تأثير المعادن الثقيلة

Chemosphere 332 (2023) 138861
Contents lists available at ScienceDirect
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
Biological and green remediation of heavy metal contaminated water and

soils: A state-of-the-art review
Aniruddha Sarker a, Md Abdullah Al Masud b, Deen Mohammad Deepo c, Kallol Das d,
Rakhi Nandi e, Most Waheda Rahman Ansary f, Abu Reza Md Towfiqul Islam g, h, **,
Tofazzal Islam f, *
a
Residual Chemical Assessment Division, National Institute of Agricultural Sciences, Rural Development Administration, Jeollabuk-do 55365, Republic of Korea
b
School of Architecture, Civil, Environmental and Energy Engineering, Kyungpook National University, Daegu 41566, Republic of Korea
c
Department of Horticultural Science, Kyungpook National University, Daegu 41566, Republic of Korea
d
College of Agriculture and Life Sciences, Kyungpook National University, Daegu 41566, Republic of Korea
e
Bangladesh Academy for Rural Development (BARD), Kotbari, Cumilla, Bangladesh
f
Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh
g
Department of Disaster Management, Begum Rokeya University, Rangpur 5400, Bangladesh
h
Department of Development Studies, Daffodil International University, Dhaka 1216, Bangladesh
H I G H L I G H T S G R A P H I C A L A B S T R A C T
• Heavy metal (HM) reclamation using

green and biological methods was criti
cally summarized.
• Elite microbes and plant species were
reported as key drivers in HM
decontamination.
• Combining approaches supersedes over
single remediation strategy for HM
reclamation.
• The underlying mechanism and research
bottlenecks of HM bioremediation were
explored.
• Bioengineering of microbes and plants
improves the scale and speed of HM
remediation.
A R T I C L E I N F O A B S T R A C T
Handling Editor: Lena Q. Ma Contamination of the natural ecosystem by heavy metals, organic pollutants, and hazardous waste severely
impacts on health and survival of humans, animals, plants, and microorganisms. Diverse chemical and physical
Keywords: treatments are employed in many countries, however, the acceptance of these treatments are usually poor
Heavy metals because of taking longer time, high cost, and ineffectiveness in contaminated areas with a very high level of
Bioremediation
metal contents. Bioremediation is an eco-friendly and efficient method of reclaiming contaminated soils and
Phytoremediation
waters with heavy metals through biological mechanisms using potential microorganisms and plant species.
Mechanism
Research bottleneck Considering the high efficacy, low cost, and abundant availability of biological materials, particularly bacteria,
algae, yeasts, and fungi, either in natural or genetically engineered (GE) form, bioremediation is receiving high
attention for heavy metal removal. This report comprehensively reviews and critically discusses the biological
* Corresponding author.
** Corresponding author.
E-mail addresses: towfiq_dm@brur.ac.bd (A.R.M.T. Islam), tofazzalislam@bsmrau.edu.bd (T. Islam).
https://doi.org/10.1016/j.chemosphere.2023.138861
Received 11 April 2023; Received in revised form 29 April 2023; Accepted 5 May 2023
Available online 5 May 2023
0045-6535/© 2023 Elsevier Ltd. All rights reserved.
A. Sarker et al. Chemosphere 332 (2023) 138861
and green remediation tactics, contemporary technological advances, and their principal applications either in-
situ or ex-situ for the remediation of heavy metal contamination in soil and water. A modified PRISMA review
protocol is adapted to critically assess the existing research gaps in heavy metals remediation using green and
biological drivers. This study pioneers a schematic illustration of the underlying mechanisms of heavy metal
bioremediation. Precisely, it pinpoints the research bottleneck during its real-world application as a low-cost and
sustainable technology.
1. Introduction combating HM pollution in aquatic environments including wastewater

treatments (Igiri et al., 2018; Sreedevi et al., 2022). Besides, HM
Heavy metals (HM) are a group of naturally occurring elements that bioremediation by microorganisms has some pitfalls, which include the
come from the earth’s crust. However, HM can be released into the non-biodegradability of HM and sometimes the generation of hazardous
environment by human activities like industrial discharges, mining, and metabolites by bacteria (Igiri et al., 2018). Noticeably, phytor
agricultural activities (Sarwar et al., 2017; Sarker et al., 2022). The emediation and microbial bioremediation are two prominent green
concentration of heavy metals in soil, groundwater, and various water remediation strategies, which can be well accepted by the researcher
bodies is exceeding the acceptable limits in many countries as a result of and users due to multifaceted advantages including eco-friendly facile
unplanned urbanization, industrialization, population growth, and poor in-situ approach, and inexpensive methods for the surrounding envi
management policies leading to a hidden threat to the human food chain ronment (Sharma et al., 2021; Shen et al., 2022). In general, phytor
(Khalid et al., 2017; Rakib et al., 2022; Sarker et al., 2022). emediation is a robust green technology for the reclamation of
There are various innovative technologies have been used to reme HM-contaminated soils that may comprise vital mechanisms such as
diate heavy metal contaminations from soil and water, such as physical, phytoextraction, phytoaccumulation, phytostabilization, phytovolatili
chemical, and biological processes (Akhtar et al., 2020; Masud et al., zation, and phytodegradation (Sarwar et al., 2017; Bhat et al., 2022).
2023c). For example, HM has been removed using a variety of physical Similarly, microbial bioremediation was dominated by metal bio
techniques, such as soil washing, adsorption, photocatalysis, membrane sorption, bioaccumulation, biomineralization, bioprecipitaiton, and
filtration, granular activated carbon, and electrokinetic method (Wang bioleaching (Kour et al., 2021; Sreedevi et al., 2022). The inclusion of
and You, 2023; Wang et al., 2023; Zhao et al., 2023; Qi et al., 2023; Kim new species of phytoaccumulators, the merger of microbial bioremedi
et al., 2022; Liu et al., 2023). In general, those methods are relatively ation with phytoremediation, and the application of biotechnological
time-consuming and highly dependent on the physicochemical feature approaches including multi-omics can accelerate the process of sus
of the studied toxic metals. However, the most commonly used chemical tainable bioremediation both in soil and aquatic environments (Sarwar
methods for HM remediation involve ion exchange (Guan et al., 2022), et al., 2017; Khalid et al., 2017; Ojuederie and Babalola, 2017; Muthu
flocculation (Sun et al., 2020), coagulation (Shao et al., 2023), and saravanan et al., 2018; Sarma et al., 2021; Malik et al., 2022).
