
gas in-out but in case of CO2 transfer it needs to give more attention as CO2 is soluble in water, and
re
1020 as it rises, the mass transfer becomes more complicated. The value of 𝐾𝐿 𝑎 may not be so unpromising
lP
1021 for small scale or O2 transfer but for large scale CO2 transfer estimation certainly requires more
na
1023 An alternative approach for CO2 mass transfer is to study the pH behavior depending on that modeling
Jo
1024 and scaling up. Using the measurement of pH profiles, a CO2 mass transfer model was built and tested
1025 in connected cultivation systems by [189] along with some kinetics. The simulation allowed
1026 researchers to learn more about CO2 mass transfer, including inorganic carbon concentration
1027 fluctuations in culture medium, 𝐾𝐿 𝑎 , and other microalgal biofilm kinetics characteristics. Higher
1028 aerated gas CO2 concentration led to decreased 𝐾𝐿 𝑎 , and the aeration rate and medium circulation
1029 rate had a somewhat favorable effect on CO2 mass transfer in the linked cultivation system.
1030 Field synergy theory can be applied to design Tubular microalgae PBRs. A model developed by Cui
1031 et al. concluded that the light/dark cycle frequency and the light-time ratio of the tangent double-tube
62
1032 photobioreactor rose by 78.2 percent and 36.2 percent, respectively, as compared to the concentric
1033 double-tube photobioreactor, reaching 1.8 Hz and 47.8 percent. The most conducive to improving the
1034 mixing performance of the innovative PBR was a downwards aeration direction of 30°, aeration rate
1035 of 0.7 vvm, and the average turbulent kinetic energy (TKE) increased by 48.1 percent, from 54 to
1036 80cm2s2 [122]. Another research investigated the hydrodynamics of a hybrid horizontal tubular
1037 photobioreactor intended for microalgae production and wastewater treatment using CFD [190].
1038 Some factors were evaluated for relationships by Zavřel et al., (2021)with growth rate or productivity
of
1039 in Synechocystis sp. Photosynthesis, respiration rates, and ratios had the strongest connections,
ro
1040 whereas additional fitness proxies included qE and Zn content in the culture medium [191]. Many
1041
-p
other modelings have been done in recent years. The main challenges are maintaining similitude and
re
1042 understanding the most dominating parameter in a particular algae photobioreactor system. The
lP
1043 optimization of models is very necessary. Implementation of machine learning is another option.
na
1044 Another challenge of modeling is the computational limitation or complexity and cost along with a
ur
1045 good understanding of the process. In the near future, the existing technique would surely offer
Jo
1046 cutting-edge possibilities for algae cultivation in a low-cost medium for maximal biomass output and
1047 a sustainable economy. To determine feasibility, a techno-economic evaluation of energy, water use,
1050 It can be argued that it can meet the needs of the present without comprising the future, especially
1051 considering the inputs during its cultivation process. These inputs are sewage water and carbon
1052 dioxide, whose reuse is extremely important especially owing to the issues of climate change and
1053 waste disposal during this day and age. Millions of carbon dioxide are emitted into the environment
63
1054 while a large amount of money is spent on sewage water treatment. Hence, using microalgae biomass
1055 as a feedstock will solve both these problems while producing green energy to replace fossil fuels.
1056 Secondly, the sustainability of microalgae biomass has been highly appreciated, especially recently,
1057 considering the high yield of proteins and fats from these microorganisms [192]. It is argued that
1058 these yields are both cost-effective and meet the world's energy demands, especially to curb and
1060 However, it can be argued that microalgae biomass is not currently a sustainable feedstock
of
1061 considering the high costs involved in its production due to the lack of quality information concerning
ro
1062 the process of producing it. Furthermore, the inputs, despite being carbon dioxide and sewage water,
1063
-p
also increase their cost. This is because the carbon dioxide must be piped into the algal from nearby
re
1064 factories while the sewage water must be transported. Thereby further increasing both the
lP
1065 complication and the cost of the process. To increase the productivity of microalgae biomass to be
na
1066 used in producing renewable energy, treating wastewater, and mitigating carbon from the atmosphere,
ur
1067 a lot of challenges can be faced for the enhancement of the microorganisms, the enhancement of the
Jo
1068 system designing, and the scaling up process [194]. Stimulation means can aid in predicting the
1069 quantitative performance measure of the bioreactor and hence aid in improving its design and
1070 enhancing the scale-up. Being dependent on light, temperature, nutrients, and strains makes the
1071 chemical reactors better than the photoreactors in stimulation. The opportunity to find a bioreactor
1072 that is good for design and scale-up is very low [1].
1073 Many challenges still exist in the path to full-scale production of biofuels with the help of microalgae
1074 biomass. Firstly, the experiments carried out on photobioreactors are still preliminary. Microalgae
1075 biomass is a recent technology, unlike crops that are also used to produce biofuels. Few studies exist
1076 regarding microalgae biomass growth compared to crops that centuries of knowledge support.
64
1077 Secondly, microalgae biomass is produced commercially as a biofuel only in open systems due to
1078 less energy consumption. However, the cost-effectiveness of these systems is low, considering that it
1079 is still a huge challenge to control environmental factors such as temperature, pH, and so on. Thirdly,
1080 many parasites are also growing in mass cultures; it will initially be a challenge to these parasites.
1081 Furthermore, it is also generally difficult to eliminate parasites; therefore, at least a balance should
1082 be found between the loss due to the parasite and the output from the microalgae biomass [195].
1083 Fourthly, the energy consumption in closed systems is very high; this high level of energy
of
1084 consumption hinders the commercial production of biofuel from microalgae biomass due to a lack of
ro
1085 profitability. Furthermore, several other factors also negatively impact the profitability of the process
1086
-p
[196]. Hence, the fifth challenge is cost-effectiveness. Achieving cost-effectiveness at this early stage
re
1087 will be almost impossible especially due to the lack of knowledge. It will therefore take a few years
lP
1088 to achieve cost-effectiveness and ensure profitability. Furthermore, the sixth challenge is reaching
na
1089 the price level of fossil fuels to become a strong competitor and eventually replace it as the main
1091 The acceptable price of biomass should be equal to or lesser than the diesel price per barrel. However,
1092 reaching profitability and matching the diesel price will also not solve all the challenges. This is
1093 because another challenge for the use of biofuel is that most of the cars or means of transportation
1094 are not currently compatible with this source of energy. Therefore, there is a long list of challenges
1095 that are a hindrance to not only the production of biofuels from microalgae but also its use as the
1096 main energy source. Nonetheless, these challenges must be overcome especially considering the
1097 benefits of using microalgae biomass as the main source of energy that would replace fossil fuels
1098 [198]. Furthermore, the challenges are only one side of the coin, as there are several opportunities for
1099 both the use and the production of microalgae biomass. These are discussed in the next subsection.
65
1100 Ocean has a huge potential to produce microalgae with the reduction in cost as it has a large cultivable
1101 area and mixing energy from waves. In this regard, Kim et al., (2016)made progress by developing a
1102 prototype floating PBR for microalgae growing in the ocean. He also suggested that installing a
1103 partition is beneficiary as it increases mass transfer and mixing property to yield higher biomass
1104 production. Further scale-up with modified partition is in progress [130]. The research and
1105 deployment of sustainable radiation sources of light are still required for microalgae scale-up
1106 production [1]. Continuous analysis and optimization of the culture cycle in terms of microalgae
of
1107 growth rate and biomolecule production rate are required for efficient scaling up from the laboratory
ro
1108 to pilot size and, eventually, to industrial-scale photo-bioreactor units from the aspect of performing
1109
-p
culture and from the standpoint of station ergonomics.
re
1110 Microalgae biomass production is one of the widely studied topics, yet many areas need improvement
lP
1111 and development for global needs. Solar Photobioreactor with greenhouse construction is being
na
1112 investigated, but the problem in this design is to handle the climatic changes and availability of
ur
1113 sunlight throughout the year. Integration of various processes, such as bioremediation, wastewater
Jo
1114 treatment, and bioenergy production, can be considered for future research. The shape of the
1115 photobioreactor can be studied further, as space limitation is one of the challenges. Artificial
1116 intelligence (AI) can be applied to develop numerous techniques for tracking algal density and cell
1117 growth. In this regard, it is necessary to include all the growth parameters, such as pH, light intensity,
1118 dissolved oxygen, carbon, and temperature. AI technique shall help in developing optimal cultivation
1120 The challenges outlined in the passage can be met with the following solutions:
66
1121 1. Efficient Resource Utilization: To address resource cost challenges, it is essential to
1122 optimize resource usage during microalgae cultivation. This entails enhancing the efficiency
1123 of carbon dioxide capture and delivery systems and streamlining the transportation and
1124 treatment of sewage water. Implementing closed-loop resource recycling systems can
1127 requires a multi-faceted approach. Research should prioritize the development of enhanced
of
1128 microorganism strains and improved cultivation systems to maximize biomass yields.
ro
1129 Exploring the use of chemical reactors, which are less reliant on external factors like light and
1130
-p
temperature, alongside photoreactors can enhance overall efficiency.
re
1131 3. Scaling Up with Precision: Overcoming the complexities of scaling up microalgae biomass
lP
1133 experimentation and refinement of photobioreactor design, including factors such as mass
1134 transfer, pH regulation, and hydrodynamics, are critical for successful upscaling from
ur
1137 particularly in open systems, necessitates innovative solutions. Research should focus on
1138 advanced automation and monitoring systems to maintain optimal growth conditions for
1139 microalgae. Balancing parasite control with biomass output is a key consideration.
