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A review on photobioreactor design and

Cite this: DOI: 10.1039/d0re00450b
modelling for microalgae production
Jack Legrand, *a Arnaud Artub and Jérémy Pruvosta
A microorganism culture process is a complex system in which physical operating parameters and
biological responses strongly interact. Mathematical formulation and modelling of the different phenomena
involved in the process enable a better understanding of the behaviour of the process, and therefore
enable the process parameters to be defined accordingly. The contribution of a model, even a simple one,
is highly beneficial to the understanding of the process. The definition of a model for the particular case of
photobioreactors is not easy, however, and requires the integration of multiple and often complex
knowledge. This article reports a review on the biological aspects of the photosynthetic microorganisms
Received 1st December 2020, culture necessary to model kinetic growths, the designs of photobioreactor used for deep analysis of the
Accepted 14th April 2021
physiologic aspects of the microalgae culture and for the industrial culture. The different approaches to
DOI: 10.1039/d0re00450b
model the kinetic growth are described together with the modelling of the radiative field and its coupling
to a simple biological model in order to illustrate the particular influence of the light factor, which is the
rsc.li/reaction-engineering main specific feature of photobioreactors.
Introduction a wide range of applications. Large-scale cultivation of

microalgae is nowadays mainly reserved for certain species,
Photosynthetic microorganisms, through cyanobacteria, are at known as extremophilic, and is mainly carried out in open
the origin of the oxygen contained in the atmosphere. These ponds. However, research into the production of microalgae in
microorganisms have also used since thousands of years, to closed systems is still in progress. This is particularly the case
feed populations thanks to their nutritional quality. The in recent years, especially due to the increasing scarcity of fossil
interest in photosynthetic microorganisms has only been fuels, to produce third-generation biofuel from microalgal
stopped increasing, in particular due to the diversity of existing biomass. This application of microalgae certainly appears to be
species and metabolites of interest they contain. The the most important today, given the objectives and constraints
composition of microalgae is of interest in many fields, such as that this imposes. There is a strong need for research,
human and animal food, cosmetics, health, or energy.1,2 Many particularly on closed cultivation systems. Indeed, these culture
researches are turning to so-called third-generation fuels from systems equipped with of instrumentation allow the
photosynthetic microorganism biomass (microalgae and maintenance of optimal conditions for growth (reduction of
cyanobacteria, etc.).3 This possible valorisation is in addition to the risks of contamination, control of physico-chemical
the many ways of use microalgal biomass. Agri-food parameters such as pH, temperature, etc. …). These systems
applications (dietary supplements for food or feed),4 called photobioreactors (PBRs) thus make it possible to convert
environmental (water pollution and smoke control, etc. …), energy biomass light via the photosynthesis mechanism more
medical (dietary deficiencies, anti-cancer drugs)5–8 can thus be efficiently than open systems. Biomass composition, growth
cited. Compared to other plant resources, the exploitation of rate, and metabolites depends depend strongly on the strain
photosynthetic microorganisms has several advantages: their and on the cultivation conditions. Important factors are light
high growth rate gives access to higher yields than the intensity, composition of the medium, temperature, pH,
terrestrial plants and their biodiversity combined with their carbon dioxide. The complex interactions between the different
ability to orientate their metabolism to promote the synthesis parameters affecting the biomass growth could be investigated
of a compound, by imposing specific growing conditions offer through the development of models which are able to predict
the biomass productivity. There are several ways to grow
a
photosynthetic microorganisms, depending on the desired
University of Nantes, CNRS, ONIRIS, GEPEA, UMR6144, 37 bd de l'Université, BP
406, 44602 Saint-Nazaire Cedex, France. E-mail: Jack.Legrand@univ.nantes.fr
application. Two modes of culture can be operated: autotrophy
b
Total, Direction générale Raffinage-Chimie, Division Biofuels, Tour Coupole, 2 and heterotrophy. Autotrophy consists of the addition of an
Place Jean Millier, 92078 Paris La Défense, France inorganic carbon source while heterotrophy uses an organic
This journal is © The Royal Society of Chemistry 2021 React. Chem. Eng.
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Review Reaction Chemistry & Engineering
carbon source. Mixotrophy is obtained when the two sources In the first part, a reminder of photosynthesis and the
are mixed. In this article, only autotrophic cultures are associated production of microalgae is given, as well as the
considered. Two main families of culture systems can be factors limiting their growth. Then, some examples of culture
distinguished: open reactors and closed reactors (PBR). system design are described, with focus on laboratory culture
Although expensive due to their high level of technology, the systems, which are necessary to study the behaviour of
latter allow total control of the reactor and growing conditions microalgae and to get information on growth kinetics, on
and give access to performances far superior to those of the open, closed and developing systems. The last part concerns
obtained in extensive cultivation systems (raceway type). This is the different modelling approaches.
mainly due to that PBRs allow a certain control level of
operating conditions obtaining reproducible conditions for the Photosynthesis and production of
culture9 and all nutritional limitations can be deleted with the microalgae
exception of light. The growth rate of the microorganisms is
then controlled solely by the thermodynamic efficiency of The term “microalgae” includes, strictly speaking, any
photon use,10 corresponding, to photolimited growth. This microscopic algae. This includes microalgae (eukaryotes) as
mode of cultivation makes it possible to obtain performances well as prokaryotic organisms (cyanobacteria) and
close to maximum productivity on the surface (mass of photosynthetic bacteria. Three modes of culture are to be
biomass produced per unit area). For a reduction of the distinguished: autotrophy, which consists in the feeding of
impacts of biomass production, several ways are being studied, an inorganic carbon source, heterotrophy, an organic carbon
such the recycling of industrial flue gases as a source of carbon, source, and mixotrophy, when inorganic and organic sources
the recycling of the culture media to limit water consumption, are mixing. In this article only autotrophic cultures, then
the use of waste water as a basis for culture media with in cultivation by photosynthesis, are considered. Photosynthesis
addition environmental benefits. In fact, the CO2 from is described by the following equation:
industrial plants can be fixed for mitigation of the greenhouse
light
gas emission as well as nitrogen or phosphorus removal in CO2 þ H2 O → ½CH2 O þ O2 (1)
wastewater treatment processes.11 The majority of the culture
systems are built in a small scale medium (maximum a few ha) This process converts light energy into chemical energy (ATP
for a total worldwide biomass production around 30 000–50 000 and NADPH) which is then used by cells to synthesize
tonnes of dry matter per year. This production is obviously not organic carbon from inorganic carbon (CO2 or other
enough to meet the demand for biofuel, an insufficient dissolved inorganic carbon). This conversion is made
quantity for the real worldwide demand.12,13 Moreover, the possible by the succession of two types of reactions: (i) light
production costs of biofuels from microalgae are too high to (or photochemical) reactions and dark (or biochemical)
compete in energy markets. To further reduce the production reactions. The light reactions take place in the thylakoids.
cost of the system, it is necessary to employ the use of Thylakoid membranes have photosynthetic pigments
advanced control strategies to ensure an optimization of the grouped into photosystems. Two photosystems called PSI and
system is a way to reduce the production cost.14 To control the PSII absorb light at slightly different wavelengths. Incident
pH of the culture and reducing significantly the cost and the photons having a wavelength within a domain of radiation,
CO2 losses of the system, techniques based on model predictive called photosynthetically active radiation (PAR, 400 nm < λ <
control have obtained successful results in this target.15–17 It is 700 nm) are picked up by a photon collecting antenna,
necessary to take into account all the system variables to have a named here light harvesting complex II (LHCII), composed of
cost reduction by a good use of the resources. For example, pigments (chlorophyll a and b and protective carotenoids
Ifrim et al. (2013)14 developed a nonlinear multivariable (PPC, photo-protective carotenoids)). The energy of photons
controller based on dynamical model with an exact feedback having an energy equivalent higher than that of a photon
linearization to control biomass concentration and pH by emitted at 680 nm or 700 nm (E = hc/λ) is degraded to the
acting on the dilution rate and the injected carbon dioxide gas same energy level accepted by the corresponding
flow rate. Depending on the control complexity, different types photosystem. Excess energy is dissipated in the form of heat
of system models are developed. Fernández et al. (2014)18 has or fluorescence by the collector antenna. The energy
developed a dynamic model for microalgae production in equivalent to one photon emitted at 680 nm (PSII) or 700 nm
tubular photobioreactor for the prediction of the main (PSI) is then transmitted to the reaction centers (primary
parameters influencing the microalgae growth rate: electron donors), called P680 and P700) by proteins D1 and
temperature, pH, dissolved oxygen and biomass concentration. D2. This contribution of energy at the reaction center will
Calibration and validation tests have been made in an outdoor change it from a P680 state to an excited state noted P680*,
tubular photobioreactor. A review on the use of Computational thus releasing an electron. The latter will be transferred by
Fluid Dynamics (CFD) for the optimization of bioreactor design the plastoquinone (PQ) which will take two protons available
and for the study of the interaction of hydrodynamics, light in the stroma (inside the chloroplast) to switch to its oxidized
supply, heat and mass transfer with biological kinetics has state PQH2. The electrons recovered by the PQ are removed
been done by Pires et al. (2017).19 from the water by oxidation (photolysis of water). This
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reaction takes place at the level of the tyrosine Z complex group. The G3P molecule is a three-carbon sugar. For every
and allows the release of 4 protons, 4 electrons and 1 oxygen twelve moles of G3P synthesized, only two are transported to
molecule per molecule of oxidized water. The protons are the metabolic pathway of sugars, the remainder being
released in the lumen (inside the thylacoid). The PQ directed to the third phase of the cycle, the regeneration of
transmits its two electrons to the cytochrome b6f and rejects RuBP. This last phase completes the Calvin cycle by
two protons into the lumen. The cytochrome b6f also pumps synthesizing RuBP molecules from G3P under the action of
two protons from the stroma into the lumen, thus ATP to regenerate the first CO2 acceptor.
contributing to accentuate the proton gradient between the The efficiency of photosynthesis is directly related to the
inside (highly charged proton) and the outside of the amount at the photon rate received at a point. This rate is
thylacoid (weakly charged). The two electrons are then called irradiance (G) and its unit is the micromole of photons
transferred to a second electron carrier, the plastocyanine absorbed per square meter of surface area per second (μmolh
(PC). The PC will transmit one electron at a time to the P700 m−2 s−1). Three behaviours are distinguished: (i) a
(PSI). The P700 is similar to P680, except that it operates at photolimited regime, in which photosynthesis increases with
an energy equivalent of one photon at 700 nm. The P700 will irradiance, (ii) a second, so-called photosaturated regime, in
accumulate two electrons, which will take it to its excited which photosynthesis is independent of the light received,
state P700*. He will then give up his electrons to ferredoxin and (iii) a photoinhibition regime in which the efficiency of
(Fd). The ferredoxin transfers its electrons to the enzyme photosynthesis decreases with the increase in irradiance
ferredoxin NADP reductase (FNR) which will allow the received by the microorganism. It should be added to this
reduction of NADP+ to NADPH, H+, which induces the that below a certain irradiance value, called compensatory
pumping of an additional proton from the stroma to the irradiance, and characterized by a zero oxygen balance at the
lumen. The proton gradient generated by the protolysis of cell level, the phenomenon of respiration is predominant
the water is used as a proton-motor force for the synthesis of over photosynthesis. This is characterised by negative
ATP by the enzyme ATP synthase at from ADP and inorganic biomass production (consumption of carbon reserves).
phosphate. There are two electron transfer paths: an acyclic
pathway, leading to the synthesis of ATP and NADPH, H+ by Factors limiting growth of microalgae
photophosphorylation (Z-schema), and a second, called cyclic
electron transfer. This is a direct transfer of a electron from Many parameters can affect the productivity of a
ferredoxin to PQ. This results in the pumping of protons by photobioreactor. Biological parameters such as bacterial and