chemical precipitation (Matlock et al., 2002). On the other hand, A large body of literature discusses the application of biological
Advanced Oxidation Processes (AOPs) involve the use of powerful approaches for the remediation of heavy metals at both laboratory and
oxidizing agents to break down and remove contaminants (Masud et al., field conditions (Ojuederie and Babalola, 2017; Sarwar et al., 2017;
2023b). These processes can be applied to both organic and inorganic Shen et al., 2022). However, the studies concerning the comparative
pollutants, including heavy metals and emerging contaminants (Sarker advantages over traditional approaches for the remediation of HM are
et al., 2023). AOPs are highly effective at breaking down even the most limited. In fact, the sustainability of biological and green remediation of
stubborn pollutants and can achieve near-complete removal of heavy HM is still in research infancy. Additionally, the technical barriers
metals from contaminated water and soil. Several types of AOPs can be during field application and controversial mechanistic insights of plant-
used for heavy metal remediation, including ozonation (Chen and and microbe-based bioremediation have marked the vital research gap,
Chang, 2022), Fenton’s reagent (Masud et al., 2022a), Fenton-like pro which needs to be addressed. Considering the contemporary research
cesses (Masud et al., 2022b, 2023c), photo-Fenton’s reagent (Nidheesh advances in HM remediation and existing research bottlenecks, this re
et al., 2022), electrochemical oxidation (Yang et al., 2020), metal oxide view aims to decipher the sustainable remediation approaches for HM
as heterogeneous catalyst (Sarker et al., 2023), and photocatalysis decontamination using natural or eco-friendly methods. The specific
(Jiang et al., 2021; Huang et al., 2023). In the photocatalytic remedia objectives of this critical review are to (1) pinpoint the current research
tion process, the pair of positively charged hole (h+) and electron (e− ) gaps concerning HM remediation from the modified PRISMA-review
can, respectively migrate to the surface of the semiconductor to undergo derived outcomes; (2) shed light on mechanistic insights of HM reme
a series of oxidation and reduction reactions, which are embodied in the diation using green and biological drivers, (3) discuss the sustainability
conversion of different valence states in the treatment of heavy metals of HM decontamination by the merger of phyto-, bio-, and
(Gao and Meng, 2021; Guo et al., 2022). In the photocatalysis process, nano-remediation processes; and (4) suggest potential recommendations
the most important limiting factors are the high energy requirements of for further research expedition through biological and green
the incident light caused by the wide bandgap and the easy recombi approaches.
nation of photogenerated carriers (e− and h+). TiO2, the most typical
photocatalyst (Jiang et al., 2022), is expensive and difficult to control 2. Review methodology
and remediate at real contamination sites. Although these methods are
effective in removing heavy metals, the excessive use of chemicals This review systematically assembles the present trends, mechanistic
makes it harder to dispose of the sludge and sediments and increases the insights, and research updates concerning biological and environmen
risk of secondary pollution may limit the widespread applications tally friendly heavy metal remediation following the critical discussion
(Marques et al., 2009). for addressing the existing challenges and research bottlenecks. The
Consequently, biological remediation (e.g., plant-, and microbe- review narrative is sketched following the customized PRISMA review
based approaches) is found as one of the promising technologies used protocol for compiling peer-reviewed article archives (including original
to remediate the polluted environment using potential microbes or plant research and review studies) concerning biological and green remedia
species to detoxify the hazardous form of metals to their less harmful tion studies. According to the concept and objective of this critical
states (Goswami et al., 2022; Song et al., 2022). In particular, microbial assessment, the original PRISMA procedures were slightly modified.
bioremediation is considered a sustainable and cheap strategy for However, the basic steps of review data arrangements were screening
2
(including online database and respective websites), eligibility 2015). The abundance of manganese in the environment is relatively
(including accepting/excluding criteria), and inclusion (final screening high, and it is not considered to be a rare element. However, the con
and meta-analysis), respectively. Academic search engines such as Sci centration of manganese can vary widely depending on the specific
ence Direct, Web of Science, Google Scholar, Scopus, and respective location and source. High levels of manganese can be found in areas with
websites of reputed publishers were meticulously employed to collect a manganese mines or smelters, and exposure to these high levels can have
raw database of target review themes. The vital keywords including negative health effects on humans and other organisms (Loranger and
“bioremediation of heavy metals”, “phytoremediation of heavy metals”, Zayed, 1995). Mercury is produced naturally through volcanic erup
mechanism of heavy metal bioremediation”, “research gap of heavy tions, rock weathering, and ocean degassing. The release of Hg into the
metal bioremediation”, “advanced remediation of heavy metals”, and environment can also be facilitated by human activities including min
“mechanism of phytoremediation” were used during web surfing. To ing, the burning of fossil fuels, and waste disposal. Mercury can exist in
avoid the obsolete data/research findings of HM remediation, a ten-year different forms, including elemental mercury (Hg), inorganic mercury
timeframe (i.e., 2013–2022) was employed except for a few classical compounds (HgCl2), and organic mercury compounds (methylmercury,
references. In a nutshell, 418 publications (original and review study CH3Hg). Methylmercury is the type of mercury that is of particular
included) were initially gathered; after meticulous screening using the concern as it can accumulate in the food chain and potentially harm
inclusion-exclusion criteria of the review methodology, 184 articles human health (Gworek et al., 2020). Cobalt is widespread in the envi
were ultimately chosen. The articles that were ultimately chosen were ronment and is used to manufacture alloys. Co is found in abundance in
skimmed for crucial details and critically reviewed throughout the re flora, soil, rocks, and water. Considerable levels of cobalt often have no
view process. A prime goal of this review is to pinpoint the mechanistic deleterious effects, but large-scale environmental releases can be lethal
insights and research uncertainties of heavy metal remediation through (Leyssens et al., 2017). Copper is commonly found in rocks, soil, water,
biological and green remediation approaches. Thus, the eligible and and sediment. Natural processes including erosion, volcanic eruptions,
relevant articles were finally scrutinized. However, the irrelevant ones and rock weathering release Cu into the environment. Agriculture, in
were discarded due to non-accessibility, lack of key points, and invalid dustrial operations, and human activities such as mining cause copper to
web references (e.g., invalid doi links). The summary of this review be released into the environment. Copper can exist in different forms,
motivation focusing on the contemporary biological and green remedi including elemental copper (Cu), copper oxide (CuO), and copper sulfate
ation of heavy metals, their mechanistic insights, and research gaps (CuSO4). Both plants and animals need Cu as a nutrient, but high con
derived from the modified PRISMA is illustrated in the supplementary centrations of Cu in the environment can be toxic to some organisms and
file (Figs. S1 and S2). can potentially harm human health (Yamuna et al., 2023).
Zn is a noble metal in the surface layer. As a result of its function as a
3. Abundance and toxicity of heavy metals (HM) in the cofactor, it is connected to numerous enzyme reactions. Zinc toxicity is