1140 5. Energy Efficiency: Reducing energy consumption in closed systems can be achieved through
1142 photobioreactor designs and the incorporation of renewable energy sources, such as solar
67
1144 6. Cost Optimization: While achieving cost-effectiveness may take time, it can be expedited
1146 and technological advancements can enhance the economic viability of microalgae-based
1148 7. Competing in the Market: To compete with conventional fossil fuels, microalgae-based
1149 biofuels should aim for cost parity or superiority. Continued research and development efforts
1150 should concentrate on cost reduction in production while improving the efficiency of
of
1151 microalgae-based biofuel processes.
ro
1152 8. Infrastructure Adaptation: Adapting existing infrastructure for biofuel use should be
1153
-p
aligned with biofuel production efforts. Research and development can explore strategies to
re
1154 make vehicles and transportation systems more compatible with microalgae-derived biofuels.
lP
1155 9. Ocean Cultivation Potential: Exploring ocean-based microalgae cultivation can expand
na
1156 capacity and reduce costs. Research into sustainable ocean-based photobioreactor systems,
1158 10. Leveraging Advanced Technologies: Integrating advanced technologies, such as artificial
Jo
1159 intelligence (AI), can optimize microalgae cultivation. AI can enhance monitoring and control
1160 of growth parameters, thereby improving overall cultivation efficiency while minimizing
1163 bioremediation, wastewater treatment, and bioenergy production can lead to comprehensive
1164 and efficient solutions. Collaborative efforts across various fields can address multiple
68
1166 12. Innovative Photobioreactor Design: Further research into photobioreactor shape and design
1167 can overcome space limitations and enhance efficiency. Exploring innovative designs that
1170 research, and innovation. Systematically tackling these issues will unlock the full potential of
1171 microalgae biomass production for sustainable energy, environmental remediation, and biofuel
1172 applications.
of
ro
1173
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re
1174 7. Conclusions
lP
1175 In conclusion, the cultivation of microalgae in photobioreactors holds great promise for the future of
na
1176 sustainable industrial-scale production. Understanding the various physical and biological parameters
1177 that influence microalgae growth and biomass yield is crucial in the design and operation of
ur
1178 photobioreactors. This review has provided a comprehensive overview of the different types of
Jo
1179 photobioreactors and the important parameters to consider in scaling up from laboratory to industrial-
1180 scale production. By optimizing the various operating parameters and controlling the growth
1181 conditions, microalgae can be grown efficiently in large-scale photobioreactors for various
1182 applications such as biofuel production, wastewater treatment, and food supplements. With further
1183 research and development, photobioreactor technology will continue to advance, making it an even
1185 Scaling up photobioreactors for industrial production requires careful consideration of several
1186 important parameters. Light intensity and regime, hydrodynamics, mass transfer of CO2, temperature,
69
1187 pH, and nutrient concentration (e.g., nitrogen and phosphorus) all play a critical role in designing
1188 large-scale photobioreactors. To optimize performance and control criteria, multiple operating
1189 parameters such as light period, light/dark cycle, light intensity, color, and variation must be carefully
1190 considered. The supply of CO2 concentration in the gas phase is also crucial for increasing mass
1191 transfer, and various mechanical methods can be used to optimize gas distribution and separation.
1192 Proper maintenance of nutrient ratios is important as well, as starving algae of nitrogen and
1193 phosphorus at high temperatures can lead to high lipid formation, which may be desirable for some
of
1194 industrial applications. Recent advances in photobioreactor design have helped to overcome some of
ro
1195 the challenges associated with scaling up, and continued research and development in this area will
1196
-p
be important for meeting the growing demand for sustainable industrial production.
re
lP
1197 Acknowledgements
na
1198 Authors would like to acknowledge the support received from Interdisciplinary Research Centre for Refining
ur
1199 and Advanced Chemicals, King Fahd University of Petroleum & Minerals, Dhahran, Saudi Arabia with
Jo
1200 funding grant and financial support for this work through project No. INRC2318.
1201 Nomenclature
70
1211 𝑀𝑐 Atomic weight of carbon
1212 d day
1213 𝐷𝐶𝑂2 Diffusivity of Carbon dioxide
1217 g gravity
of
1219 𝑉𝐿 Velocity of the liquid
ro
1220 𝜇𝑚𝑎𝑥 Maximum Specific growth rate
𝐼𝑎𝑣
-p
1221 Intensity of Light
1226
Jo
1227
71
1228 References
1229 [1] S.A. Razzak, S.A.M. Ali, M.M. Hossain, H. deLasa, Biological CO2 fixation with
1230 production of microalgae in wastewater – A review, Renew. Sustain. Energy Rev. 76 (2017)
1231 379–390. https://doi.org/10.1016/j.rser.2017.02.038.
1232 [2] S.M. Rahman, F.S. Al-Ismail, M.E. Haque, M. Shafiullah, M.R. Islam, M.T. Chowdhury,
1233 M.S. Alam, S.A. Razzak, A. Ali, Z.A. Khan, Electricity generation in Saudi Arabia: Tracing
1234 opportunities and challenges to reducing greenhouse gas emissions, IEEE Access. (2021).
1235 https://doi.org/10.1109/ACCESS.2021.3105378.
1236 [3] A.N. Khondaker, S.M. Rahman, K. Malik, N. Hossain, S. Abdur Razzak, R.A. Khan,
1237 Dynamics of energy sector and GHG emissions in Saudi Arabia, Clim. Policy. 15 (2015)
of
1238 517–541. https://doi.org/10.1080/14693062.2014.937387.
ro
1239 [4] S.M.Z. Hossain, M.M. Hossain, S.A. Razzak, Optimization of CO2 Biofixation by Chlorella
1240 vulgaris Using a Tubular Photobioreactor, Chem. Eng. Technol. 41 (2018) 1313–1323.
-p
1241 https://doi.org/10.1002/ceat.201700210.
re
1242 [5] V.C. Eze, S.B. Velasquez-Orta, A. Hernández-García, I. Monje-Ramírez, M.T. Orta-
1243 Ledesma, Kinetic modelling of microalgae cultivation for wastewater treatment and carbon
lP
1246 [6] M. Li, G. Nakhla, J. Zhu, Simultaneous carbon and nitrogen removal with enhanced
1247 bioparticle circulation in a Circulating Fluidized Bed Biofilm Reactor, Chem. Eng. J. 181–
1248 182 (2012) 35–44. https://doi.org/10.1016/j.cej.2011.12.073.
ur
1249 [7] P.D. Álvarez-Díaz, J. Ruiz, Z. Arbib, J. Barragán, M.C. Garrido-Pérez, J.A. Perales,
Jo
1250 Freshwater microalgae selection for simultaneous wastewater nutrient removal and lipid
1251 production, Algal Res. 24 (2017) 477–485. https://doi.org/10.1016/j.algal.2017.02.006.
1252 [8] T.M. Mata, A. a. Martins, N.S. Caetano, Microalgae for biodiesel production and other
1253 applications: A review, Renew. Sustain. Energy Rev. 14 (2010) 217–232.
1254 https://doi.org/10.1016/j.rser.2009.07.020.
1255 [9] S.F. Mohsenpour, N. Willoughby, Luminescent photobioreactor design for improved algal
1256 growth and photosynthetic pigment production through spectral conversion of light.,
1257 Bioresour. Technol. 142 (2013) 147–53. https://doi.org/10.1016/j.biortech.2013.05.024.
1258 [10] G. Huang, F. Chen, D. Wei, X. Zhang, G. Chen, Biodiesel production by microalgal
1259 biotechnology, Appl. Energy. 87 (2010) 38–46.
1260 https://doi.org/10.1016/j.apenergy.2009.06.016.