the cytochrome, which increases the proton gradient and fungal contamination, predation by protozoa, or even
promotes the production of ATP, without producing of sometimes contamination by another microalgae than the
NADPH, H+. The specific production rates of ATP and desired one.22 Several physico-chemical parameters are also
NADPH, H+ directly affect the metabolism and growth of a influential: light energy supply, temperature, pH, salinity and
photosynthetic microorganism. The ratio of these two terms the supply of nutrients necessary for growth (including
(defined as the P/2e− by Cornet et al. (1998)20 will reflect the inorganic carbon). The homogeneity of temperature, pH and
adjustment of the cells energy metabolism. Similarly, the salinity, as well as the nutrient accessibility to microalgae and
phthosynthetic quotient, QP, is denoted, as the ratio between light access in the system are controlled by the hydrodynamics
the production rate of one mole of oxygen and the of the system, making it a key parameter for the optimization
consumption rate of one mole of carbon dioxide. Similarly, of PBR production. The dynamics of operation under solar
the ratio QRO2 (quantum requirement for oxygen production) conditions brings an additional particularity, a notion of
denotes the number of photons necessary to produce one instability over time, which does not allow the system to
mole of oxygen. Theoretically this value is eight photons per operate at the optimum throughout the day. This applies in
oxygen molecule.21 The ATP and NADPH, H+ molecules will particular to light, or even temperature and pH depending on
then be used for Calvin cycle (dark reactions). The dark the control conditions of the culture system.
reactions are related to carbon fixation take place through a
cycle called Calvin cycle. This cycle takes place in the stroma Light energy in photobioreactors
and uses the energy stored during the light phase in the form The efficiency of photosynthesis is directly related to the
of ATP and NADPH, H+ to fix inorganic carbon and amount of light absorbed by the microalgae. At the cell level, it
synthesize organic carbon. The first phase is the carbon is possible to know the quantity of light necessary to obtain the
fixation by the synthesis of 3-phosphoglycerate (3PGA) from maximum performance of the microalgae. When considering
CO2 and ribulose-1,5-biphosphate (RuBP), a reaction the photobioreactor system, it is easy to understand that if
triggered by an enzyme, RuBisCO. The second phase is the microalgae absorb part of the light transmitted to it, the rest of
reduction phase, during which each 3PGA molecule receives the microalgae contained in this system will share the
an additional phosphate from ATP (synthesized in clear remaining flux. As a consequence, light energy is
phase), then an electron pair released by the NADPH, H+ heterogeneous in the volume of the photobioreactor. It will be
molecule reduces the 1,3-biphosphoglycerate molecule to then impossible to maintain maximum performance for all the
D-glycéraldéhyde-3-phosphate (G3P), releasing a phosphate microorganisms in the PBR. When considering a flat PBR, the
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attenuation of light, when transmitted homogeneously to the considering the light received by the microalgae in the reactor,
PBR, occurs in only one dimension, in the thickness of the characterized by irradiance G. This parameter γ is the ratio of
culture. The light attenuation profile depends on several the illuminated volume to the total volume of the PBR. The
parameters: (i) the amount of light transmitted at the surface boundary between these two zones is then given by the
of the PBR also called PFD (photon flux density in μmol m−2 compensating irradiance (Gc). When the local irradiance is
s−1), (ii) the concentration of microalgal biomass (CX in gX l−1) below this value, the zone is considered to be a dark volume, in
and (iii) the radiative properties of the microalgae, depending which the phenomenon of respiration is predominant, and
in particular on the pigment content of the microalgae (wpig in thus negatively impacts biomass productivity. The three
%) and the shape of the cultured microalgae.23 Pruvost and operating regimes are as follows (Fig. 1):
Cornet (2012)24 identified three light attenuation regimes - Photo-limited regime (case a): in this case γ < 1, the
corresponding to distinct performances. These are entire photon flux transmitted to the crop is absorbed. A dark
differentiated by the parameter γ, representing the illuminated zone is present due to the high biomass concentration. This
volume fraction in a PBR. In the literature, this is defined by is achieved by a high residence time of the microalgae and
Fig. 1 Light attenuation profiles for a planar PBR and associated productivities:24 (a) case for γ < 1, (b) case for γ = 1, (c) case for γ > 1 (this figure
was published in J. Pruvost and J.-F. Cornet, Microalgal Biotechnology: Potential and Production, 2012, De Gruyter, Berlin, Germany, 181–224,
Copyright De Gruyter).
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does not allow maximum biomass productivity due to the consumption of the cell's carbohydrates (energy source) in the
negative impact of respiration. metabolism of cell maintenance and protein synthesis.32
- Strict physical limitation or luminostat regime (case b): Photosynthetic microorganisms are unequal to the phenomenon
here γ = 1, i.e. all the light transmitted to the system is of respiration. Indeed, cyanobacteria will lose on average less
absorbed by the microalgae without the appearance of a biomass at night than the eukaryotic cells.33 Moreover, within
respiration zone (G(L) = Gc). It is this regime that leads to the eukaryotic microorganisms, there is a great disparity in
maximum performance of a PBR for a given light flux. respiration rates at night depending on the cultured.31 The most
- Kinetic regime (case c): here γ > 1, i.e. part of the light is influential parameter on the loss of biomass in the dark phase
not absorbed in the culture volume and is therefore of a given microalgae is temperature. Edmundson and
transmitted. This translates in energy terms into biomass Huesemann (2015)31 showed that when the temperature at night
productivity below the maximum achievable productivity was reduced from 25 °C to 10 °C, it was possible to reduce
(because not all the transmitted energy is converted). This biomass decrease. The most impressive case is that of the
regime is very particular because the residence time is low, microalga Nanochloropsis salina, which loses 20% of its dry
which leads to a decrease in biomass concentration and a matter concentration after ten hours in the dark at 25 °C,
risk of culture leaching. Moreover, the system performance whereas reducing the temperature to 10 °C over the same period
can be reduced by poor absorption of the luminous flux. only results in a decrease in concentration of around 2%. The
Indeed, due to the low light attenuation, the amount of slowing down of metabolic activity, and therefore of the decrease
energy absorbed by the microalgae is important, which can in biomass by temperature reduction has been confirmed by
induce a phenomenon of photosynthesis oversaturation or numerous studies on numerous microorganisms.32–35
even photoinhibition, damaging the photosynthetic In order to guarantee a good thermal management in a
apparatus of the microalgae and significantly reducing the PBR (to maximise production) and to be able to estimate the
performance of the PBR. energy needs linked to the control of a PBR, it is essential to
be able to represent the different exchanges taking place
within it. Knowing the exchanges taking place in a growing
Temperature and microalgal growth system allows to model the temperature evolution in a given
A non-optimal culture temperature affects the growth of culture system throughout the year. It also serves as a tool for
microalgae. Although not directly affecting photochemical dimensioning the thermal exchanger necessary for the
reactions, the temperature at which the microorganism grows regulation of a solar PBR (and for estimating the associated
plays a major role in enzyme activity.25 This has the costs), and thus as a tool for comparing temperature-
consequence of reducing the growth capacity of a given regulated closed PBRs. Solar radiation is responsible for the
microorganism when growth deviates from the optimum, heating of microalgae cultures, but other thermal exchanges
and in some cases even leading to cell death. In addition, a take place between a PBR and its environment.
change in the temperature of the medium can force the
microalgae to change its composition. This has been shown
for example on lipids.25 For the culture of the study Nutrients and carbon supply
microalga, C. vulgaris, the optimal growth temperature is For a photosynthetic microorganism, essential nutrients are
estimated to be between 20 and 30 °C.26–28 Most microalgae needed, at least a source of nitrate (or ammonium), sulphates
are so-called mesophilic, i.e. they have an optimal growth and phosphates ions. These nutrients are provided under
temperature between 15 and 40 °C. For the latter, a chemical salts dissolved in aqueous solution. The
temperature of the environment surrounding the microalgae composition of the culture medium is adjusted according to
above 45 °C for more than 24 hours can have an irreversible the specific needs of the cultured microorganisms. Nutrients
effect on the culture.29 There are other strains which, due to can be supplied in three different ways. A high dose is only
their natural environment, have totally different optimal given at the beginning of the cultivation, this is called a
growth temperatures, such as the so-called psychrophilic batch culture. The solution is brought continuously to the
(Topt <15 °C) and thermophilic (Topt >50 °C) microalgae.28 culture, a part of the culture is then continuously renewed),
No photosynthetic microorganisms with an optimal growth it is called continuous culture mode. The fed-batch mode
temperature above 75 °C have so far been identified, corresponds to the addition of new medium is done
probably due to the instability of chlorophylls at this punctually during the cultivation process. For the continuous
temperature.28 Generally, the temperature control must be mode, two cases can be distinguished: the chemostat mode
addressed for the evaluation of the technical feasibility of for which the supply of the medium is fixed by the flow rate
large-scale algae production.30 of the feed pump, and the turbidostat mode for which the
When producing microalgal biomass under solar conditions, supply of the medium is regulated according to the quantity
the night period is often a period when no production takes of biomass in the culture.
place. However, the loss of biomass due to respiration can be Carbon is the majority element in the biomass, it
major, sometimes up to 20% biomass loss for a ten-hour represents about half of the dry mass of the microalgae. In
night.31 The night period is generally accompanied by a autotrophic culture, it is brought into the medium in the
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form of inorganic salts dissolved in the culture medium agitation speed should be around 15 cm s−1.38 In a raceway-
(HCO3− or CO32−) or in gaseous form (CO2) transferred to the type basin, the preferred agitation system is the paddle wheel
culture. When grown in an open system, the liquid is in for several reasons.36 The presence of vertical velocities
equilibrium with the atmosphere containing a very low allows good agitation and distribution of biomass in all
quantity of CO2(g), i.e. about 400 ppm. Consequently, if the dimensions. Moreover, this system causes very low shear and
medium contains dissolved carbon in a quantity greater than is suitable for all microalgae strains, including the most
that given by the equilibrium with the atmosphere, a fragile. Finally, the electrical consumption linked to agitation
desorption of CO2 in its aqueous form towards its gaseous with this type of system remains low (around 6 W m−2).
form will be generated by this concentration gradient. In Nevertheless, recent studies highlight the interest of stirring
addition, the form in which inorganic carbon is present is raceway systems by airlift, which would be up to three times
pH dependent. With a pH above 9, desorption is low because less energy consuming than the paddle wheel, while
only the aqueous form of CO2 is in equilibrium with the maintaining the same quality of agitation.39
gaseous phase. Therefore, at high pH, it is not necessary to A wide variety of PBRs technologies exist, such as tubular,
cover a culture system to avoid carbon limitation, this cylindrical or flat panel systems with specific mixing
explains why Spirulina platensis culture is generally grown in problems. However, the criteria for a “good” mixing can be
an open system. As is the case with temperature, each stated: avoid sedimentation of the biomass, give the same
microalga has an optimal pH for growth. For example, story about the light received to the whole algal population,
Chlorella vulgaris grows at pH values between 5 and 9 with an satisfy heat transfer to maintain an optimal temperature and
optimal pH between 7 and 8.36 For the cyanobacterium gas–liquid mass transfer for CO2 supply and O2 removal,
Anabaena, this optimum is between 9 and 10. During avoid biofilm formation and shear rates too high in relation
cultivation, when growth occurs, the total carbon to cell fragility. From the conception point of view, different
concentration decreases. Since CO2 is an acid, the pH then criteria have to be taken into account: cost, limitation of the
increases.37 Increasing this pH may reduce growth. One dark zones, limitation of the thickness of the culture media
method of ensuring the presence of carbon (avoiding to increase the volumic productivity, easiness to scale up and
limitation) and maintaining the pH at the optimal level is energy efficiency. The various PBR technologies available
therefore to occasionally add gaseous (acidic) CO2 to the have advantages and limitations in terms of hydrodynamics
culture when the pH exceeds the set value. conditions and biomass productivity relatively to the
construction cost.50,69,76,81
Mixing and microalgal growth Design of photobioreactors