environment influenced by the type and volume of exposure. The two main ways to
get zinc are through smelting and mining, which affect ecosystems as
3.1. Abundance of HM well as living organisms (Zhang et al., 2012).
In the environment, heavy metals are present naturally, but human 3.2. Toxicity effect HM on the human and plants
activities have significantly increased their levels. Lead (Pb) is a com
mon heavy metal that occurs in nature in relatively small amounts, In general, heavy metals (HM) can be classified as plant-essential and
which are released into the environment through the production and non-essential elements based on their necessity in plant nutrition. Non-
disposal of industrial products such as batteries, paints, and electronics. essential metals can pose a significant threat to human and plant
Manufacturing, mining, and the burning of fossil fuels are examples of physiology and even can be lethal while the scale of toxicity is higher
human activities that contribute to the ongoing rise in atmospheric lead (Rice et al., 2014; Samreen et al., 2017). In a nutshell, heavy metals are
levels (Loh et al., 2016). Cadmium (Cd) pollution in the aquatic envi metallic elements that may be toxic to living organisms, including
ronment is caused by absorptions, industrial waste, and surface runoff humans. The major toxicity may include deformation of reproductive
into soil and sediments (Hayat et al., 2019). Nickel (Ni) and chromium systems, kidney dysfunction, respiratory difficulties, hypertension, cell
(Cr) are naturally occurring elements found in the environment (Har mutation, lung cancer, and abdominal damage (Loh et al., 2016; O’Neal
asim et al., 2015). The average concentration of Cr in the earth’s crust is and Zheng, 2015; Rehman et al., 2018; Frisbie and Mitchell, 2022). In
about 100 parts per million (ppm) (US EPA). Cr exists in two oxidation addition, HM ions cause fatality in plants in three different ways: they
states: trivalent chromium (Cr III) and hexavalent chromium (Cr VI). displace necessary cations from binding sites, they produce reactive
Trivalent chromium is a vital nutrient for humans, whereas hexavalent oxygen species to generate oxidative stress, which tests antioxidant
chromium is a pernicious and carcinogenic compound (Coetzee et al., defenses, and they directly bind to carboxyl, histidyl, and thioyl groups
2020). The abundance of chromium in the environment varies on proteins to interact with proteins (Hezbullah et al., 2016; Pie
depending on the location and the specific form of chromium. In some trowska-Borek et al., 2020; Fakhar et al., 2022). The detailed toxicity of
areas, the concentrations of chromium can be elevated due to natural HM including a comprehensive table is available in the supplementary
geological processes or civilization. file (Section S1 and Table S1). The schematic illustration of the source,
In the lithosphere, arsenic is extensively spread and can be found in abundance, and toxicological impact of HM in humans and plants is
rocks, soil, water, air, and living organisms. Arsenic concentrations in presented below (Fig. 1).
soil and rock can range from less than 1.0 part per million (ppm) to
several thousand ppm (Masuda, 2018). The World Health Organization 4. Phytoremediation of HM in soil and water: a green and
(WHO) has set a guideline value for arsenic in drinking water of 10 μg/L. innovative clean-up strategy
However, in some parts of the world, including certain regions of Asia
(10–50 μg/L) (McCarty et al., 2011), South America (10 μg/L) (Bund Phytoremediation is the classical process of green remediation
schuh et al., 2021), and Africa (10–300 μg/L) (O’Neal and Zheng, 2015), technology for managing heavy metal (HM) contamination using po
arsenic concentrations in groundwater can be much higher than this tential hyperaccumulating plant species either in pristine forms or
guideline value, leading to significant health problems for local pop genetically modified (GM) species for enhanced performance (Mahar
ulations. Manganese (Mn) is the 12th most abundant element in the et al., 2016; Muthusaravanan et al., 2018; Bhat et al., 2022). This
lithosphere and has an abundance of 0.1%. Mn is found in many min remediation technique gains traction due to its facile in-situ application
erals, including pyrolusite, rhodonite, and braunite (O’Neal and Zheng, with comparatively less expensive inputs than contemporary physical
3
Fig. 1. Heavy metals abundance and toxicity on the humans/living organisms and plants.
and chemical remediation strategies for combating HM contamination addressing HM-contaminated sites.
(Muthusaravanan et al., 2018). In general, the hyperaccumulating Several lines of evidence suggest that Brassica species are effective
plants can tolerate a higher concentration of toxic metals and can uptake phytoextractors for the majority of toxic trace metals including cad
a considerable amount of HM from the contaminated soils (Sarwar et al., mium (Cd), chromium (Cr), copper (Cu), nickel (Ni), and zinc (Zn) in
2017). Several lines of evidence indicate that various plant species soils (Saraswat and Rai, 2009; Zhang et al., 2011). The examined heavy
including perennial plants, ornamental plants, and some species of metals were sequestered into the shoots of Brassica species without
bamboo have tolerance to high concentrations of HM (Bian et al., 2020; hampering the soil fertility and structural aggregates. However, the HM
Bhat et al., 2022). Besides, some of the aquatic macrophytes, halophytes, phyto-adsorption capacity of the studied plant species will be dependent
and saltmarshes are also hyperaccumulators in the aquatic environment on several factors including plant biomass, soil types, level of contami
suitable for remediation of HM contamination in waterways and nation, experimental phase, and rhizosphere interaction (Shen et al.,
wastewaters (Sakakibara et al., 2011; Shukla et al., 2012; Ali et al., 2022). In particular, the root exudate of hyperaccumulating plant spe
2020; Hossain et al., 2021). The current advancement of phytor cies, and soil chemical features (e.g., organic carbon, pH, and CEC) will
emediation for managing HM contamination is described in the affect the HM adsorption process (Ojuederie and Babalola, 2017; Bhat
following sections. et al., 2022). The transgenic Nicotiana tabacum can accumulate a sig
nificant amount of tested HMs (e.g., Cd, Cu, and Zn) in contaminated soil
than the naturally grown tobacco species due to improved root systems
4.1. Phytoremediation of HM – current advances
and greater biomass structures (Zhang et al., 2008). Similarly, the
enhanced potential of a genetically modified water lotus (Nelumbo
The application of hyperaccumulating plants for the removal of HM
nucifera) for phytoremediation of cadmium in the aquatic environment
from the contaminated sites was considered novel and cheap remedia
through overexpression of the NnPCS1 gene in the PCS enzyme system of
tion technology with an in-situ application approach (Ma et al., 2001;
transgenic Arabidopsis has been demonstrated (Liu et al. (2012).
Ojuederie and Babalola, 2017). Even though phytoremediation using
Although classical phytoremediation has been extensively reported
plant species with adsorption, sequestration, and uptake potential of HM
as a traditional plant-based remediation technique for sustainable
from the contaminated soils was an orthodox remediation technology,
mitigation of HM contamination in soil, the coupling of traditional
the sustainability of this cost-effective and green approach is still a
phytoremediation using phytoaccumulators with soil organic amend
matter of research interest in the field of environmental remediation of
ment (e.g., organic fertilizer, biochar, activated carbon) will expand the
pollutants including trace metals, pesticides, and related emerging
scale and efficiency of existing strategy (Sarwar et al., 2017; Bhat et al.,
contaminants both is soil and aquatic environments (Ma et al., 2001;
2022). In addition, the augmentation of commercial metal chelators,
Mahar et al., 2016; Muthusaravanan et al., 2018; Bhat et al., 2022; Shen
and surfactants will be a wondrous option for the enhancement of or
et al., 2022). A diversified plant species including ornamental plants,
thodox phytoremediation of HM-contaminated soils (Mahar et al., 2016;
saltmarsh, flowering species, and grass species could be utilized as the
Mishra et al., 2021). However, the extensive application of metal che
HM accumulating plant species both for in-situ and ex-situ remediation
lators may pose a threat to secondary pollution in the environment.