1261 [11] S.A. Razzak, Biomass and Lipid Productivity of Neochloris oleoabundans for CO 2
1262 Biofixation and Biodiesel Application, Chem. Eng. Technol. 41 (2018) 2177–2185.
1263 https://doi.org/10.1002/ceat.201800330.
72
1264 [12] S.A. Razzak, In situ biological CO2 fixation and wastewater nutrient removal with
1265 Neochloris oleoabundans in batch photobioreactor, Bioprocess Biosyst. Eng. 42 (2019) 93–
1266 105. https://doi.org/10.1007/s00449-018-2017-x.
1267 [13] S.F. Mohsenpour, S. Hennige, N. Willoughby, A. Adeloye, T. Gutierrez, Integrating micro-
1268 algae into wastewater treatment: A review, Sci. Total Environ. 752 (2021) 142168.
1269 https://doi.org/10.1016/j.scitotenv.2020.142168.
1270 [14] X. Lu, Y. Cui, Y. Chen, Y. Xiao, X. Song, F. Gao, Y. Xiang, C. Hou, J. Wang, Q. Gan, X.
1271 Zheng, Y. Lu, Sustainable development of microalgal biotechnology in coastal zone for
1272 aquaculture and food, Sci. Total Environ. 780 (2021).
1273 https://doi.org/10.1016/j.scitotenv.2021.146369.
1274 [15] T.T. Nguyen, X.T. Bui, H.H. Ngo, T.T.D. Nguyen, K.Q. Nguyen, H.H. Nguyen, K.P.H.
1275 Huynh, J. Némery, T. Fujioka, C.H. Duong, B.T. Dang, S. Varjani, Nutrient recovery and
of
1276 microalgae biomass production from urine by membrane photobioreactor at low biomass
ro
1277 retention times, Sci. Total Environ. 785 (2021).
1278 https://doi.org/10.1016/j.scitotenv.2021.147423.
1279
1280 -p
[16] B.R. Kumar, T. Mathimani, M.P. Sudhakar, K. Rajendran, A.S. Nizami, K. Brindhadevi, A.
Pugazhendhi, A state of the art review on the cultivation of algae for energy and other
re
1281 valuable products: Application, challenges, and opportunities, Renew. Sustain. Energy Rev.
1282 138 (2021). https://doi.org/10.1016/j.rser.2020.110649.
lP
1283 [17] S.A. Razzak, In situ biological CO 2 fixation and wastewater nutrient removal with
1284 Neochloris oleoabundans in batch photobioreactor, Bioprocess Biosyst. Eng. 42 (2019) 93–
na
1286 [18] S.A. Razzak, M.M. Hossain, R.A. Lucky, A.S. Bassi, H. De Lasa, Integrated CO2 capture,
1287 wastewater treatment and biofuel production by microalgae culturing - A review, Renew.
Jo
73
1303 [23] A. Altriki, I. Ali, S.A. Razzak, I. Ahmad, W. Farooq, Assessment of CO2 biofixation and
1304 bioenergy potential of microalga Gonium pectorale through its biomass pyrolysis, and
1305 elucidation of pyrolysis reaction via kinetics modeling and artificial neural network, Front.
1306 Bioeng. Biotechnol. 10 (2022). https://doi.org/10.3389/fbioe.2022.925391.
1307 [24] H. Razzak, Shaikh A. Lucky, Rahima A. Hossain, Mohammad M. deLasa, Valorization of
1308 Microalgae Biomass to Biofuel Production: A review, Energy Nexus. (2022).
1309 [25] M.A. Kazeem, S.M.Z. Hossain, M.M. Hossain, S.A. Razzak, Application of Central
1310 Composite Design to Optimize Culture Conditions of Chlorella vulgaris in a Batch
1311 Photobioreactor: An Efficient Modeling Approach, Chem. Prod. Process Model. (2018).
1312 https://doi.org/10.1515/cppm-2017-0082.
1313 [26] C.Y. Chen, K.L. Yeh, R. Aisyah, D.J. Lee, J.S. Chang, Cultivation, photobioreactor design
1314 and harvesting of microalgae for biodiesel production: A critical review, Bioresour. Technol.
of
1315 102 (2011) 71–81. https://doi.org/10.1016/j.biortech.2010.06.159.
ro
1316 [27] Y. Chisti, Biodiesel from microalgae beats bioethanol., Trends Biotechnol. 26 (2008) 126–
1317 31. https://doi.org/10.1016/j.tibtech.2007.12.002.
1318
-p
[28] J. Lorenzen, N. Igl, M. Tippelt, A. Stege, F. Qoura, U. Sohling, T. Brück, Extraction of
re
1319 microalgae derived lipids with supercritical carbon dioxide in an industrial relevant pilot
1320 plant, Bioprocess Biosyst. Eng. 40 (2017) 911–918. https://doi.org/10.1007/s00449-017-
lP
1321 1755-5.
1322 [29] P. Erbland, S. Caron, M. Peterson, A. Alyokhin, Design and performance of a low-cost,
na
1323 automated, large-scale photobioreactor for microalgae production, Aquac. Eng. 90 (2020).
1324 https://doi.org/10.1016/j.aquaeng.2020.102103.
ur
1325 [30] F. Rezvani, M.H. Sarrafzadeh, S. Ebrahimi, H.M. Oh, Nitrate removal from drinking water
1326 with a focus on biological methods: a review, Environ. Sci. Pollut. Res. 26 (2019) 1124–
Jo
74
1341 M. Mohamad, J.W. Lim, Comparative performances of microalgal-bacterial co-cultivation to
1342 bioremediate synthetic and municipal wastewaters whilst producing biodiesel sustainably,
1343 Processes. 8 (2020) 1–12. https://doi.org/10.3390/pr8111427.
1344 [36] W.H. Leong, J.W. Lim, M.K. Lam, S.M. Lam, J.C. Sin, A. Samson, Novel sequential flow
1345 baffled microalgal-bacterial photobioreactor for enhancing nitrogen assimilation into
1346 microalgal biomass whilst bioremediating nutrient-rich wastewater simultaneously, J.
1347 Hazard. Mater. 409 (2021). https://doi.org/10.1016/j.jhazmat.2020.124455.
1348 [37] P.L. Gorry, L. Sánchez, M. Morales, Microalgae Biorefineries for Energy and Coproduct
1349 Production, Green Energy Technol. (2018) 89–140. https://doi.org/10.1007/978-3-319-
1350 69093-3_5.
1351 [38] M. Nayak, A. Karemore, R. Sen, Performance evaluation of microalgae for concomitant
1352 wastewater bioremediation, CO2 biofixation and lipid biosynthesis for biodiesel application,
of
1353 Algal Res. 16 (2016) 216–223. https://doi.org/10.1016/j.algal.2016.03.020.
ro
1354 [39] N. Tasnim Sahrin, K. Shiong Khoo, J. Wei Lim, R. Shamsuddin, F. Musa Ardo, H.
1355 Rawindran, M. Hassan, W. Kiatkittipong, E. Alaaeldin Abdelfattah, W. Da Oh, C. Kui
1356
1357 -p
Cheng, Current perspectives, future challenges and key technologies of biohydrogen
production for building a carbon–neutral future: A review, Bioresour. Technol. 364 (2022).
re
1358 https://doi.org/10.1016/j.biortech.2022.128088.
lP
1359 [40] B. Zhao, Y. Su, Process effect of microalgal-carbon dioxide fixation and biomass production:
1360 A review, Renew. Sustain. Energy Rev. 31 (2014) 121–132.
1361 https://doi.org/10.1016/j.rser.2013.11.054.
na
1362 [41] J. Legrand, A. Artu, J. Pruvost, A review on photobioreactor design and modelling for
ur
1365 [42] V. Balan, B. Maddi, Microbial Lipid Production Methods and Protocols, Microb. Lipid Prod.
1366 1995 (2019) 91–101. http://www.springer.com/series/7651.
1367 [43] Y. Zhou, L. Liu, M. Li, C. Hu, Algal biomass valorisation to high-value chemicals and
1368 bioproducts: Recent advances, opportunities and challenges, Bioresour. Technol. 344 (2022).
1369 https://doi.org/10.1016/j.biortech.2021.126371.
1370 [44] J. Hur, S. Rezania, B. Oryani, J. Park, B. Hashemi, K.K. Yadav, E.E. Kwon, J. Cho, Review
1371 on transesterification of non-edible sources for biodiesel production with a focus on
1372 economic aspects, fuel properties and by-product applications, Energy Convers. Manag.
1373 (2019).
1374 [45] M. Plaza, A. Cifuentes, E. Ibáñez, In the search of new functional food ingredients from
1375 algae, Trends Food Sci. Technol. 19 (2008) 31–39. https://doi.org/10.1016/j.tifs.2007.07.012.