Although this parameter is not directly a factor inhibiting or
promoting growth, it acts at the reactor scale as an overall The photobioreactors are most often categorized according to
parameter acting on all the other parameters presented their size, agitation mode (when available), light source (solar
above. Indeed, all the considerations concerning thermal, or artificial), culture depth, or shape (flat or tubular).22,29,40–42
salinity, pH, biomass concentration (and consequently light This highlights the complexity and thus the non-universal
attenuation) are valid only if agitation makes the medium, in nature of the microalgae culture bioprocess. Indeed, the
which the microalgae grow, homogeneous. Since the 1950s, choice of a given technology will depend on the application
Richmond and Hu (2013)29 concluded after simple trials (energy, food, cosmetics…), the geographical area, the
(culture with and without agitation) that the growth of a available resources (surface area, electricity…), and the
dense culture of microalgae was promoted by setting the cultivated strain (extremophilic, fragile…). Changing one of
microalgae in motion. This can be explained, for example, by these parameters may favour the use of a different system.
the presence of thermal stratification or a pH gradient within
the culture system in the absence of agitation. There are Labscale photobioreactors
different mechanical and non-mechanical systems for the Lab-scale cultures are made in photobioreactors with
movement of microalgae in a PBR. Non-mechanical stirring artificial lighting. To study the impact of a parameter on
is bubble stirring. This type of agitation has two advantages: the growth or production of a particular metabolite, it is
the shear is generally low, which will not generate any necessary to perfectly control all the parameters acting on
agitation stress; moreover, it promotes the transfer of production, i.e.: light intensity, pH, temperature, nutrient
dissolved oxygen from the liquid phase to the gas phase, concentration, agitation and biomass concentration. The
which reduces the risk of growth inhibition due to too high most classic of the chemical or biological reactors is the
an oxygen concentration in the culture medium. Circulation perfectly stirred reactor, because of the possibility to get a
by mechanical system can be done via a recirculation pump, homogeneous mixture, including biomass. In contrast to
a marine propeller, a paddle wheel or by manual agitation common chemical nutrients, it is not possible to distribute
depending on the application and the geometry of the culture the light homogeneously in whole reactor volume, because
system used. To ensure agitation for maximum performance of the light attenuation caused by the light absorption by
of a culture system regardless of geometry, the average the microalgae.
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Fig. 3 EOSS-PBR (with courtesy of GEPEA laboratory – UMR CNRS 6144).
parallel (Fig. 3). Each column has a volume of 30 ml and