strategy for cleaning up the HM contaminated sites (Sarwar et al., 2017;
Nevertheless, the number of potential plant species is limited for phy
Rahman and Singh, 2020). In general, the HM-tolerant plant species in
toremediation both in soil and aquatic environment, while current
their natural system (i.e., without any genetic modification) were
advancement of phytoremediation for searching untapped research av
assessed using contaminated soil or water. However, genetic engineer
enues to explore diversified plant species including terrestrial, orna
ing for transgenic plants also is applied as a stable phytoaccumulators
mental, bamboo, and saltmarsh species have been documented by the
for HM bioremediation (Zhang et al., 2008; Liu et al., 2012). Due to the
earlier research groups (Ali et al., 2020; Bian et al., 2020; Hossain et al.,
simplicity of application, and inexpensiveness this plant-based biore
2021; Bhat et al., 2022). In recent years, potential microbes including
mediation is still a competitive green remediation approach as
rhizospheric bacteria, and plant growth promoting bacteria (PGPB) have
compared to advanced chemical and nanobioremediation techniques for
4
been employed for efficient removal or mitigation of HM contamination hyperaccumulators is a promising option for tackling HM contamination
for in-situ and ex-situ remediation approaches under terrestrial and in aquatic and wetland ecosystems (Shukla et al., 2012; Sruthi et al.,
aquatic environments (Verma and Kuila, 2019; Sharma et al., 2021; 2017; Hossain et al., 2021). The acceptance and sustainability of phy
Kour et al., 2021; Sreedevi et al., 2022). The coupling of those microbial toremediation are promising and contemporary due to its simplicity of
strategies with plant-based phytoremediation emerged as a ‘new phy application either in pot investigations or direct field applications.
toremediation’ approach with the enhancement of HM bioremediation
without hampering the surrounding environment (Bhat et al., 2022; 4.2. Underlying molecular mechanism of phytoremediation
Shen et al., 2022). Thus, combined bio-phytoremediation is considered a
feasible and sustainable approach for HM reclamation. The basic step of phytoremediation may include phytoaccumulation
The salient feature of phytoremediation of HM through potential through the root systems of the tested plant species following the
plant species derived from the previous research findings is presented in vascular transportation within the plant biomass through the root-shoot-
Table 1. According to the table, phytosequestration/phytoextraction, foliage uptake approach (Mani and Kumar, 2014). The plant species
phytostabilization, phytovolatilization, and phytodegradation are listed which is employed in the phytoremediation technology has a strong root
as vital processes for the green remediation of HM using potential plant architecture and enhanced biomass structure along with a hyper tolerant
species. The phytoremediation potential of HM by a diversified plant capacity of relatively higher concentration of toxic trace metals
species including terrestrial, aquatic, mangrove, saltmarsh, perennial (Muthusaravanan et al., 2018). A common metal stress mechanism is
grass, and ornamental plants are unveiled (Shukla et al., 2012; Khalid driven by the hyperaccumulating plant through robust adaptation of the
et al., 2017; Radziemska et al., 2017; Hossain et al., 2021; Khan et al., antioxidant system or enzyme interaction during the suppression of
2021; Yang et al., 2022). The selection of plant species and performance plant stress generated by the reactive oxygen species (ROS) derived from
of phytoremediation is hooked on the purpose, state of contamination, redox toxic metals (Sarwar et al., 2017; Shen et al., 2022). On the other
and experimental phase (Yang et al., 2022; Shen et al., 2022). Those hand, the non-redox toxic metals were adsorbed by the plant root and
kinds of phytoremediation are widely applied in agricultural and arable shoot system of tolerant plant species through gene expression. The
soils that are contaminated by toxic HM, by using vegetative structures graphic explanation of a well-explored mechanism concerning the
of selected plants including plant shoots, leaves, and roots (Mahar et al., phytoremediation of toxic heavy metals is presented in Fig. 2.
2016; Shen et al., 2022). Thus, the alternate name for phytoremediation Based on the illustration, the most common and widely explored
is agroremediation, or vegetative remediation. On the other hand, the mechanism of phytoremediation is ‘phytoextraction or phytoaccumu
application of aquatic macrophyte, saltmarsh, and aquatic lation’ where the uptakes of HM from the contaminated soil followed by
Table 1
Screened research summary concerning phytoremediation of heavy metals by various hyper-accumulating plant species.
Remediation mechanism Plant species Studied heavy Results summary Experimental phase Reference
metal
Phytoextraction Brassica junea Zn, Ni, Cr and Phyto-adsorption of studied Ni, and Cr was evident Pot experiment Saraswat and
Cd through the shoot of Brassica species through shoot of Rai (2009)
Brassica
Pteris vittata As, and Cr Enhanced translocation of As and Cr in presence of sulfate Hydroponic De Oliveira
experiment et al. (2014)
Brassica napus Cu Increased absorption, and uptake and of Cu in presence of Pot experiment Zhang et al.
tolerant bacterial strain (2011)
Hyperaccumulation Arabis Paniculata Pb, Zn and Cd A. paniculata can help in decontaminate the field with Hydroponic Tang et al.
Franch multi-metal contamination experiment (2009)
Sedum alfredii Cd and Zn Combined root enzyme activity and glutathione of leaves Lab trial Jin et al. (2009)
helps in reducing Cd and Zn.
Alyssum heldreichii Ni Leaves of A. heldreichii can accumulate significant Field sampling and Bani et al.
amount of Ni. lab analysis (2010)
Phytostabilization Festuca rubra L. Cu Halloysite treatment enhanced the reduction of trace Pot investigation in Radziemska
metal glasshouse et al. (2017)
A total of 8 hyper tolerant Cd, Mn, Pb and Bioconcentration factor (BCF) and soil types triggers the Field studies at Mn Yang et al.
plant species Zn hypertolerance and phytostabilized potential of studied mine tailings (China) (2014)
heavy metals
Hyparrhenia hirta Pb, Zn and Cu Accumulated nearly 150 mg/kg Pb in roots through Mine cleanup Conesa et al.
phytostabilized process experiment (2007)
Norway spruce (Picea Cu and Zn The fine root system of studied plant species may Open-top chambers Brunner et al.
abies) and poplar (Populus accumulate metals but the phytostabilized potential was experiment (2008)
tremula) not well with those plant species
Athyrium wardii Pb Mining ecotype hypertolerance was found to be higher Pot experiment Zhao et al.
than non-mining ecotype species (2016)
Phytodegradation or Nicotiana tabacum Cd, Zn and Cu A greater accumulation of examined heavy metals (Cu, Lab trial Zhang et al.
phytoremediation and Zn) by transgenic tobacco plant due to improved (2008)
biomass and root system
Nelumbo nucifera Cd The activation of PCS enzyme through NnPCS1 gene in In vitro bioassy Liu et al. (2012)
transgenic Arabidopsis thaliana showed better metal
tolerance by lotus
Porteresia sp. Fe, Zn, Mn, Cu, The roots of tested saltmarsh was found to be more active Saltmarsh Hossain et al.
Co, Rb, Sr, and for accumulating the heavy metals as compared to above investigation (2021)
Pb ground shoots and leaves due to BCF vaiation
Aquatic macrophyte As, and Cd Heterologous expression of CdPCS1 (a PCS gene) cause an In-vitro lab trial Shukla et al.
Ceratophyllum demersum enhanced Cd and As accumulation in transgenic Nicotiana (2012)
tabacum
Eleocharis acicularis Cu, Zn, As, and The shoot of studied plant species accumulates the Pilot scale river Sakakibara
C highest concentration of toxic metals from the experiment et al. (2011)
contaminated water.