1376 [46] L. Novoveská, M.E. Ross, M.S. Stanley, R. Pradelles, V. Wasiolek, J.F. Sassi, Microalgal
1377 carotenoids: A review of production, current markets, regulations, and future direction, Mar.
1378 Drugs. 17 (2019). https://doi.org/10.3390/md17110640.
75
1379 [47] H. Nazih, J.M. Bard, Microalgae in human health: Interest as a functional food, Microalgae
1380 Heal. Dis. Prev. (2018) 211–226. https://doi.org/10.1016/B978-0-12-811405-6.00010-4.
1381 [48] M.A. Borowitzka, High-value products from microalgae-their development and
1382 commercialisation, J. Appl. Phycol. 25 (2013) 743–756. https://doi.org/10.1007/s10811-013-
1383 9983-9.
1384 [49] M. Koller, A. Muhr, G. Braunegg, Microalgae as versatile cellular factories for valued
1385 products, Algal Res. 6 (2014) 52–63. https://doi.org/10.1016/j.algal.2014.09.002.
1386 [50] A.J. Meléndez-Martínez, C.M. Stinco, P. Mapelli-Brahm, Skin carotenoids in public health
1387 and nutricosmetics: The emerging roles and applications of the UV radiation-absorbing
1388 colourless carotenoids phytoene and phytofluene, Nutrients. 11 (2019).
1389 https://doi.org/10.3390/nu11051093.
of
1390 [51] I. Barkia, N. Saari, S.R. Manning, Microalgae for high-value products towards human health
1391 and nutrition, Mar. Drugs. 17 (2019). https://doi.org/10.3390/md17050304.
ro
1392 [52] P. Das, W. Lei, S.S. Aziz, J.P. Obbard, Enhanced algae growth in both phototrophic and
-p
1393 mixotrophic culture under blue light, Bioresour. Technol. (2011).
1394 https://doi.org/10.1016/j.biortech.2010.11.102.
re
1395 [53] A.P. Abreu, B. Fernandes, A.A. Vicente, J. Teixeira, G. Dragone, Mixotrophic cultivation of
lP
1396 Chlorella vulgaris using industrial dairy waste as organic carbon source, Bioresour. Technol.
1397 118 (2012) 61–66. https://doi.org/10.1016/j.biortech.2012.05.055.
na
1398 [54] S.M.Z. Hossain, N. Al-Bastaki, A.M.A. Alnoaimi, H. Ezuber, S.A. Razzak, M.M. Hossain,
1399 Mathematical Modeling of Temperature Effect on Algal Growth for Biodiesel Application,
1400 (2020) 517–528. https://doi.org/10.1007/978-3-030-18488-9_41.
ur
1401 [55] D. Tang, W. Han, P. Li, X. Miao, J. Zhong, CO2 biofixation and fatty acid composition of
Jo
1402 Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels,
1403 Bioresour. Technol. 102 (2011) 3071–3076. https://doi.org/10.1016/j.biortech.2010.10.047.
1404 [56] S.F. Mohsenpour, B. Richards, N. Willoughby, Spectral conversion of light for enhanced
1405 microalgae growth rates and photosynthetic pigment production, Bioresour. Technol. (2012).
1406 https://doi.org/10.1016/j.biortech.2012.08.072.
1407 [57] V. Andruleviciute, V. Makareviciene, V. Skorupskaite, M. Gumbyte, Biomass and oil
1408 content of Chlorella sp., Haematococcus sp., Nannochloris sp. and Scenedesmus sp. under
1409 mixotrophic growth conditions in the presence of technical glycerol, J. Appl. Phycol. (2014).
1410 https://doi.org/10.1007/s10811-013-0048-x.
1411 [58] S.P. Singh, P. Singh, Effect of temperature and light on the growth of algae species: A
1412 review, Renew. Sustain. Energy Rev. 50 (2015) 431–444.
1413 https://doi.org/10.1016/j.rser.2015.05.024.
1414 [59] Y. Xu, I.M. Ibrahim, P.J. Harvey, The influence of photoperiod and light intensity on the
1415 growth and photosynthesis of Dunaliella salina (chlorophyta) CCAP 19/30, Plant Physiol.
1416 Biochem. 106 (2016) 305–315. https://doi.org/10.1016/j.plaphy.2016.05.021.
76
1417 [60] O. Tricolici, C. Bumbac, C. Postolache, Microalgae-bacteria system for biological
1418 wastewater treatment, J. Environ. Prot. Ecol. 15 (2014) 268–276.
1419 [61] Q. Huang, F. Jiang, L. Wang, C. Yang, Design of Photobioreactors for Mass Cultivation of
1420 Photosynthetic Organisms, Engineering. 3 (2017) 318–329.
1421 https://doi.org/10.1016/J.ENG.2017.03.020.
1422 [62] H.-W. Kim, S. Park, B.E. Rittmann, Multi-component kinetics for the growth of the
1423 cyanobacterium Synechocystis sp. PCC6803, Environ. Eng. Res. 20 (2015) 347–355.
1424 https://doi.org/10.4491/eer.2015.033.
1425 [63] K. Schediwy, A. Trautmann, C. Steinweg, C. Posten, Microalgal kinetics — a guideline for
1426 photobioreactor design and process development, Eng. Life Sci. 19 (2019) 830–843.
1427 https://doi.org/10.1002/elsc.201900107.
of
1428 [64] Y. Maltsev, K. Maltseva, M. Kulikovskiy, S. Maltseva, Influence of light conditions on
1429 microalgae growth and content of lipids, carotenoids, and fatty acid composition, Biology
ro
1430 (Basel). 10 (2021). https://doi.org/10.3390/biology10101060.
-p
1431 [65] M.N. Metsoviti, G. Papapolymerou, I.T. Karapanagiotidis, N. Katsoulas, Effect of light
1432 intensity and quality on growth rate and composition of Chlorella vulgaris, Plants. 9 (2020).
re
1433 https://doi.org/10.3390/plants9010031.
lP
1434 [66] A. Khalili, G.D. Najafpour, G. Amini, F. Samkhaniyani, Influence of nutrients and LED light
1435 intensities on biomass production of microalgae Chlorella vulgaris, Biotechnol. Bioprocess
1436 Eng. 20 (2015) 284–290. https://doi.org/10.1007/s12257-013-0845-8.
na
1437 [67] X. Wan, X.R. Zhou, G. Moncalian, L. Su, W.C. Chen, H.Z. Zhu, D. Chen, Y.M. Gong, F.H.
1438 Huang, Q.C. Deng, Reprogramming microorganisms for the biosynthesis of astaxanthin via
ur
1441 [68] K.J. Chavan, S. Chouhan, S. Jain, P. Singh, M. Yadav, A. Tiwari, Environmental Factors
1442 Influencing Algal Biodiesel Production, Environ. Eng. Sci. 31 (2014) 602–611.
1443 https://doi.org/10.1089/ees.2014.0219.
1444 [69] O. Bernard, B. Rémond, Validation of a simple model accounting for light and temperature
1445 effect on microalgal growth, Bioresour. Technol. 123 (2012) 520–527.
1446 https://doi.org/10.1016/j.biortech.2012.07.022.
1447 [70] N. Brown, A. Shilton, Luxury uptake of phosphorus by microalgae in waste stabilisation
1448 ponds: Current understanding and future direction, Rev. Environ. Sci. Biotechnol. 13 (2014)
1449 321–328. https://doi.org/10.1007/s11157-014-9337-3.
1450 [71] K. Liang, Q. Zhang, M. Gu, W. Cong, Effect of phosphorus on lipid accumulation in
1451 freshwater microalga Chlorella sp., J. Appl. Phycol. 25 (2013) 311–318.
1452 https://doi.org/10.1007/s10811-012-9865-6.
1453 [72] M.G. de Morais, J.A.V. Costa, Isolation and selection of microalgae from coal fired
1454 thermoelectric power plant for biofixation of carbon dioxide, Energy Convers. Manag. 48
77
1455 (2007) 2169–2173. https://doi.org/10.1016/j.enconman.2006.12.011.
1456 [73] S.M.Z. Hossain, M.M. Hossain, S.A. Razzak, Optimization of CO 2 Biofixation by Chlorella
1457 vulgaris Using a Tubular Photobioreactor, Chem. Eng. Technol. 41 (2018) 1313–1323.
1458 https://doi.org/10.1002/ceat.201700210.