could be operated in batch and semi-continuous conditions.
Fig. 2 Torus photobioreactor (with courtesy of GEPEA laboratory –
UMR CNRS 6144).
Other photobioreactor geometries have been developed for
the same research use. The geometries found in the literature
are: (i) cylindrical geometry, inspired by stirred-tank fermenters
with internal or external illumination,50,51 (ii) tubular
Csögör et al. (1999)43 have developed a PBR, which geometry,52 (iii) plane geometry,52,53 (iv) bubble column,54,55 (v)
combine the advantages of a stirred reactor and a plate airlift column,56,57 (vi) helical tubular,58 (vii) conical.59
reactor to reduce the light path length. Another example is
the torus-shaped PBR, which was designed44 for lab-scale
experiments requiring a full control of culture conditions Open industrial systems
(Fig. 2). The culture is circulated in a torus-shape tank by the The first use of microalgae by humans dates back more than
rotation of a marine impeller. The combination of the culture 2000 years, to China, where the cyanobacterium Nostoc was
rotation and the torus configuration allows good mixing harvested in response to famine.1 Nowadays there are many
without dead volume and with reasonable shear stress.44 The commercial applications, which is why microalgae, originally
light-supplying device (LED panel) is placed in front of the harvested in their natural environment, are now produced in
PBR. The plane front surface and the square-sectioned torus real farms or even factories. It should be noted that although
channel prevents optical distortion along the light emission research into large-scale production dates back to the 1950s,
direction. As a consequence, light attenuation occurs along
only one main direction, leading to facilitate calculation of
light transfer and light attenuation conditions.
The torus-shaped PBR has been used to model and
optimize microalgal biomass productivity23,45 and to
investigate the coupling between hydrodynamics and
photosynthetic conversion for the “light/dark cycles effect”.46
Another example can be found in Martzolff et al. (2012).47
The possibility to control of mixing time with respect to the
circulation time and the plug-flow behavior was used for
isotopic nonstationary 13C-metabolic flux analysis. The
characterization of the kinetics of 13C-labeling incorporation
allows to define the biochemical reaction network of C.
reinhardtii.48 For the screening of operating conditions for a
given strain or comparing microalgae strains in the same
conditions, a cultivation system, named efficient
overproducing screening system-photobioreactor (EOSS-PBR), Fig. 4 D. salina ponds at Hutt Lagoon (Australia) (http://www.bsb.
was developed by Taleb et al. (2015).49 It consists of six fully murdoch.edu.au/groups/beam/BEAM-Appl0.html, with permission of
automated small-scale bubble columns PBRs operated in Professor Michael A. Borowitzka).
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the term “farming” appeared in the 1960s.22 The first systems to reduce the thickness of the culture as much as possible for
dedicated to the cultivation of microalgae were artificial the same ground surface area. For this purpose, a slightly
ponds, also called lagoons. This is the simplest production inclined plane system was developed (inclination of 1.7%,67
system. It consists of a body of water between 20 and 40 on which the microalgae culture flows down and is then
centimeters deep without agitation. This system was used by reinjected at the reactor head via a pump (Fig. 6).
the Cognis company in Hutt Lagoon (Australia) to cultivate This cultivation system reduces the costs of biomass
the microalga Dunaliella salina (Fig. 4). These microalgae are production and processing. Indeed, since production is only
cultivated for their high carotene content. Today, the global dependent on the lighting area, a reduction in thickness
company BASF farms these 700 hectares of land, making it will have under identical conditions no impact on the
the largest production site in the world.60 quantity of biomass produced. Agitation and separation of
Subsequently, agitated basins were developed in order to biomass from water will therefore be cheaper due to the
avoid sedimentation and thus optimize light distribution in small amount of water to be treated. An industrial version
the culture volume. Moreover, this avoids the presence of of this concept has been implemented in Portugal by the
concentration gradients or thermal stratification, reducing the company A4F in 2014. This system comprises a succession
overall performance of the process.42 Thus, in order to of four inclined planes for a total production area of 3000
guarantee homogeneity in the culture basin, Andersen (2005)61 m2 (Fig. 7).
recommends an average velocity between 20 and 30 cm s−1 to Even today, open systems are still the most widely used on
avoid the risk of sedimentation. This generally guarantees an industrial scale because of their low manufacturing cost
minimum local velocities in the basin greater than 10 cm s−1. and ease of extrapolation. However, they are not suitable for
This velocity is defined as the velocity at which the risks of all types of production. Indeed, these systems are reserved
biomass sedimentation appear (for most strains). The most for the production of extremophilic strains, because of the
popular open agitated systems on a large scale are circular and risk of contamination by airborne microorganisms. There is
raceway-type systems.114 Circular systems are agitated via an no problem for strains such as Dunaliella salina or Arthrospira
arm with a size of the radius of the basin set in motion by the platensis because these two photosynthetic microorganisms
axis. This type of basin has two major disadvantages, a non- grow in conditions where most contaminants cannot
optimal surface area (due to the circular shape) and difficulty proliferate (hypersalinity and highly alkaline medium,
in extrapolating beyond 1000 m2.62 respectively). The second point limiting production in this
Notoriety of circular systems remained relatively low as they type of system is the input of inorganic carbon. Since these
were supplanted by basins called raceways because of their systems are in contact with air (containing very little CO2),
shape. Initially developed in the field of wastewater treatment the dissolved inorganic carbon in the basins will tend to
by Oswald and Goleuke (1967)63 and Benemann and Oswald equilibrate with the atmosphere (except in the case of highly
(1996),64 this technology consists in a loop (or sometimes alkaline pH). This difference in inorganic carbon
several interconnected loops) consisting of two straight zones concentration will induce desorption of the latter from the
and two turning zones (Fig. 5) in which a thin layer of basin into the ambient air, which may lead to a limitation in
microalgae culture (about 20 to 40 centimeters for industrial nutrients, which will tend to significantly reduce the
systems) is set in motion, usually by means of a paddle wheel.
A final type of open system was developed in the 1960s in
the Czech Republic, in Trebon66,67 The aim of this system is
Fig. 5 Raceway of 3000 m2 in NBT, Israël (https://www.israel21c.org/ Fig. 6 Inclined plane system (200 litres) developed in Trebon, Czech
wp-content/uploads/2016/02/algae-NBT.jpg)65 (this figure was Republic68 (original figure was published in J. R. F. Malapascua, C. G.
published in P. J. Harvey and A. Ben-Amotz, Algal Research, 2020, 50, Jerez, M. Sergejevová, F. L. Figueroa and J. Masojídek, Aquat Biol.,
102002, Copyright Elsevier). 2014, 22, 123–140, under the Creative Commons CC-BY License).
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Because of its ease of extrapolation, the tubular