5
Fig. 2. A schematic showing the major mechanisms including phytoextraction, phytostabilization, phytovolatilization, and phytodegradation of phytoremediation
approaches during plant-based green remediation of toxic heavy metals.
adsorption, or sequestration of the translocated HM into the shoots or phytoextraction, the phytostabilization process is mediated by the re
biomass was evident (Saraswat and Rai, 2009; Yang et al., 2022). The striction of adsorbed toxic metal in the vadose zone through inorganic
key mechanisms of the phytoextraction process can be corroborated ligands precipitation, alkalization, and complexation with polymeric
with metal-chelation, cell wall binding with examined metal ions, and substances (Ma et al., 2016; Gavrilescu, 2022). The enhanced phytos
metal-biomass complex formation mediated by glutathione (GSH), tabilization can be achieved through the addition of organic amendment
phytochelatins, Metallothioneins, etc. Common metal binders in the cell (OA), or biochar (BC) as a soil filler in the rhizospheric zone, while the
cytosol (Sabir et al., 2015; Sarwar et al., 2017). However, the specified migration of HM in the plant vascular system is inhibited through the
mechanism of phytoextraction was highly varied due to plant-, soil-, and stable sequestration of the root system of potential plant species
environment-specific factors. Thus, meticulous, and separate studies (Muthusaravanan et al., 2018). The key triggering factors for enhanced
were encouraged using the specific metal phytoextractor plant species phytostabilization are soil pH, soil organic matter, soil microbial in
under varying environmental conditions including abiotic adverse stress teractions, and rhizospheric exudates during HM bioremediation (Sar
to explore specified metal remediation mechanisms. In general, the war et al., 2017).
rapidly growing plant species with extensive biomass structures were Phytovolatilization is also a prospective and perpetual mechanism of
selected for the phytoextraction or phytoaccumulation process (Shen HM remediation through the volatilization of biomass-derived HM into
et al., 2022). Amongst the popular phytoaccumulator species, Brassica the atmosphere by the transformation of non-toxic volatile metabolites
species were mostly studied species for global metal remediation in or aerosol intermediates (Muthusaravanan et al., 2018). In contrast, the
vestigations (Zhang et al., 2011; Muthusaravanan et al., 2018). A wider earlier investigation through the phytovolatilization procedure has
application of Brassica species for a successful phytoaccumulation documented the emission of harmful volatiles, indicating potential
approach was facilitated by the well-defined root system and succulent environmental risk or research ambiguity during pollutant decontami
foliage to accelerate the metal adsorption and metal chelation mecha nation (Sakakibara et al., 2011). In particular, the tobacco plant was
nism. Similarly, the common sunflower (Helianthus annuus species) was utilized for the conversion of toxic metals into non-toxic volatiles
documented as another vital phytoaccumulator for toxic HM remedia through stomatal transpiration have been documented (Rayu et al.,
tion with a wider leaf canopy and better survival potential under 2012). For example, the organic form of toxic mercury (i.e., methyl
extreme climatic adverse conditions (Madejón et al., 2003; Ojuederie mercury) can be absorbed through tobacco roots and translocated to the
and Babalola, 2017). Because phytoaccumulators cannot survive in biomass including leaves (Wang et al., 2014; Song et al., 2022). The
severely polluted environments, the field implementation of the phy temperature-, humidity-, and light-sensitive stomatal transpiration can
toextraction technique is only feasible for sites with moderate to low exert the less toxic or non-toxic elemental mercury (Wang et al., 2014).
levels of HM contamination (Sabir et al., 2015; Khalid et al., 2017). Likewise, Arundo donax mediated absorption and volatilization of As
The next important mechanism is ‘phytostabilization’, where po (III) into less toxic elements was reported by earlier investigation
tential plant species are applied for the stable sequestration or immo (Guarino et al., 2020). The key mechanism involved the assimilation of
bilization of HM that can significantly limit the bioavailability and toxic metals (e.g., Hg, As, etc.) into organic volatile compounds
mobility of adsorbed HM from the contaminated site through chemical including amino acids, cysteine, and methionine (Rai et al., 2020;
sequestration, rhizospheric interaction, and chemistry of root exudates Gavrilescu, 2022) However, the detoxification mechanism using the
(Sarwar et al., 2017; Ali et al., 2020). The rhizosphere is the dynamic phytovolatilization strategy is still unclear because of contradictory
root zone where a multiplayer interaction is occurring for triggering the research results. Plant phyllosphere acting a key considering role during
plant-soil interaction during the management of abiotic plant stress the phytovolatilization process, where biomass-derived secondary me
including heavy metal stress (Sarker et al., 2021a). Unlike the tabolites may limit the extensive application of the volatilization process
6
(Song et al., 2022). attention for the removal/detoxifying/transformation/neutralize the

Phytodegradation or rhizodegradation is the process of breakdown negative effects of HMs, while protecting the surrounding environment
or degradation of toxic metal or metalloid into non-toxic compounds (Jeyakumar et al., 2023; Riseh et al., 2022; Sreedevi et al., 2022; Tar
through biochemical or enzymatic breakdown (Khalid et al., 2017; Shen ekegn et al., 2020). Unlike a number of widely used physicochemical
et al., 2022). The phytodegradation in the plant biomass can be trig methods used to alleviate HM pollution, bioremediation offers a range of
gered by enzymatic interaction and secondary metabolite production economic feasibility due to its high HM removal efficiency,
capability of the plant species, while the rhizoremediation was governed cost-effectiveness, ease of handling, and ready availability both in
by root exudates and rhizosphere chemistry (Khalid et al., 2017; contaminated soil and water (Kour et al., 2021; Sharma et al., 2021;
Muthusaravanan et al., 2018). The presence of bioenzymes (e.g., lac Sreedevi et al., 2022). Among the biological agents, microorganisms
case, peroxidase, nitroreductase, and oxidoreductase) and play a crucial role in HMs bioremediation. These organisms are not only
ACC-deaminase could foster the phytodegradation process during helpful in dissolving HMs but also take part in the oxidation and
organic pollutant remediation including pesticides, trace metals, and reduction of transition HMs. This green technology exploits the meta
antibiotics (Muthusaravanan et al., 2018; Sarker et al., 2021b). The bolic capacity of microorganisms to eliminate HM contamination. In
factors affecting the performance of photodegradation are soil pH, particular, this technique aims to convert highly valent toxic heavy
moisture, and level of contamination during green remediation of toxic metals into less toxic ions. Numerous microbial genera, including
metals (Bhat et al., 2022). In contrast, rhizofiltration, evapotranspira Arthrobacter, Alcaligenes, Aspergillus, Azotobacter, Bacillus, Burkholderia,
tion, hydraulic control, and phytostimulation were reported as the Fusarium, Mucor, Penicillium, Pseudomonas, Rhizopus, Streptomyces,
minor mechanism of phytoremediation (Ojuederie and Babalola, 2017; Stenotrophomonas, Thiobacillus, Talaromyces, and Trichoderma have been
Rahman and Singh, 2020). used in bioremediation. Archaea from severe environments, notably
Natrialba and Haloferax, have also been described as potent bioresources
4.3. Challenges toward sustainable management of plant species for biological remediation. It is worth noting that the application of
potential microbes is generally not site-specific, but rather can be uti
Phytoremediation using naturally growing toxic metal tolerant plant lized both in soil and aquatic environments (Manoj et al., 2020; Sreedevi
species or genetically engineered plant species can be an effective et al., 2022). A list of different microbes used in the bioremediation of
remediation strategy, but the management of the hyperaccumulators HMs is enlisted in Table 2. These bioagents possess large surface area to
along with plant biomass after the remediation treatment is a big chal volume ratios and numerous binding sites with strong binding affinities
lenge. The plant biomass contaminated with toxic metals is traditionally and other unique characteristics that provide high HM removal effi
disposed of by integrated management strategies including in ciency (Cameron et al., 2018).