1459 [74] S.A. Razzak, S.A.M. Ali, M.M. Hossain, A.N. Mouanda, Biological CO2 fixation using
1460 Chlorella vulgaris and its thermal characteristics through thermogravimetric analysis,
1461 Bioprocess Biosyst. Eng. 39 (2016) 1651–1658. https://doi.org/10.1007/s00449-016-1640-7.
1462 [75] S.Y. Chiu, C.Y. Kao, M.T. Tsai, S.C. Ong, C.H. Chen, C.S. Lin, Lipid accumulation and
1463 CO2 utilization of Nannochloropsis oculata in response to CO2 aeration, Bioresour. Technol.
1464 100 (2009) 833–838. https://doi.org/10.1016/j.biortech.2008.06.061.
1465 [76] S.A. Razzak, M. Ilyas, S.A.M. Ali, M.M. Hossain, Effects of CO2 Concentration and pH on
of
1466 Mixotrophic Growth of Nannochloropsis oculata, Appl. Biochem. Biotechnol. 176 (2015)
1467 1290–1302. https://doi.org/10.1007/s12010-015-1646-7.
ro
1468 [77] L. Moraes, G.M. Rosa, I.M. Cara, L.O. Santos, M.G. Morais, E.M. Grima, J.A.V. Costa,
-p
1469 F.G.A. Fernández, Bioprocess strategies for enhancing the outdoor production of
1470 Nannochloropsis gaditana: an evaluation of the effects of pH on culture performance in
re
1471 tubular photobioreactors, Bioprocess Biosyst. Eng. 43 (2020) 1823–1832.
1472 https://doi.org/10.1007/S00449-020-02373-X/FIGURES/4.
lP
78
1493 Marzocchella, G. Pinto, A. Pollio, Effects of CO 2 and pH on Stichococcus bacillaris in
1494 Laboratory Scale Photobioreactors, 27 (2012).
1495 [85] D. Ippoliti, C. Gómez, M. del Mar Morales-Amaral, R. Pistocchi, J.M. Fernández-Sevilla,
1496 F.G. Acién, Modeling of photosynthesis and respiration rate for Isochrysis galbana (T-Iso)
1497 and its influence on the production of this strain, Bioresour. Technol. 203 (2016) 71–79.
1498 https://doi.org/10.1016/j.biortech.2015.12.050.
1499 [86] M.K. Ji, R.A.I. Abou-Shanab, S.H. Kim, E.S. Salama, S.H. Lee, A.N. Kabra, Y.S. Lee, S.
1500 Hong, B.H. Jeon, Cultivation of microalgae species in tertiary municipal wastewater
1501 supplemented with CO2 for nutrient removal and biomass production, Ecol. Eng. 58 (2013)
1502 142–148. https://doi.org/10.1016/j.ecoleng.2013.06.020.
1503 [87] L. Xin, H. Hong-ying, G. Ke, Y. Jia, Growth and nutrient removal properties of a freshwater
1504 microalga Scenedesmus sp. LX1 under different kinds of nitrogen sources, Ecol. Eng.
of
1505 (2010). https://doi.org/10.1016/j.ecoleng.2009.11.003.
ro
1506 [88] Y. Gao, J. Feng, J. Lv, Q. Liu, F. Nan, X. Liu, S. Xie, Physiological changes of parachlorella
1507 kessleri ty02 in lipid accumulation under nitrogen stress, Int. J. Environ. Res. Public Health.
1508
-p
16 (2019). https://doi.org/10.3390/ijerph16071188.
re
1509 [89] S.M.Z. Hossain, N. Sultana, M.F. Irfan, S.M. Haque, N. Nasr, S.A. Razzak, Artificial
1510 intelligence-based super learner approach for prediction and optimization of biodiesel
lP
1513 [90] L. Xin, H. Hong-ying, Y. Jia, Lipid accumulation and nutrient removal properties of a newly
1514 isolated freshwater microalga, Scenedesmus sp. LX1, growing in secondary effluent, N.
ur
1517 Hossain, Soft-computing modeling and multiresponse optimization for nutrient removal
1518 process from municipal wastewater using microalgae, J. Water Process Eng. 45 (2022).
1519 https://doi.org/10.1016/j.jwpe.2021.102490.
1520 [92] P.J. McGinn, K.E. Dickinson, S. Bhatti, J.C. Frigon, S.R. Guiot, S.J.B. O’Leary, Integration
1521 of microalgae cultivation with industrial waste remediation for biofuel and bioenergy
1522 production: Opportunities and limitations, Photosynth. Res. 109 (2011) 231–247.
1523 https://doi.org/10.1007/s11120-011-9638-0.
1524 [93] A.M. Silva Benavides, G. Torzillo, J. Kopecký, J. Masojídek, Productivity and biochemical
1525 composition of Phaeodactylum tricornutum (Bacillariophyceae) cultures grown outdoors in
1526 tubular photobioreactors and open ponds, Biomass and Bioenergy. 54 (2013) 115–122.
1527 https://doi.org/10.1016/j.biombioe.2013.03.016.
1528 [94] R. Harun, M. Singh, G.M. Forde, M.K. Danquah, Bioprocess engineering of microalgae to
1529 produce a variety of consumer products, Renew. Sustain. Energy Rev. 14 (2010) 1037–1047.
1530 https://doi.org/10.1016/j.rser.2009.11.004.
79
1531 [95] J. Sen Tan, S. Ying Lee, K. Wayne Chew, M. Kee Lam, J. Wei Lim, S.-H. Ho, P. Loke
1532 Show, A review on microalgae cultivation and harvesting, and their biomass extraction
1533 processing using ionic liquids, Bioengineered. (2020).
1534 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6999644/.
1535 [96] A. Neori, P.S.M. Celis-pl, K. Ranglov, M. Caporgno, G. Torzillo, R. Abdala, G. Cintia, A.
1536 Margarita, S. Benavides, P.J. Ralph, F. Thaís, R. Atzmüller, J. Vega, P. Ch, A new approach
1537 for cultivating the cyanobacterium Nostoc calcicola ( MACC-612 ) to produce biomass and
1538 bioactive compounds using a thin-layer raceway pond o, 59 (2021).
1539 https://doi.org/10.1016/j.algal.2021.102421.
1540 [97] S. Koley, T. Mathimani, S.K. Bagchi, S. Sonkar, N. Mallick, Biomass and Bioenergy
1541 Microalgal biodiesel production at outdoor open and polyhouse raceway pond cultivations :
1542 A case study with Scenedesmus accuminatus using low-cost farm fertilizer medium, Biomass
of
1543 and Bioenergy. 120 (2019) 156–165. https://doi.org/10.1016/j.biombioe.2018.11.002.
ro
1544 [98] L. Xu, P.J. Weathers, X.-R. Xiong, C.-Z. Liu, Microalgal bioreactors: Challenges and
1545 opportunities, Eng. Life Sci. 9 (2009) 178–189. https://doi.org/10.1002/elsc.200800111.
1546
1547 -p
[99] S. Mehariya, R.K. Goswami, P. Verma, R. Lavecchia, A. Zuorro, Integrated approach for
wastewater treatment and biofuel production in microalgae biorefineries, Energies. 14
re
1548 (2021). https://doi.org/10.3390/en14082282.
lP
1549 [100] J. Oleszkiewicz, D.J. Kruk, T. Devlin, M. Lashkarizadeh, Q. Yuan, Options for Improved
1550 Nutrient Removal and Recovery from Municipal Wastewater in the Canadian Context,
1551 Environ. Technol. 20(7) (2015) 681–695. https://doi.org/10.1088/1367-2630/8/12/318.
na
1552 [101] H. Ting, L. Haifeng, M. Shanshan, Y. Zhang, L. Zhidan, D. Na, Progress in microalgae
ur
1555 [102] L. Yuan-Kun, Commercial production of microalgae in the Asia-Pacific rim, J. Appl. Phycol.
1556 9 (1997) 403–411.
1557 [103] J.L. Mendoza, M.R. Granados, I. de Godos, F.G. Acién, E. Molina, S. Heaven, C.J. Banks,
1558 Oxygen transfer and evolution in microalgal culture in open raceways, Bioresour. Technol.
1559 137 (2013) 188–195. https://doi.org/10.1016/j.biortech.2013.03.127.
1560 [104] F. Romagnoli, B. Ievina, Novel Stacked Modular Open Raceway Ponds for Microalgae
1561 Biomass Cultivation in Biogas Plants : Preliminary Design and Modelling, 24 (2020) 1–19.
1562 [105] Q. Lu, Y. Xiao, F. Chen, Application of microalgae biotechnology for the sustainable
1563 development of aquaculture, Adv. Bioenergy. 6 (2021) 117–163.
1564 https://doi.org/10.1016/bs.aibe.2021.06.001.