photobioreactor is the most widely used system under solar
conditions.38,42,50,62,69,72,75–78 On this same basis of
construction, several alternatives can be distinguished
according to: (i) the mode of agitation (airlift or mechanical
by means of a pump), (ii) the regulation system (internal via
a concentric tube, external by immersing the tubes in a

swimming pool,76 by spraying water on the surface of the
tubes or without thermal regulation), (iii) the construction
material (PVC, PMMA, glass…), (iv) the type of construction
(PVC, PMMA, glass…). One of the most world's largest closed
tubular PBR is in Klötze (Germany) and operated by
Fig. 7 Cascade of inclined plane photobioreactor of A4F in Pataias, Roquette. The system consists of 20 independent modules
Portugal (reproduced with the permission of A4F company, www.a4f.pt).
with a total volume of about 600 m3 with 500 km of glass
tubes arranged in a 1.2 hectare greenhouse (Fig. 8).
Alga Technologies, Ltd, based in Israel, the world leader in
maximum performance of the reactor in terms of the production of naturally occurring astaxanthin has also
productivity. Some performance data for Chlorella vulgaris are chosen tubular PBR. Microalgae are cultivated in 300 kilometres
reported in the following table for different culture of tubes on a production area of more than one hectare.79
technologies (Table 1). As regards flat systems, although often considered to be
The results presented in Table 1 are for the most part more efficient78 due to ease of light attenuation
maximum productivities obtained during the summer management, they are more complicated to scale up than
periods. Tredici (2003)72 estimates that the average annual tubes, due in particular to their lower resistance to
surface productivity of any open basin is around 40 t ha−1 per hydrostatic pressure. Nevertheless, research on this geometry
year. An annual culture of the cyanobacterium A. platensis has led to the marketing of various industrial production
has been carried out in Spain,73 with an annual surface systems. This is the case of the Green Wall Panels developed
productivity of 30 t ha−1 per year. In their report, Benemann by Tredici et al. (2015),80 the second version of which is now
and Oswald (1994)64 reduce the crop yield in temperate zones on the market (Fig. 9).
to 10–20 t ha−1 per year, which is confirmed by an experiment Other vertical PBRs are marketed by the German company
carried out by Tredici over several years obtaining a Subitec. These have a variable thickness depending on the
productivity on Spirulina of 20 t ha−1 per year.74 height in order to promote mixing. There are also, on the
same principle as the submerged tubular system, two types
of planar systems sold respectively by Proviron81 and Solix,82
Closed industrial systems in which airlift planar PBRs are immersed in a layer of water
to increase the thermal inertia of the cultivation system.
Photobioreactors have many advantages over open ponds: (i) The GICON® Photobioreactor, also called the Christmas
contamination can be controlled because there is no contact tree reactor due to its truncated conical shape, was designed
with outside, so it is sufficient to sterilize the PBR before for providing optimum light supply thanks to its geometry.
cultivation; (ii) desorption is also limited because of the low Self-shading of algae could be prevented, depending on the
exchange with the ambient air, which avoids the risk of biomass concentration obtained in the culture system, and
carbon limitation; (iii) water consumption is low compared light incidence could be maximized by allowing variable
to open systems because evaporation is almost nil. There are angles of radiation.
many types of closed PBRs, and these culture systems will be
presented in three categories: (i) conventional systems with
artificial lighting, (ii) conventional systems with solar lighting PBRs under development
(pilot or large-scale) and (iii) breakthrough systems (at the A new tubular photobioreactor design based on the Fibonacci
development stage). equation is proposed by Diaz et al. (2019).83 The idea is to
Table 1 Surface productivity of C. vulgaris in open culture systems
Culture system Surface productivity (t ha−1 per year) Ref.

Lagoon 3.6 Richmond and Hu (2013)29
Raceway 43–47 Richmond and Hu (2013)29
Raceway/circular 36–91 Pulz (2001)69
Cascade 40–84 Doucha and Lívanský (2006)70
Cascade 91 Chen (2009)71
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Fig. 8 Tubular photobioreactor in greenhouse in Klötze, Germany69

(agreement from Springer Nature in the framework of Copyright
Clearance Center).
Fig. 10 Scheme of the Fibonacci-type tubular photobioreactor83 (this

mimic plants, which develop varied leaf distribution
figure was published in J. P. Diaz, C. Inistrosa and F. G. Acien
geometries to optimize light absorption. Fibonacci-type Fernandez, Process Biochemistry, 2019, 86, 1–8, Copyright Elsevier).
tubular photobioreactor is based on a helical spiral and could
be considered as artificial photosynthetic trees (Fig. 10). The
design of the PBR allows up to a 1.4-times increase in
intercepted solar radiation with respect to that received on a concentrations up to 100 times higher than in a raceway-type
horizontal surface. PBR, for the same productivity on the illumination area. This
SunOleo firm develops photobioreactors, which are simple can be achieved by reducing the thickness of the culture,
tanks with immersed inflatable light wells, which bring which increases the ratio of illumination area to culture
sunlight up to 6 m deep in the tanks (Fig. 11) and volume. This PBR works on the principle of a falling film
theoretically allow to increase surfacic productivity with with small inclination angle, making it possible to obtain a
respect of raceway ponds. culture thickness of 1.5 mm. The culture of microalgae on
Photobioreactor technology is still evolving. In order to biofilm is also one of the solutions to reduce the amount of
reduce consumption (especially water consumption) and water used.85–87 Indeed, microalgae are fixed and grow on a
increase the efficiency of photosynthesis in photobioreactors, support, nutrients are then provided by immersing this film
new cultivation systems currently under development could in water supplemented with minerals essential to the growth
be the conventional technologies of tomorrow. This is the of microalgae. Although this process consumes little water
case of the Algofilm photobioreactor.84 This system is an and energy for harvesting, it is difficult to manage the light
intensified photobioreactor, as it allows biomass attenuation in a film of immobilized microalgae and
therefore to optimize productivity. Cornet88,112 has developed
a PBR called DiCoFluV (Solar Flux Volume Controlled
Dilution) based on the dilution of the luminous flux in the
culture volume. Based on the principle that the efficiency of
photosynthesis is inversely proportional to the luminous flux
captured, they have developed a culture system in which a
sheath of optical fibres brings energy to the culture. The aim
is to reduce the luminous flux sent to the culture for the
same overall amount of energy supplied to the system. This
principle makes it possible to approach the maximum
thermodynamic limit of conversion of light energy into
biomass through photosynthesis.
PRIAM (Internal Radiation Photobioreactor and Modular
Layout) photobioreactor, which was patented by the CNRS –
ENSCCF University of Nantes,89 is based on the principle of
Fig. 9 PBR green wall panels in Siesto Fiorentino, Italie80 (this figure
was published in M. R. Tredici, N. Bassi, M. Prussi, N. Biondi, L. Rodolfi,
internal lighting by flat panels, these panels delimiting
G. Chini Zittelli and G. Sampietro, Applied Energy, 2015, volumes of culture whose repetition allows, in a design
154(September), 1103–1111, Copyright Elsevier). mode close to the filter press, to extrapolate in volume by
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Fig. 11 SunOleo photobioreactor (with the kind permission of the company SunOleo).
simply increasing the number of panels (Fig. 12). This observed. The parameters of the model are adjusted for
conception brings many advantages on key points in the each case, but are not necessarily representative of the
culture of photosynthetic microorganisms, namely (i) an physical, chemical or biological reactions that take place.
optimised contribution of light within the culture itself, The most widely used are those of Monod (1942)90 and
with thus an optimal exploitation of the photons emitted, Andrews–Haldane.91 Monod's model is commonly used to
(ii) a design limiting the risks of adhesion on the lighting describe bacterial growth. This model is based on the
structures, easily dismantled and facilitating cleaning, and assumptions that the yield of growth (in g of biomass per
(iii) a modular production that can be simply extrapolated g of substrate) of conversion of a given substrate
in volume while maintaining constant surface and volume (concentration of this substrate noted S, in g l−1) into
productivity. biomass remains constant over time, and that the
New types of photobioreactor with a coupling between a evolution the specific growth rate (μ, in h−1) with the
photobioreactor and a photovoltaic cell are currently in evolution of the substrate concentration considered follows
development.115,116 A pilot-scale spectrally-selective, a hyperbolic trend:
insulated-glazed photovoltaic flat plate photobioreactor was
developed with an infrared reflecting system embedded in μ = μmaxS/(KS + S) (2)
the illumination surface for the thermal regulation of
outdoor photobioreactors. The interest is to produce both where μmax is the maximum specific growth rate and KS
microalgal biomass and electricity and to increase the net represents the half-saturation constant of the microorganism
energy ratio.117 with respect to the substrate under consideration. This
constant is dependent on the microorganism and its culture
Modelling of the PBR conditions, which express the affinity of the microorganism
to the substrate. A limitation of the Monod model is the non-
Growth models inclusion of the inhibitor effect of a substrate present in
The overall approach generally consists of a mathematical excess. The Andrews–Haldane model91 introduced a term for
law that correctly translates the experimental behaviour the substrate inhibition:
μ = μmaxS/(K1 + S + S2/K2) − μm (3)
where μ is the specific growth rate, in h−1, μmax the