cinerations, open dumping, composting, and pyrolysis (Kovacs et al.,
2013; Shen et al., 2022). Amongst the existing management of plant 5.1. Mechanisms of bioremediation of HM contamination
biomass during post-treatment of HM remediation, thermal strategy (i.
e., incineration and pyrolysis) is employed for the concentration of In general, a majority of HMs were grouped as toxic, but potential
adsorbed toxic metals into the solid fraction (i.e., black carbon or ash biological organisms have evolved specific resistance mechanisms and
portion) after the thermal treatment as compared to liquid and gaseous complex intracellular pathways to utilize, interact, acclimate, and
fraction derived from the pyrolysis process (Al Chami et al., 2014). Thus, detoxify HMs for cellular regeneration (de Alencar et al., 2017). Biore
effective post-treatment of hyperaccumulating plant species still needs mediation can be done in several ways including detoxification, bio
to be addressed properly. sorption, degradation, mineralization, and transformation from highly
Hyperaccumulation of toxic metals through pristine plant species is a toxic to low toxic forms, intracellular sequestration by bioaccumulation,
lengthy process, and tedious for the post-management after treatments extracellular sequestration as insoluble compounds by precipitation,
(Mench et al., 2010). In addition, the root systems of investigated plant and production of metabolites that solubilize and chelate metal com
species are superficial and limited within the plough layers, resulting in pounds that lead to leaching (Jasrotia et al., 2017). In addition, the plant
the ineffective adsorption and subsequent transfer of heavy metals to growth promoting microbes (PGPMs) including bacteria, mycorrhizae,
ward plant biomass (Shen et al., 2022). In previous observations, and fungi may also contribute to the bioremediation of HM (Rai et al.,
comparatively lower sequestration and bioaccumulation of toxic metal 2020; Raklami et al., 2022). Amongst the PGPM, bacteria, and mycor
were evident when using naturally growing hyperaccumulating plant rhizae can secret bioactive molecules including metal chelators, which
species (Mench et al., 2010; Lee et al., 2019). Thus, an extensive facilitate the biosorption and bioaccumulation process (Raklami et al.,
application of perennial plant species including eucalyptus, bamboo, 2022). However, several probiotic bacteria and fungi can accelerate the
and ornamental plant species could not be feasible in the field scale microbial precipitation and biosurfactants-mediated release of metal
application. The search for new alternative hyperaccumulating plant ions for the reclamation of trace metal contamination (Manoj et al.,
species such as marine saltmarsh and roadside perennial woody species 2020). However, these potential mechanisms are largely influenced by
to overcome the existing challenge will be an option (Hossain et al., the nature and efficiency of the organisms as well as the type and con
2021; Madanan et al., 2021). Furthermore, biotechnological advance centration of HMs (Akhtar et al., 2020; Sharma, 2020). The different
ment through gene editing using the most popular CRISPR-Cas9 tech mechanisms of microorganisms involved to remove HMs are depicted in
nology for enhancing the performance of naturally available Fig. 3.
salt-tolerant species was revealed as the pioneering approach (Sarma
et al., 2021). In recent years, gene editing and related omics-driven 5.2. Lab-to-field challenges
technologies have gained priority for addressing those critical research
pitfalls. Cost-effectiveness and environmental sustainability were the For the design, development, and implementation of bioremediation
reported challenges during the phytoremediation of toxic trace elements techniques, it is critical to select the optimal bacterial strain according to
in field-scale applications. its remedial potential and underlying processes (Choudhury and Chat
terjee, 2022; Li et al., 2022). Recently, different biotechnological tools
5. Bioremediation: interaction between HM and microbes such as genetic engineering, and genetically modified organisms
(GMOs) have increased the efficiency of bioremediation technology,
Bioremediation, or biological remediation is an innovative technol however, dealing with large volumes of polluted land and wastewater
ogy that uses multiple potential biological agents, mainly bacteria, remains a big challenge. The industrial implications of engineered or
fungi, algae, yeasts, molds, and plants, which is gaining increasing ganisms face several obstacles. In addition, the genetic stability of these
7
Table 2
Different highly efficient microorganisms used in alleviating heavy metals from contaminated environments.
Microbial species Studied HM Removal efficiency Removal mechanisms References
Ochrobactrum MT180101 Cu 90% removal Biosorption Torres (2020)

Bacillus cereus Cr 81% biosorption Biosorption Nayak et al. (2018)
B. thuringiensis Hg 62% metal sorption Biosorption Saranya et al. (2019)
Cellulosimicrobium sp. Pb Nearly complete remediation Biosorption Bharagava and Mishra (2018)
(KX710177) (99%)
Burkholderia sp. Z-90 As, Cd, Pb, Cu, Zn, Mn 24%–52% bioleaching Combined bioleaching and Yang et al. (2018)
flocculation
Pseudomonas aeruginosa ATCC Cu, and Zn A wide range of removal Soil washing Mulligan et al. (2001)
9027 (18–65%)
P. aeruginosa Ba, Cd, Pb, Ni, Sr, and Adsorption varied from 7% to Adsorption Elouzi et al. (2012)
Zn 62%
P. aeruginosa FZ-2 Hg Above 99% Biosorption Hwang and Jho, 2018
Pseudomonas sp. Cd, Pb N/A Biosorption Huang and Lin (2013)
LKS06
Bacillus sp. MSI 54 Cd, Pb, Mn, and Hg 75%–99% precipitation achieved Co-precipitation Ravindran et al., 2020
2020
Bacillus sp. HIP3 Cd, Cu, Cr, Zn Metal chelation was evident up to Metal chelation Hisham et al. (2019)
13%
Citrobacter freundii Al, Cd, Cu, Fe, Mn, Zn 40–80% precipitation Precipitation Gomaa and El-Meihy (2019)
MG812314.1 documented
Alcaligenes sp. MMA Cd, and Zn Nearly 70% accumulation of Bioaccumulation Sodhi et al. (2020)
metal
Desulfovibrio desulfuricans Zn A complete removal (100%) Biosorption Mwandira et al., 2020
Oceanobacillus profundus Pb, and Zn 54%–97% metal sorption Biosorption Abd El-Motaleb et al. (2020)
Klebsiella sp. USL2D Pb 97% efficiency Biosorption Orji et al. (2021)
Streptomyces sp. Pb 83% removal Biosorption Hamdan et al. (2021)
P. azotoformans JAW1 Cd, and Pb 78–98% metal sorption Biosorption Choińska-Pulit et al., 2018; Orji et al.,
2021
Acinetobacter sp. B9 Ni 69% removal Biosorption Bhattacharya and Gupta (2013)
Sterigmatomyces halophilus Pb, and Zn 57%–90% effectiveness Biosorption Bano et al. (2018)
Paecilomyces sp. Co 70–93% removal Biosorption Gonzalez et al., 2019
Aspergilus niger
Penicillium sp.