1565 [106] N.R. Moheimani, M.A. Borowitzka, The long-term culture of the coccolithophore
1566 Pleurochrysis carterae (Haptophyta) in outdoor raceway ponds, J. Appl. Phycol. 18 (2006)
1567 703–712. https://doi.org/10.1007/s10811-006-9075-1.
1568 [107] K. Kumar, S.K. Mishra, A. Shrivastav, M.S. Park, J.W. Yang, Recent trends in the mass
80
1569 cultivation of algae in raceway ponds, Renew. Sustain. Energy Rev. 51 (2015) 875–885.
1570 https://doi.org/10.1016/j.rser.2015.06.033.
1571 [108] Y. Lee, Microalgal mass culture systems and methods: their limitation and potential, J. Appl.
1572 Phycol. (2001) 307–315.
1573 [109] X.B. Tan, M.K. Lam, Y. Uemura, J.W. Lim, C.Y. Wong, K.T. Lee, Cultivation of
1574 microalgae for biodiesel production: A review on upstream and downstream processing,
1575 Chinese J. Chem. Eng. 26 (2018) 17–30. https://doi.org/10.1016/j.cjche.2017.08.010.
1576 [110] D. Pal, I. Khozin-Goldberg, Z. Cohen, S. Boussiba, The effect of light, salinity, and nitrogen
1577 availability on lipid production by Nannochloropsis sp., Appl. Microbiol. Biotechnol. 90
1578 (2011) 1429–1441. https://doi.org/10.1007/s00253-011-3170-1.
1579 [111] T.L. Walker, C. Collet, S. Purton, Algal transgenics in the genomic era, J. Phycol. 41 (2005)
of
1580 1077–1093. https://doi.org/10.1111/j.1529-8817.2005.00133.x.
ro
1581 [112] A. Richmond, Principles for attaining maximal microalgal productivity in photobioreactors:
1582 An overview, Hydrobiologia. 512 (2004) 33–37.
-p
1583 https://doi.org/10.1023/B:HYDR.0000020365.06145.36.
re
1584 [113] L. Brennan, P. Owende, Biofuels from microalgae-A review of technologies for production,
1585 processing, and extractions of biofuels and co-products, Renew. Sustain. Energy Rev. 14
lP
1590 [115] S. Öncel, A. Köse, D. Öncel, Façade integrated photobioreactors for building energy
1591 efficiency, Start-Up Creat. Smart Eco-Efficient Built Environ. (2016) 237–299.
Jo
1592 https://doi.org/10.1016/B978-0-08-100546-0.00011-X.
1593 [116] Z. Yin, L. Zhu, S. Li, T. Hu, R. Chu, F. Mo, D. Hu, C. Liu, B. Li, A comprehensive review
1594 on cultivation and harvesting of microalgae for biodiesel production: Environmental
1595 pollution control and future directions, Bioresour. Technol. 301 (2020).
1596 https://doi.org/10.1016/j.biortech.2020.122804.
1597 [117] L. Rodolfi, G. Chini Zittelli, N. Bassi, G. Padovani, N. Biondi, G. Bonini, M.R. Tredici,
1598 Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation
1599 in a low-cost photobioreactor., Biotechnol. Bioeng. 102 (2009) 100–12.
1600 https://doi.org/10.1002/bit.22033.
1601 [118] S.M.Z. Hossain, A. Alnoaimi, S.A. Razzak, H. Ezuber, N. Al-Bastaki, M. Safdar, S. Alkaabi,
1602 M.M. Hossain, Multiobjective optimization of microalgae ( Chlorella sp .) growth in a
1603 photobioreactor using Box-Behnken design approach, Can. J. Chem. Eng. (2018).
1604 https://doi.org/10.1002/cjce.23168.
1605 [119] A. Niccolai, G. Chini Zittelli, L. Rodolfi, N. Biondi, M.R. Tredici, Microalgae of interest as
1606 food source: Biochemical composition and digestibility, Algal Res. 42 (2019).
81
1607 https://doi.org/10.1016/j.algal.2019.101617.
1608 [120] O. Pulz, W. Gross, Valuable products from biotechnology of microalgae., Appl. Microbiol.
1609 Biotechnol. 65 (2004) 635–48. https://doi.org/10.1007/s00253-004-1647-x.
1610 [121] C.M. James, A.M. Al-Khars, An intensive continuous culture system using tubular
1611 photobioreactors for producing microalgae, Aquaculture. 87 (1990) 381–393.
1612 https://doi.org/10.1016/0044-8486(90)90075-X.
1613 [122] X. Cui, J. Yang, Y. Feng, W. Zhang, Simulation of a Novel Tubular Microalgae
1614 Photobioreactor with Aerated Tangent Inner Tubes: Improvements in Mixing Performance
1615 and Flashing-Light Effects, Archaea. 2020 (2020). https://doi.org/10.1155/2020/8815263.
1616 [123] K.M. Deamici, B.B. Cardias, J.A.V. Costa, L.O. Santos, Static magnetic fields in culture of
1617 Chlorella fusca: Bioeffects on growth and biomass composition, Process Biochem. 51 (2016)
of
1618 912–916. https://doi.org/10.1016/j.procbio.2016.04.005.
ro
1619 [124] K. Miyamoto, O. Wable, J.R. Benemann, Vertical tubular reactor for microalgae cultivation,
1620 Biotechnol. Lett. 10 (1988) 703–708. https://doi.org/10.1007/BF01025286.
1621
-p
[125] A. Sánchez-Mirón, F. García Camacho, A. Contreras Gómez, E. Molina Grima, Y. Chisti,
re
1622 Bubble-Column and airlift photobioreactors for algal culture, AIChE J. 46 (1999) 1872–
1623 1887.
lP
1624 [126] C.U. Ugwu, H. Aoyagi, H. Uchiyama, Photobioreactors for mass cultivation of algae.,
1625 Bioresour. Technol. 99 (2008) 4021–8. https://doi.org/10.1016/j.biortech.2007.01.046.
na
1626 [127] A. Richmond, Z. Cheng-Wu, Optimization of a flat plate glass reactor for mass production of
1627 Nannochloropsis sp. outdoors, J. Biotechnol. 85 (2001) 259–269.
ur
1628 https://doi.org/10.1016/S0168-1656(00)00353-9.
Jo
1629 [128] I. Ahmad, N. Abdullah, I. Koji, A. Yuzir, S. Eva Muhammad, Evolution of Photobioreactors:
1630 A Review based on Microalgal Perspective, IOP Conf. Ser. Mater. Sci. Eng. 1142 (2021)
1631 012004. https://doi.org/10.1088/1757-899x/1142/1/012004.
1632 [129] O. Pulzl, N. Gerbsch, R. Buchholz, Light energy supply in plate-type and light diffusing
1633 optical fiber bioreactors, J. Appl. Phycol. 7 (1995) 145–149.
1634 https://doi.org/10.1007/BF00693061.
1635 [130] Z.H. Kim, H. Park, S.J. Hong, S.M. Lim, C.G. Lee, Development of a floating
1636 photobioreactor with internal partitions for efficient utilization of ocean wave into improved
1637 mass transfer and algal culture mixing, Bioprocess Biosyst. Eng. 39 (2016) 713–723.
1638 https://doi.org/10.1007/S00449-016-1552-6/TABLES/2.
1639 [131] L. Brennan, P. Owende, Biofuels from microalgae—a review of technologies for production,
1640 processing, and extractions of biofuels and co-products, Renew. Sustain. Energy Rev.
1641 (2010).
1642 [132] D. Klein-Marcuschamer, Y. Chisti, J.R. Benemann, D. Lewis, A matter of detail: Assessing
1643 the true potential of microalgal biofuels, Biotechnol. Bioeng. 110 (2013) 2317–2322.
82
1644 https://doi.org/10.1002/bit.24967.
1645 [133] S. Paul, S. Bera, R. Dasgupta, S. Mondal, S. Roy, Review on the recent structural advances
1646 in open and closed systems for carbon capture through algae, Energy Nexus. 4 (2021)
1647 100032. https://doi.org/10.1016/j.nexus.2021.100032.
1648 [134] P. Schlagermann, G. Göttlicher, R. Dillschneider, R. Rosello-Sastre, C. Posten, Composition
1649 of algal oil and its potential as biofuel, J. Combust. 2012 (2012).
1650 https://doi.org/10.1155/2012/285185.
1651 [135] B. Ketheesan, N. Nirmalakhandan, Feasibility of microalgal cultivation in a pilot-scale
1652 airlift-driven raceway reactor, Bioresour. Technol. 108 (2012) 196–202.
1653 https://doi.org/10.1016/j.biortech.2011.12.146.