maximum specific growth rate, in h−1, S the substrate
concentration in the extracellular medium, in g l−1 or mol l−1,
K1 the limiting constant, in g l−1 or mol l−1, K2 the inhibition
constant, in g l−1 or mol l−1. The term μm corresponds to the
term maintenance of microorganisms (respiration), which
allows access to the negative values of biomass productivity
observed for low substrate values. As for the Monod model,
the modeling of the growth of photosynthetic
microorganisms photolimited by the Andrews–Haldane
Fig. 12 PRIAM (internal radiation photobioreactor and modular layout)
model will be done by replacing the substrate, S, by
photobioreactor prototype patented by CNRS – University of Nantes89 irradiance, G, for local values of growth rate, or an averaged
(with courtesy of GEPEA laboratory – UMR CNRS 6144). value, Gmoy, over the whole photon flux culture for an average
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value of the growth rate. The type of model is often used for metabolism in response to changes in the illumination
the good approximation of the experimental behaviours,92,93 conditions. Current state of the art of constraint-based
although its formulation is problematic in the case of modeling and computational method development are
photosynthetic microorganisms. There is thus no discussed by Tibocha-Bonilla et al. (2018).100
proportionality between respiration and luminous intensity.94 Light attenuation modelling. Light attenuation can be
Some approaches are based on artificial intelligence with represented by the Beer–Lambert equation using an
deep learning technology and data-driven surrogate modeling extinction coefficient representing the biomass absorption
framework.95 A stochastic optimization algorithm was used coefficient.101 Beer–Lambert's law is a relatively simple law
in order to develop models from hydrodynamic and allowing to model correctly the exponential attenuation of
biochemical kinetic results to optimise biosystems and monochromatic radiation through a homogeneous medium,
obtain decision-making for choosing the best parameters for absorbent and non-diffusive. It is a law which is very widely
microalgae production. used in spectrophotometry, especially for the determination
of chemical species in solution. This law does not take into
account the phenomena of radiation diffusion. Its simplicity
Predictive models of use means that this law, even if it neglects an important
A dynamic semi-predictive model for microalgal culture in phenomenon, namely diffusion, is still widely used for
tubular photobioreactor have been developed by Fernández modeling, in the first instance, the approximation, light
et al. (2014).18 The model is based on a photosynthesis rate transfer to PBR.101–104
equation taking into account light intensity and the others However, this model does not take into account the effects
most important variables (temperature, pH, and dissolved of light scattering by microalgae. For this reason, Cornet
oxygen) that influence the growth and performance of the et al. (1992, 1995)97,105 used a different approach to
culture in any microalgal production system. The accurately describe light attenuation in a photobioreactor. By
thermodynamic approach of the irreversible processes was adapting Schuster's (1905)106 model describing the behaviour
applied by Stucki (1978)96 to describe the biological of light in a foggy atmosphere, the proposed radiative
reactions observed in microorganism cultures. This transfer model describes light attenuation by taking into
approach consists in considering that, in a complex account light absorption by pigments and light scattering
biological process such as photosynthesis, the average state throughout the cell. The assumptions are as follows: the
of the measured reactions (not thermodynamically stable in medium is assumed to be absorbing, scattering and non-
instantaneous value, due to the autocatalytic steps of fluorescent. Therefore, it is sufficient to determine three
enzyme activation and inhibition) is stable on a parameters to characterize the light path: the mass
appropriated time scale.97 Cornet's analysis of the Z-scheme coefficient of light absorption (Eaλ in m2 kg−1), the mass
of photosynthesis has led to the establishment of a growth coefficient of scattering (Esλ in m2 kg−1) and the coefficient
model, which was compared with experiments on cultures of backscattering (b2λ, without unit). When this model
of two microorganisms: Arthrospira platensis and considers the light attenuation as monodirectional (on the
Rhodospirillaceae sp.10,98 This predictive method requires a z-axis), it is called a two-flux model, and takes into account
high degree of theoretical knowledge, since it is based on the propagation of light, for a given wavelength (in nm) along
the precise analysis of the major phenomena governing the z-axis and in two opposite directions, Iλ+ and Iλ−.97 The
growth, as the energetics of photosynthetic conversion, sum of these two specific intensities gives the local irradiance
anabolism and catabolism. G (eqn (4)):
Flux metabolic modeling. Metabolic flux analysis allows ðð
the modeling of intracellular metabolism in response to Gλ ¼ I λ dω ¼ I λ þ þ I λ − (4)
4π
genetic and/or environmental variations in a system
biological. All modeling is based on the reconstruction of a
where dω represents the solid angle defining a radiation
metabolic network associating each reaction involved for the
beam. The system of differential equations to be solved as a
conversion of a given substrate into products of interest.
function of culture depth is as follows:
Cogne et al. (2003)99 established the metabolic network of
autotrophic growth of Arthrospira platensis; 121 reactions dI λ þ
¼ −Eaλ ·CX ·I λ þ − Esλ ·b̄ 2λ ·CX ·ðI λ þ þ I λ − Þ (5)
associated with 134 metabolites made it possible to dz
reconstruct a metabolic network linked to the production of
C-phycocyanin. Cogne et al. (2011),48 based on two dI λ −
computational approaches of metabolic flux, modeled of the ¼ −Eaλ ·CX ·I λ − − Esλ ·b̄ 2λ ·CX ·ðI λ− þ I λ þ Þ (6)
dz
behavior of the eukaryotic microalgae Chlamydomonas
reinhardtii grown under photoautotrophic conditions. The The boundary conditions for a planar system, illuminated by
reconstruction of a metabolic network comprising 280 a collimated light source at normal incidence, having a rear
metabolic reactions linked to 278 metabolites was carried out. face of reflectivity ρ are as follows (qλ,0 is the surface incident
The study was able to demonstrate a reorientation of flux of the PBR):
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(
z ¼ 0; I λ þ ¼ qλ;0 and 10 times the wavelength of the received radiation. To
− þ
(7) solve these equations, the following parameters are
z ¼ L; I λ ¼ ρI λ
required:107,108 (i) the complex refractive index of the
Finally, the expression of irradiance as a function of the particle mλ, (ii) its size, and (iii) the refractive index of the
thickness of a planar PBR is given by Pottier et al. 2005:107 medium surrounding the particles nm,λ. The complex