Maugeotia genuflexa As Up to 98% metal sorption Biosorption Leong and Chang (2020)
Ulothrix cylindricum
Chlorella sp. (immobilized) Cd More than 92% removal Biosorption Shen et al. (2018)
Scenedesmus quadricauda Cr 98%–100% removal Biosorption Daneshvar et al., 2019; Khoubestani
et al., 2015
C. sorokiniana Cd 65% metal accumulation Bioaccumulation León-Vaz et al. (2021)
Aphanothess sp. Pb Higher efficiency (99.9%) Biosorption Keryanti and Mulyono (2021)
Phormidium sp. Pb Above 92% Biosorption Das et al. (2016)
C. kessleri Pb 97% efficiency Biosorption Sultana et al. (2020)
organisms in the field is always a subject of speculation (Hu et al., 2022; microbes including bacteria and fungi were reported as a key coupling
Pham et al., 2022). A strong understanding of the bioremediation strategy for enhanced phytoremediation (Muthusaravanan et al., 2018).
mechanisms is needed to modify the research on the right track. Last but The inoculation of arbuscular mycorrhizal fungi (AMF) boosts the
not least, further research in bioprocess level development, imple magnitude and potency of classical phytoremediation near the vadose
menting faster operation procedures both in industry and the field, and zone (Shen et al., 2022). In general, AM fungi are functioning as plant
metagenomic manipulation of microorganisms are highly stress mitigation under adverse climatic conditions (Mitra et al., 2021).
recommended. However, a meticulous inoculation of plant growth promoting microbes,
and AM fungi species can improve the root architecture and modulates
6. Combining methods for enhanced remediation: a cutting- the root exudates of hyperaccumulator species, resulting in a simulta
edge approach neous enhancement of a holistic approach (Sarwar et al., 2017; Ojued
erie and Babalola, 2017).
6.1. Phytoremediation in the presence of potential microbes
6.2. Nano-bioremediation- a merger of nanotechnology with
Microbial bioremediation is a robust approach to address various
bioremediation
environmental pollutants including pesticides, heavy metals, and
emerging contaminants through the direct microbial transformation of
Over the last few years, nanobioremediation, a combination of
investigated contaminants, or potential bio-enzymatic alteration both in
nanoremediation with bioremediation, has emerged as a powerful
contaminated soil and water (Sarker et al., 2021b; Kour et al., 2021;
approach for detoxifying heavy metals due to its superior performance
Sreedevi et al., 2022). Likewise, phytoremediation was a classical green
over traditional ones (Kaur and Roy, 2021). It is a novel, promising, and
remediation strategy practiced since a decade-long investigation as a
sustainable technology compared to other technologies in several as
cheap and sustainable soil reclamation technique for HM remediation
pects such as relative cost, generation of secondary pollutants, technical
(Mahar et al., 2016; Shen et al., 2022). The competence of phytor
complexity, environmental concerns, and conflicting results (Wu et al.,
emediation can be accelerated through various coupling methods such
2019; Amin et al., 2021; Saleem et al., 2022). Chemically produced
as biochar-based phytoremediation, application of transgenic plants,
nanoparticles can be expensive and also require the use of potentially
microbe-assisted phytoremediation, and nanotechnology-based phytor
environmentally undesirable toxic substances, which may lead to the
emediation (Sarwar et al., 2017). Among the biostimulators, potential
generation of secondary pollutants (Song et al., 2022). To reduce costs
8
Fig. 3. Various bioremediation mechanisms of microorganisms including bioaccumulation, biosorption, biomineralization, bioleaching, bioprecipitation, redox, and
biodegradation during potential microbes-HM interaction. Red round shapes represent the heavy metals, MT- Metallothionein, GSH- Glutathione, and GSSG-
Glutathione disulfide.
and produce clean and environment-friendly nanoparticles, biogenic been explored as a promising green strategy for combating HM
synthesis of nanoparticles can be done using various microorganisms as contamination under wastewater conditions, the systematic advance
well as plants that can be further used for heavy metal remediation ment and mechanistic insight are still under observation. Microalgae can
(Muzahid et al., 2023; Saravanan et al., 2023). With the application of remove the heavy metals directly from the contaminated water through
nanobioremediation, the technical shortcomings of microbial bioreme a low-concentration metabolism-dependent absorption into their cells,
diation can be fixed (Sunanda et al., 2022). For decontaminating heavy and a non-active biosorption adsorption process (Narayanan et al.,
metals, this technology stimulates microbial functions for the secretion 2021). Additionally, the decontamination of heavy metal-contaminated
of potential bioenzymes. The reported metal removal efficiency of soil and water using phycoremediation has been demonstrated with
bio-nanoparticles ranges from 12% with bio-palladium nanoparticles several species of algae, indicating the promising aspects and potential
prepared from Spirulina platensis to 100% with iron oxide nanoparticles of plant remediation (Saxena et al., 2021). The underlying mechanisms
from Geobacter sulforeducens against palladium and chromium, respec of microalgae-derived bioremediation of toxic metals are summarized as
tively (Saleem et al., 2022). Synthetic silver nanoparticles from the follows:
fungus Rhizopus oryzae have been used for treating wastewater and
pesticide adsorption (Das et al., 2012). Besides, silver nanoparticles
synthesized from fungi are used as air and surface disinfectants (Zhang 7.1. Heavy metals removal mechanisms using microalgae
et al., 2016; Muzahid et al., 2023). The behavior of the nanoparticles
largely depends on the particle size distribution, morphology, specific In earlier studies, the application of microalgae was extensively re
surface area, and charge, and therefore, different biogenic nanoparticles ported for the removal of heavy metals through various robust mecha
are now widely used in removing heavy metals (Rizwan et al., 2014). nisms, while the presence of a higher concentration of HM could pose a
hidden threat to human, plant, and animal life due to their toxicity and
7. Microalgae-a new perspective bioremediation option for carcinogenic properties by trophic transfer from the aquatic ecosystem
aquatic and wetland ecosystem into human bodies (Leong and Chang, 2020; Rakib et al., 2022). How
ever, microalgae due to its photosynthetic by-product (oxygen) were
Microalgae are regarded as preferable options among the bioactive naturally utilized as the ‘biological purifier’ in the wastewater and
drivers because of their ease of application, inexpensive inputs, and surrounding waterways that were heavily polluted with toxic metals
persistent efficacy during the phycoremediation of HMs in both terres (Priya et al., 2022). The mechanistic insights from transcriptomics
trial and aquatic environments, as opposed to both chemical and phys analysis have been meticulously utilized to pinpoint the cellular activ
ical techniques of HM remediation (Leong and Chang, 2020; Singh et al., ities under heavy metal stress and understand the strategic responses of
2021). Recent research has successfully examined the tolerance and microalgae. The basic benefit of microalgae-based bioremediation of
responses of various strains of microalgae against toxic metals in HM presents in the aquatic environment was the in-situ application of
wastewater treatments (Singh et al., 2021). In addition, the bio living algae with improved green biomass and the concentration of HM
accumulation capacity of studied trace metals with the transformation can be reduced by several physical and biogeochemical processes hosted
into the byproducts having added value and the use of non-living ma by efficient metal tolerant microalgae genera (Danouche et al., 2020;
terial as biosorbent was evident during cleaner production of industrial Priya et al., 2022). Among the various metal stress defense mechanisms,
wastewater in the presence of potential microalgae species (Salama toxic metal chelation using the reduction activity of enzymes (e.g.,
et al., 2019; Leong and Chang, 2020). Although microalgae in solitary or phytochelatin) or antioxidants by redox reaction was documented as the
in tandem with contemporary biological remediation approaches have prominent mechanism during algal remediation of mercury contami
nation (Gómez-Jacinto et al., 2015).