1654 [136] A.P. Carvalho, L. a Meireles, F.X. Malcata, Microalgal reactors: a review of enclosed system
of
1655 designs and performances., Biotechnol. Prog. 22 (2006) 1490–506.
1656 https://doi.org/10.1021/bp060065r.
ro
1657 [137] Q. Béchet, A. Shilton, B. Guieysse, Modeling the effects of light and temperature on algae
-p
1658 growth: State of the art and critical assessment for productivity prediction during outdoor
1659 cultivation, Biotechnol. Adv. 31 (2013) 1648–1663.
re
1660 https://doi.org/10.1016/j.biotechadv.2013.08.014.
lP
1661 [138] J. Nielsen, Bioreaction Engineering Principles, Psychol. Sci. 25 (2014) 1682–1690.
1662 [139] E. Greenwald, J.M. Gordon, Y. Zarmi, Physics of ultra-high bioproductivity in algal
na
1665 microalgae culture photobioreactor in series with recirculation system, CTyF - Ciencia,
1666 Tecnol. y Futur. 7 (2017) 101–116. https://doi.org/10.29047/01225383.68.
Jo
83
1681 outdoor pilot-scale photobioreactors, Biotechnol. Biofuels. 8 (2015).
1682 https://doi.org/10.1186/s13068-015-0400-2.
1683 [146] A.M. Blanco, J. Moreno, J.A. Del Campo, J. Rivas, M.G. Guerrero, Outdoor cultivation of
1684 lutein-rich cells of Muriellopsis sp. in open ponds, Appl. Microbiol. Biotechnol. 73 (2007)
1685 1259–1266. https://doi.org/10.1007/s00253-006-0598-9.
1686 [147] B. Crowe, S. Attalah, S. Agrawal, P. Waller, R. Ryan, J. Van Wagenen, A. Chavis, J. Kyndt,
1687 M. Kacira, K.L. Ogden, M. Huesemann, A comparison of nannochloropsis salina growth
1688 performance in two outdoor pond designs: Conventional raceways versus the arid pond with
1689 superior temperature management, Int. J. Chem. Eng. (2012).
1690 https://doi.org/10.1155/2012/920608.
1691 [148] A. Jacob, E.C. Bucharsky, K. GuenterSchell, The Application of Transparent Glass Sponge
1692 for Improvement of Light Distribution in Photobioreactors, J. Bioprocess. Biotech. 02
of
1693 (2012). https://doi.org/10.4172/2155-9821.1000113.
ro
1694 [149] J. Masojídek, J. Kopecký, L. Giannelli, G. Torzillo, Productivity correlated to
1695 photobiochemical performance of Chlorella mass cultures grown outdoors in thin-layer
1696
1697 -p
cascades, J. Ind. Microbiol. Biotechnol. 38 (2011) 307–317. https://doi.org/10.1007/s10295-
010-0774-x.
re
1698 [150] G. Olivieri, I. Gargano, R. Andreozzi, R. Marotta, A. Marzocchella, G. Pinto, A. Pollio,
lP
1702 [151] M. Leupold, S. Hindersin, G. Gust, M. Kerner, D. Hanelt, Influence of mixing and shear
ur
84
1720 [156] S. Sarkar, M.S. Manna, T.K. Bhowmick, K. Gayen, Effect of different illumination patterns
1721 on the growth and biomolecular synthesis of isolated Chlorella Thermophila in a 50 L pilot-
1722 scale photobioreactor, Process Biochem. 109 (2021) 87–97.
1723 https://doi.org/10.1016/J.PROCBIO.2021.07.007.
1724 [157] S. Azizi, B. Bayat, H. Tayebati, A. Hashemi, F. Pajoum Shariati, Nitrate and phosphate
1725 removal from treated wastewater by Chlorella vulgaris under various light regimes within
1726 membrane flat plate photobioreactor, Environ. Prog. Sustain. Energy. 40 (2021) e13519.
1727 https://doi.org/10.1002/EP.13519.
1728 [158] S. Azizi, A. Hashemi, F. Pajoum Shariati, B. Bonakdarpour, M. Safamirzaei, Fouling
1729 identification in reciprocal membrane photobioreactor (RMPBR) containing Chlorella
1730 vulgaris species: Hydraulic resistances assessment, J. Chem. Technol. Biotechnol. 96 (2021)
1731 404–411. https://doi.org/10.1002/JCTB.6552.
of
1732 [159] A. Klepacz-Smółka, D. Pietrzyk, R. Szeląg, P. Głuszcz, M. Daroch, J. Tang, S. Ledakowicz,
ro
1733 Effect of light colour and photoperiod on biomass growth and phycocyanin production by
1734 Synechococcus PCC 6715, Bioresour. Technol. 313 (2020) 123700.
-p
1735 https://doi.org/10.1016/j.biortech.2020.123700.
1736 [160] M. Patelou, C. Infante, F. Dardelle, D. Randewig, E.D. Kouri, M.K. Udvardi, E. Tsiplakou,
re
1737 L. Mantecón, E. Flemetakis, Transcriptomic and metabolomic adaptation of Nannochloropsis
1738 gaditana grown under different light regimes, Algal Res. 45 (2020) 101735.
lP
1739 https://doi.org/10.1016/J.ALGAL.2019.101735.
1740 [161] I.A. Avila-León, M.C. Matsudo, L.S. Ferreira-Camargo, J.N. Rodrigues-Ract, J.C.M.
na
1743 [162] Q. Ye, J. Cheng, X. Lai, Y. An, F. Chu, J. Zhou, K. Cen, Promoting Photochemical
Jo
1744 Efficiency of Chlorella PY-ZU1 with Enhanced Velocity Field and Turbulent Kinetics in a
1745 Novel Tangential Spiral-Flow Column Photobioreactor, ACS Sustain. Chem. Eng. 7 (2019)
1746 384–393. https://doi.org/10.1021/ACSSUSCHEMENG.8B03718.
1747 [163] J.C.M. Pires, M.C.M. Alvim-Ferraz, F.G. Martins, Photobioreactor design for microalgae
1748 production through computational fluid dynamics: A review, Renew. Sustain. Energy Rev.
1749 79 (2017) 248–254. https://doi.org/10.1016/j.rser.2017.05.064.
1750 [164] K. Kumar, C.N. Dasgupta, B. Nayak, P. Lindblad, D. Das, Development of suitable
1751 photobioreactors for CO2 sequestration addressing global warming using green algae and
1752 cyanobacteria, Bioresour. Technol. 102 (2011) 4945–4953.
1753 https://doi.org/10.1016/j.biortech.2011.01.054.
1754 [165] A. Carvalho, L.M.-B. progress, undefined 2006, Microalgal reactors: a review of enclosed
1755 system designs and performances, Wiley Online Libr. 22 (2006) 1490–1506.
1756 https://doi.org/10.1021/bp060065r.
1757 [166] G. Acien, J.M. Fernandez-Sevilla, E. Molina-Grima, F.G. Acién Fernández, • J M Fernández
1758 Sevilla, • E Molina Grima, Photobioreactors for the production of microalgae, Elsevier.
85
1759 (2016). https://doi.org/10.1007/s11157-012-9307-6.
1760 [167] K.E. McCloskey, Effects of shear stress on cells, in: Compr. Biotechnol., 2019: pp. 624–632.
1761 https://doi.org/10.1016/B978-0-444-64046-8.00037-9.
1762 [168] C.G. Khoo, M.K. Lam, K.T. Lee, Pilot-scale semi-continuous cultivation ofmicroalgae
1763 Chlorella vulgaris in bubble column photobioreactor (BC-PBR): Hydrodynamics and gas-
1764 liquid mass transfer study, Algal Res. 15 (2016) 65–76.
1765 https://doi.org/10.1016/j.algal.2016.02.001.
1766 [169] B. Le Gouic, H. Marec, J. Pruvost, J.F. Cornet, Investigation of growth limitation by CO2
1767 mass transfer and inorganic carbon source for the microalga Chlorella vulgaris in a dedicated
1768 photobioreactor, Chem. Eng. Sci. 233 (2021) 116388.
1769 https://doi.org/10.1016/j.ces.2020.116388.
of
1770 [170] S.A. Razzak, I. Al-Aslani, M.M. Hossain, Hydrodynamics and mass transfer of CO2 in water
1771 in a tubular photobioreactor, Eng. Life Sci. 16 (2016) 355–363.
ro
1772 https://doi.org/10.1002/elsc.201500063.