Gλ ðzÞ ρð1 þ α λ Þe−δλ L − ð1 − α λ Þe−δλ L eδλ z þ ð1 þ α λ Þeδλ L − ρð1 − α λ Þeδλ L e−δλ z

¼2 (8)
qλ;0 ð1 þ α λ Þ2 eδλ L − ð1 − α λ Þ2 e−δλ L − ρð1 − α λ 2 Þeδλ L þ ρð1 − α λ 2 Þe−δλ L
(8)
refractive index of the microorganism is composed of two
with:
rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi parts (eqn (13)): the first real part nλ represents the
Eaλ scattering part of the index,107 and the second κλ complex
αλ ¼ (9)
Eaλ þ 2b̄ 2λ ·Esλ part represents the absorption part of the index and is
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi strongly wavelength-dependent.107
δλ ¼ C X Eaλ ðEaλ þ 2b̄ 2λ ·Esλ Þ (10)
mλ = nλ + iκλ (16)
The coefficients αλ and δλ are referred to as linear diffusion
modulus and extinction coefficient, respectively. Pruvost and The determination of the complex index is based on the
Cornet (2012)24 modelled the light attenuation of an PBR under absorption properties of the pure pigments as well as their
solar illumination, distinguishing between the collimated (q//) proportion in the cell and the index of the refractive anchor
and diffuse (q∩) parts of the luminous flux and taking into point. Once the characteristics of the light radiation have
account the angle of inclination of the PBR (noted β) and the been determined (absorption, scattering and phase function
angle between the position of the sun and the normal to the per cell), they are converted into mass coefficients using the
PBR (noted β). This leads to the following equations: biomass water fraction xw, the density of the dry biomass and
the Sauter D32 diameter.108 Considering that the microalga
behaves like a double concentric sphere, Kandilian (2016)108
GcolðzÞ 2 ð1 þ α Þe−δcol ðz−LÞ − ð1 − α Þeδcol ðz−LÞ
¼ (11) was able to determine the radiative properties of the
q== cos θ ð1 þ α Þ2 eδcol L − ð1 − α Þ2 e −δcol L
microalga Chlorella vulgaris as a function of its pigmentary
material and compare them with experimental values
Gdif ðzÞ ð1 þ α Þe−δdif ðz−LÞ − ð1 − α Þeδdif ðz−LÞ obtained using an integrating sphere spectrophotometer.
¼4 (12)
q∩ ð1 þ α Þ2 eδdif L − ð1 − α Þ2 e−δdif L
with Characterization of the amount of light absorbed by microalgae
αCX As previously mentioned, irradiance G is the parameter used

δcol ¼ ðEa þ 2b·EsÞ (13) to characterize the local growth of a microalgae culture. It
cos θ
represents the photon flux available locally but does not give
δdif = 2αCX(Ea + 2b·Es) (14) information on the flux absorbed by the microalgae. Indeed,
depending on its shape, size or pigmentary material,
The local irradiance is then determined by: microalgae will absorb the available light differently. To
characterize the behavior of a microalgae culture it is
G(z) = Gcol(z) + Gdif(z) (15) important to analyse in terms of absorbed flux and not in
terms of available flux. This has already been done in the
In order to locally determine the amount of light absorbed by literature to characterize growth in an PBR or the production
the microalgae, it is necessary to know the biomass of metabolites.20,109,110 The photon absorption rate can then
concentration (CX), the intensity and spectrum of the light be studied per unit mass of microalgae and called MRPA
source and the optical properties of the microorganism (mean rate of photons absorption, noted in μmol kg−1 s−1),
under study. noted <>. Mass absorption cross section (Ea) (m2 kg−1)
enable to convert irradiance to rate of photon absorption.
Kandilian108,110 showed, for several strains, that mass
Radiation properties of microalgae absorption cross section is linearly linked to the pigment
Radiation properties are necessary to determine the content in the microalgal biomass. MRPA represents the
radiation field. The determination of the radiative properties specific rate of conversion of photons into biomass and takes
of microalgae can be carried out using the Lorenz–Mie into account: the light flux received at the surface, the
solution, a theory of light diffraction using Maxwell's pigment composition as well as the biomass concentration.
equations, and applying to spherical particles between 0.1 Its expression, in the case of a planar PBR, is as follows:
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ðL ðL J O2 C X M X
1 1 — rX ¼
hi ¼ ¼ EaGðzÞdz (17) (22)
L 0 L 0
vO2 –X
The MRPA can also be determined by carrying out a balance where MX and vO2–X represent, respectively, the C-molar mass of
on the photonic phase in the reactor volume.109 the biomass (kgX mol−1) and the stoichiometric coefficient of
S as oxygen production. In the reactor volume (VR), the MRPA value,
hi ¼ q0 − qL ¼ q0 − qL (18)
A, obtained from the radiative transfer model (eqn (14)–(16)),

VCX CX
changes as the light attenuates. The average volumetric velocity
where as represents the specific surface area of the PBR, i.e. is then calculated by integrating the local volumetric growth
the ratio between the illuminated surface area and the rate over the reactor volume:
volume of the PBR (in m−1), q0 and qL represent the photon ððð
1
flux density (PFD) at the input and output of the system, hr X i ¼ r X dV (23)
VR
respectively. When the entire light flux is absorbed in the VR
PBR, this expression can be summed up to:
In a photobioreactor, the balance equation giving the temporal
q as evolution of growth as a function of time is written:
hi ≃ 0 (19)
CX dCX
¼ −D·CX þ hr X i (24)
Note that the latter relationship is particularly interesting. dt
Following this parameter in dynamic conditions becomes
Solving this equation predicts the volume productivity of the
indeed trivial. It is sufficient to know the flux received at the
PBR:
surface of PBR (via a weather station for example), the
—
biomass concentration (by measuring the dried biomass) and P X ¼ hr X i ¼ D·CX (25)
the culture thickness.
where D is the dilution ratio of the photobioreactor (in h−1),
related to the passage time τp and the biomass outflow rate Qs by:
Engineering factors driving PBR productivity
1 Q
When all parameters are kept at the optimum operating level, D¼ ¼ s (26)
τp V R
the output depends solely on the amount of light absorbed.
Pruvost et al. (2015)111 modelled the growth of microalgae The productivity of a PBR for a given strain depends, as
under these conditions based on their biological and optical mentioned above, on many parameters (temperature,
properties. Locally, the specific oxygen production rate JO2 (in agitation, light attenuation…). Maximum performance for a
molO2 kg−1 s−1) is determined by the equation: given strain is therefore reached when all these parameters

K· J Kr are maintained at the optimum and the entire light flux is
J O2 ¼ ρM ϕ O̅ ′ 2 − NADH2 (20) absorbed in the culture without the appearance of dark zones
K þ  vNADH2 –O2 K r þ 
(luminostat regime). In order to determine the maximum
where ρM represents the maximum photon conversion performance of a photobioreactor under constant incident
efficiency, ϕ O̅ ′ 2 the molar quantum oxygen efficiency of the Z flux, Takache et al. (2010)45 proposed a simplified
scheme of photosynthesis (in molO2 μmol−1), K the half- engineering law for PBR sizing:
saturation constant of photosynthesis (in μmol kg−1 s−1), Kr the
——– — 2α K q Ea
saturation constant describing respiration to light (in μmol SX max ¼ ρMϕ X ln 1 þ 0 (27)
1 þ α Ea K
kg−1 s−1), JNADH2 the specific rate of regeneration of respiratory
chain co-factors (in molNADH2 kg−1 s−1) and νNADH2–O2 the When growing microalgae under solar conditions the
stoichiometric coefficient of regeneration of respiratory chain formula becomes.112