-p
1773 [171] A.P. Carvalho, F.X. Malcata, Effect of culture media on production of polyunsaturated fatty
1774 acids by Pavlova lutheri, Cryptogam. Algol. 21 (2000) 59–71. https://doi.org/10.1016/S0181-
re
1775 1568(00)00101-X.
lP
1776 [172] Y. Huang, S. Zhao, Y. dong Ding, Q. Liao, Y. Huang, X. Zhu, Optimizing the gas distributor
1777 based on CO2 bubble dynamic behaviors to improve microalgal biomass production in an
1778 air-lift photo-bioreactor, Bioresour. Technol. 233 (2017) 84–91.
na
1779 https://doi.org/10.1016/J.BIORTECH.2017.02.071.
1780 [173] F. Marazzi, M. Bellucci, S. Rossi, R. Fornaroli, E. Ficara, V. Mezzanotte, Outdoor pilot trial
ur
1781 integrating a sidestream microalgae process for the treatment of centrate under non optimal
1782 climate conditions, Algal Res. 39 (2019) 101430.
Jo
1783 https://doi.org/10.1016/j.algal.2019.101430.
1784 [174] D. Borowiak, K. Pstrowska, M. Wiśniewski, M. Grzebyk, Propagation of Inoculum for
1785 Haematococcus pluvialis Microalgae Scale-Up Photobioreactor Cultivation System, Appl.
1786 Sci. 10 (2020) 6283. https://doi.org/10.3390/app10186283.
1787 [175] G. Penloglou, C. Chatzidoukas, C. Kiparissides, Scale-up and intensification of a microalgae
1788 cultivation process for the production of high-added value biochemicals, Mater. Today Proc.
1789 5 (2018) 27463–27471. https://doi.org/10.1016/j.matpr.2018.09.065.
1790 [176] J.P. Díaz, C. Inostroza, F.G. Acién, Scale-up of a Fibonacci-Type Photobioreactor for the
1791 Production of Dunaliella salina, Appl. Biochem. Biotechnol. 193 (2021) 188–204.
1792 https://doi.org/10.1007/s12010-020-03410-x.
1793 [177] J.P. Díaz, C. Inostroza, F.G. Acién, Scale-up of a Fibonacci-Type Photobioreactor for the
1794 Production of Dunaliella salina, Appl. Biochem. Biotechnol. 193 (2021) 188–204.
1795 https://doi.org/10.1007/s12010-020-03410-x.
1796 [178] L. Zhao, Y. Gu, C. Peng, Z. Tang, Scale-up of the cross-flow flat-plate airlift
86
1797 photobioreactor, Asia-Pacific J. Chem. Eng. 15 (2020) 1–12.
1798 https://doi.org/10.1002/apj.2518.
1799 [179] C.E. Pfaffinger, T.S. Severin, A.C. Apel, J. Göbel, J. Sauter, D. Weuster-Botz, Light-
1800 dependent growth kinetics enable scale-up of well-mixed phototrophic bioprocesses in
1801 different types of photobioreactors, J. Biotechnol. 297 (2019) 41–48.
1802 https://doi.org/10.1016/j.jbiotec.2019.03.003.
1803 [180] M. Anwar, M.G. Rasul, N. Ashwath, Production optimization and quality assessment of
1804 papaya (Carica papaya) biodiesel with response surface methodology, Energy Convers.
1805 Manag. 156 (2018) 103–112. https://doi.org/10.1016/J.ENCONMAN.2017.11.004.
1806 [181] D.C. Montgomery, G.C. Runger, Applied Statistics and probability for engineers, 3rd ed.,
1807 John Wiley & Sons, Ltd, 2002.
of
1808 [182] D. Montgomery, Design and Analysis of Experiments, 2001.
ro
1809 [183] G.E.P. Box, W.G. Hunter, J. S. Hunter, Statistics for Experimenters, John Wiley & Sons,
1810 Ltd, New York, 1978.
1811
-p
[184] N. Aslan, Y. Cebeci, Application of Box-Behnken design and response surface methodology
re
1812 for modeling of some Turkish coals, Fuel. 86 (2007) 90–97.
1813 https://doi.org/10.1016/j.fuel.2006.06.010.
lP
1819 [186] X.B. Tan, X.P. Wan, L. Bin Yang, X. Wang, J. Meng, M.J. Jiang, H.J. Pi, Nutrients recycling
Jo
1820 and biomass production from Chlorella pyrenoidosa culture using anaerobic food processing
1821 wastewater in a pilot-scale tubular photobioreactor, Chemosphere. 270 (2021).
1822 https://doi.org/10.1016/j.chemosphere.2020.129459.
1823 [187] Z. Chen, Z. Jiang, X. Zhang, J. Zhang, Numerical and experimental study on the CO2 gas–
1824 liquid mass transfer in flat-plate airlift photobioreactor with different baffles, Biochem. Eng.
1825 J. 106 (2016) 129–138. https://doi.org/10.1016/J.BEJ.2015.11.011.
1826 [188] M. Ndiaye, E. Gadoin, C. Gentric, CO2 gas–liquid mass transfer and kLa estimation:
1827 Numerical investigation in the context of airlift photobioreactor scale-up, Chem. Eng. Res.
1828 Des. 133 (2018) 90–102. https://doi.org/10.1016/J.CHERD.2018.03.001.
1829 [189] C. Ji, J. Wang, R. Li, T. Liu, Modeling of carbon dioxide mass transfer behavior in attached
1830 cultivation photobioreactor using the analysis of the pH profiles, Bioprocess Biosyst. Eng. 40
1831 (2017) 1079–1090. https://doi.org/10.1007/S00449-017-1770-6/TABLES/3.
1832 [190] V. Belohlav, E. Uggetti, J. García, T. Jirout, L. Kratky, R. Díez-Montero, Assessment of
1833 hydrodynamics based on Computational Fluid Dynamics to optimize the operation of hybrid
1834 tubular photobioreactors, J. Environ. Chem. Eng. 9 (2021) 105768.
87
1835 https://doi.org/10.1016/J.JECE.2021.105768.
1836 [191] T. Zavřel, H. Schoffman, M. Lukeš, J. Fedorko, N. Keren, J. Červený, Monitoring fitness and
1837 productivity in cyanobacteria batch cultures, Algal Res. 56 (2021) 102328.
1838 https://doi.org/10.1016/J.ALGAL.2021.102328.
1839 [192] Y. Wang, S.M. Tibbetts, P.J. McGinn, Microalgae as sources of high-quality protein for
1840 human food and protein supplements, Foods. 10 (2021).
1841 https://doi.org/10.3390/foods10123002.
1842 [193] M.I. Khan, J.H. Shin, J.D. Kim, The promising future of microalgae: Current status,
1843 challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and
1844 other products, Microb. Cell Fact. 17 (2018). https://doi.org/10.1186/s12934-018-0879-x.
1845 [194] X. Gao, B. Kong, R.D. Vigil, Simulation of algal photobioreactors: recent developments and
of
1846 challenges, Biotechnol. Lett. 40 (2018) 1311–1327. https://doi.org/10.1007/s10529-018-
1847 2595-3.
ro
1848 [195] S. Petrini, P. Foladori, L. Donati, G. Andreottola, Comprehensive respirometric approach to
-p
1849 assess photosynthetic, heterotrophic and nitrifying activity in microalgal-bacterial consortia
1850 treating real municipal wastewater, Biochem. Eng. J. 161 (2020).
re
1851 https://doi.org/10.1016/j.bej.2020.107697.
lP
1852 [196] M.A. Alam, Z. Wang, Microalgae biotechnology for development of biofuel and wastewater
1853 treatment, Microalgae Biotechnol. Dev. Biofuel Wastewater Treat. (2019) 1–655.
1854 https://doi.org/10.1007/978-981-13-2264-8.
na
1855 [197] F.G. Acién, E. Molina, A. Reis, G. Torzillo, G.C. Zittelli, C. Sepúlveda, J. Masojídek,
1856 Photobioreactors for the production of microalgae, Microalgae-Based Biofuels Bioprod.
ur
1859 [198] S.A. Razzak, S.A.M. Ali, M.M. Hossain, A.N. Mouanda, Biological CO2fixation using
1860 Chlorella vulgaris and its thermal characteristics through thermogravimetric analysis,
1861 Bioprocess Biosyst. Eng. 39 (2016) 1651–1658. https://doi.org/10.1007/s00449-016-1640-7.
1862
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Highlights:
Photobioreactors promise sustainable industrial-scale production in Saudi Arabia.
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Finding the research gap and future perspectives for mass scale microalgae cultivation are
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Declaration of interests
☒ The authors declare that they have no known competing financial interests or personal relationships
that could have appeared to influence the work reported in this paper.
☐The authors declare the following financial interests/personal relationships which may be considered
as potential competing interests:
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