——– — 2α χ̅ d K 2q Ea –—— K q Ea
SX max ¼ 1 − f d ρMϕ X ln 1 þ 0 þ ð1 − χ̅ d Þ cos θ ln 1 þ –0—— (28)
1 þ α 2Ea K Ea K cos θ
where fd is the dark fraction of the reactor, θ the angle

co-factors. Each parameter depends on the microalgae growth.
formed between the position of the sun and the normal with
The saturation constant Kr is dependent on the rest of the
respect to the PBR and x̄d is the diffuse fraction of the
parameters of the kinetic model by the equation:
incident flux. In addition, the volume productivity of a PBR is
related to the area productivity by the specific surface area of
c
Kr ¼ h i (21) the PBR (as):
J NADH2 1
þ K1 − 1 — —
vNADH2–O2 ρM ϕ ̅O′ Ea C
2
P X ¼ a s SX (29)
The latter equation emphasizes the independence of the

The volumetric local growth rate rX (in kgX m−3 s−1) is related to production potential of a PBR from its geometry. Thus, the
the specific rate of oxygen production JO2 by the formula: larger the specific surface area of the photobioreactor, the
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or g l−1 h−1) increases with decreasing culture thickness (as =

S/VR = 1/L). This results in a reduction in the costs of
circulating the culture and post-treatment of the biomass,
hence the growing interest in PBR with high volumic
productivity. The model for the volumic productivity (eqn (27)
and (29)) has been tested for the cultivation of Arthrospira
platensis.10 A deviation of less than 15% was observed,10

despite the different growing conditions: batch and
continuous conditions, annular, cylindrical and plate
photobioreactors. The same model was used to predict with an
average relative error less than 10% (Fig. 13) the productivity
of Chlorella vulgaris for two light sources from a LED panel,
white LED with mean emissive wavelength at around 440 nm
and red LED (maximum emissive peak at 660 nm).113
The engineering factor are also very useful to scale-up the
Fig. 13 Comparison between experimental data and theoretical biomass productivity in photobioreactors of different sizes
predictions for C. vulgaris under white (experimental: black points; (Fig. 14). The labscale PBR has a volume of 1 l and a thickness
theoretical: black dashed line) and red (experimental: red points;
theoretical: red dashed line) radiations of volumetric productivity.
of 3 cm and the pilot scale PBR a volume of 130 l and a
thickness of 5.5 cm. A cultivation of Neochloris oleoabundans
was made in the two PBR for two values of the incident PFD.24
higher the volume productivity will be and in the case of a A maximal deviation of 15% was found for the prediction
planar system, the maximum volume productivity (kgX m−3 d−1 of biomass productivity as a function of PBR geometry and
Fig. 14 Comparison of the volumic productivity in PBR of different sizes and comparison the model of eqn (27)–(29) with for Neochloris
oleoabundans: ρM = 0.8, φM = 1.83 × 10−9 kg per μmole, K = 90 μmole per m2 s−1.
View Article Online
PFD. The positive effect of increasing the PFD on biomass 12 L. Brennan and P. Owende, Renewable Sustainable Energy
productivity and the negative effect of increasing the depth of Rev., 2010, 14, 557–577.
culture can be seen. 13 S. Taras and A. Woinaroschy, Comput. Chem. Eng., 2012, 43,
10–22.
Conclusion 14 G. A. Ifrim, M. Titica, M. Barbu, L. Boillereaux, G. Cogne, S.
Caraman and J. Legrand, Chem. Eng. J., 2013, 218, 191–203.
The development of microalgae culture processes requires
15 A. S. Kumar and Z. Ahmad, Chem. Eng. Commun.,

knowledge of their physiology, and more particularly their 2012, 199, 472–511.
ability to capture light and the associated metabolism, and 16 S. Oblak and I. Škrjanc, Chem. Eng. Sci., 2010, 65,
their behaviour according to the experimental conditions, in 1720–1728.
particular the limiting factors. The growth of photosynthetic 17 P. D. Christofides, R. Scattolini, D. M. de la Peña and J. Liu,
microorganisms is a complex process, affected by many Comput. Chem. Eng., 2013, 51, 21–41.
environmental factors such as light, mixing, gas–liquid 18 I. Fernández, F. Acién, M. Berenguel and J. L. Guzmán, Ind.
transfer, temperature, and pH. Depending on the use, different Eng. Chem. Res., 2014, 53, 11121–11136.
types of photobioreactor have been designed. For laboratory 19 C. M. Pires, M. C. M. Alvim-Ferraz and F. G. Martins,
studies, photobioreactors must be designed to control the Renewable Sustainable Energy Rev., 2017, 79, 248–254.
various parameters that influence biomass productivity as well 20 J.-F. Cornet, C. G. Dussap and J.-B. Gros, Bioprocess and
as possible. The results obtained in perfectly controlled Algae Reactor Technology, Apoptosis, Advances in
conditions are essential for modelling culture systems in order Biochemical Engineering Biotechnology, Springer Berlin
to predict their productivity. No perfect type of PBR exists for Heidelberg, 1998, vol. 59, pp. 153–224.
the mass cultivation of microalgae, because of the need to 21 M. J. de Mendonça Fragata and V. Viruvuru, Photosynth.
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In this article, some examples of photobioreactors, open 22 L. Gouveia, Microalgae as a Feedstock for Biofuels, Springer,
systems to the atmosphere, or closed systems with a culture 2011.
confined in the photobioreactor, are described. The different 23 H. Takache, J. Pruvost and J.-F. Cornet, Biotechnol. Prog.,
modelling approaches were discussed, distinguishing between 2012, 28, 681–692.
models based on parameters fitted from experiments and 24 J. Pruvost and J.-F. Cornet, Microalgal Biotechnology:
predictive models that take into account radiative models to Potential and Production, De Gruyter, Berlin, Germany, 2012,
predict the distribution of light in photobioreactors. pp. 181–224.
25 J. A. Raven and R. J. Geider, New Phytol., 1988, 110(4),
Conflicts of interest 441–461.
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Reaction

A review on photobioreactor design and

Introduction a wide range of applications. Large-scale cultivation of

Review Reaction Chemistry & Engineering

Reaction Chemistry & Engineering Review

Review Reaction Chemistry & Engineering

Reaction Chemistry & Engineering Review

Review Reaction Chemistry & Engineering

Mixing and microalgal growth Design of photobioreactors

Reaction Chemistry & Engineering Review

Fig. 3 EOSS-PBR (with courtesy of GEPEA laboratory – UMR CNRS 6144).

parallel (Fig. 3). Each column has a volume of 30 ml and

Review Reaction Chemistry & Engineering

Reaction Chemistry & Engineering Review

Because of its ease of extrapolation, the tubular

a concentric tube, external by immersing the tubes in a

Table 1 Surface productivity of C. vulgaris in open culture systems

Culture system Surface productivity (t ha−1 per year) Ref.

Review Reaction Chemistry & Engineering

Fig. 8 Tubular photobioreactor in greenhouse in Klötze, Germany69

Fig. 10 Scheme of the Fibonacci-type tubular photobioreactor83 (this

Reaction Chemistry & Engineering Review

μ = μmaxS/(K1 + S + S2/K2) − μm (3)

where μ is the specific growth rate, in h−1, μmax the

Review Reaction Chemistry & Engineering

Reaction Chemistry & Engineering Review

Gλ ðzÞ ρð1 þ α λ Þe−δλ L − ð1 − α λ Þe−δλ L eδλ z þ ð1 þ α λ Þeδλ L − ρð1 − α λ Þeδλ L e−δλ z

with Characterization of the amount of light absorbed by microalgae

αCX As previously mentioned, irradiance G is the parameter used

Review Reaction Chemistry & Engineering

A, obtained from the radiative transfer model (eqn (14)–(16)),

where fd is the dark fraction of the reactor, θ the angle

The latter equation emphasizes the independence of the

Reaction Chemistry & Engineering Review

or g l−1 h−1) increases with decreasing culture thickness (as =

platensis.10 A deviation of less than 15% was observed,10

Review Reaction Chemistry & Engineering

15 A. S. Kumar and Z. Ahmad, Chem. Eng. Commun.,

Reaction Chemistry & Engineering Review

Review Reaction Chemistry & Engineering

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