9
A two-stage remediation process was revealed during the et al., 2019).

microalgae-derived successful transformation/sequestration of heavy The most widely studied algal species for HM bioremediation are
metals from their environment including bioaccumulation and bio Chlorella and Nostoc (Singh et al., 2021). However, the most screened
sorption (Fig. 4). Concisely, the activation of negatively changed surface microalgal species that help for the bioremediation of HM from
area through an electrostatic interaction on the metal binding sites can contaminated wastewater or waterways are Micrasterias denticulate, Ulva
be promptly deposited on the microalgal cells (Salama et al., 2019). lactuca (Cd); Spirogyra hyalina (Hg); Sargassum natans, Sargassum vulgare
According to the figure, crystals, complexes, or cell precipitates can also (Pb); Cladophora fascicularis (Pb); Phormedium bohner, Spirogyra sp.,
develop from the interaction of HMs with the groups or binding enzymes Dunaliella sp. (Cr)); Spirogyra hyalina (Hg); Spirogyra hyalina (Hg); and,
on the plasma membrane of algal cells in the next phase. Once inside the Spirogyra hyalina (Cd) (Holan and Volesky, 1994; Dwivedi et al., 2010;
algal cells, these precipitates aggressively infiltrate and attach to inter Bishnoi et al., 2007; Dönmez and Aksu, 2002; Gupta et al., 2001; Kumar
nal peptides and proteins (Guldhe et al., 2017; Singh et al., 2021). Due to and Oommen, 2012; Volland et al., 2013; Sari and Tuzen, 2008; Deng
how quickly certain HMs penetrate the cell membrane through bio et al., 2007).
accumulation and biotransformation, this enrichment phase is mostly The level of contamination, types of wastewaters, algal species, HM
connected to the gradual but irreversible routine operations of cell content, light, temperature, and pH all have an impact on the removal of
metabolism (Leong and Chang, 2020). Nevertheless, polysaccharides, HMs by microalgae (Chen et al., 2015; Papry et al., 2020). High HMs
lipids, and organic proteins make up the majority of the cellulose and concentrations will hinder the biological activities of microalgae,
alginate-based cell walls of microalgae. These components also have a restricting their ability to bioremediate HMs, and even resulting in
variety of functional groups that can bind HMs, including –OH, –SH, mortality owing to the small number of binding sites on the microalgal
-PO4, C–– O, –COOH, C3H4N2, and others (Priatni et al., 2017). surface and the distinct chemical features of HMs. When treating
Microalgae are the most effective biosorbent because of the wastewater that has been contaminated with HMs, the well-defined
numerous binding sites in their cell walls and membranes that give them photosynthetic biomass of microalgae and the surface area of cell
a high affinity for biosorbing metal ions and emerging contaminants walls are beneficial to adsorb HMs because they deal with the physical
(Singh et al., 2021). Earlier studies showed that an essential factor in and chemical compositions. Even though microalgae are frequently
determining the microalgae’s ability to adsorb HM is the variety of employed as efficient heavy metal bioremediation agents, several
functional groups that have accumulated on their surface and generate technical barriers still stand in the way of their broad application in real
negative charge (Li et al., 2020; Priyadarshini et al., 2019). Moreover, polluted environments. Large-scale biomass production, harvesting, and
HMs can bind to the exopolysaccharides of microalgae by interacting drying are expensive and time-consuming processes (Leong and Chang,
with their negatively charged organic acids, which is another mecha 2020). The preferred choice for waste-to-wealth bioconversion would be
nism of HM sequestration. Active transportation is created by further the combination of microalgae with bacterial consortia for an integrated
modifying the covalent bonding of HMs with ionized cell walls and the biorefinery technique (Jaiswal et al., 2020). To strengthen the inte
ionic exchange of HM ions with cell wall cations. The process through grated biorefinery plan, it will also be advised to raise a variety of hardy
which HM builds up inside the cell is called accumulation, but it is microalgae species in wastewater. The overall objective of HM biore
comparatively a slow one. HM is actively carried over the cell membrane mediation employing prospective microalgae should always be clear
and into the cytoplasm of contaminated aquatic organisms, where they with the selection of tolerant variety in challenging contexts like acidic
interact with internal binding sites of proteins and peptides such as GSH, drainages and industrial places. Also, to support the circular economy,
metal transporters, and phytochelatins (Ibuot et al., 2017; Pradhan rigorous research should be planned for simultaneous bioconversion and
Fig. 4. The key underlying mechanism of heavy metal remediation using microalgae as a biological purifier.
10
remediation of value-added byproducts. microbes (Jaiswal et al., 2019; Pant et al., 2021). Thus, multi-omics will
be the better option to minimize the specific research pitfalls during
8. Biotechnological advancement of HM bioremediation integrated bioremediation of HM contamination (Dixit et al., 2015;
Malik et al., 2022). The design of a microbial biosensor and its field
Due to their affordability, ecological friendliness, and ease of in-situ application will also be a good option for detecting the effective mi
application during the remediation of target contaminants, such as toxic crobes or consortia for commercial application of genetically modified
heavy metals in the contaminated areas, phytoremediation, and mi rhizospheric microbes in protracted and green bioremediation (Dixit
crobial bioremediation are two green remediation approaches that have et al., 2015; Sharma et al., 2021).
become popular tools in the sustainable remediation of pollutants
(Goswami et al., 2022). The most efficient way for sustainable and 8.1. CRISPR-Cas9 technology for HM remediation through transgenic
enhanced removal of environmental contaminants has been found to be plants
the coupling of engineering approaches (also known as bioengineering
of prospective bacteria and plants). The advancement of bioremediation The engineering of potential phytoaccumulating plants, a new green
techniques will be aided by new genetic toolkits and an in-depth un weapon for remediation of HM contamination. Targeted genetic modi
derstanding of the structures and functions of microbial and plant genes fication in plants can be done using various genome editing technologies
(Jaiswal et al., 2019; Sarma et al., 2021). As a reliable biological including ZNF, TALENs, and CRISPR-Cas for enhanced phytor
method, next-generation sequencing (NGS) is being used to screen target emediation of HM contamination (Islam, 2019; Sarma et al., 2021; Shen
genes or identify novel genes from the potential biodegrading microbes et al., 2022). In general, the removal of unexpected genes can be
that may easily transform and/or mineralize harmful trace metals into replaced by target and potential genes which were considered the
non-toxic altered products. (Malik et al., 2022). In order to rapidly classical process of genome editing for improved and sustainable phy
comprehend the fundamental mechanism of gene-gene interaction and toremediation through transgenic plant species (Kim et al., 1996; Liu
its complex interpretation during the bioremediation of heavy metals et al., 2023; Sarma et al., 2021). Still, the robustness and sustainable
using advanced biotechnological tools, combined studies of multi-omics effectiveness will decipher the contemporary genome editing technol
approaches, including genomics, metagenomics, transcriptomics, pro ogy as a high-tech biotechnology tool for exploring the key genes of
teomics, metabolomics, and phenomics, are highly encouraged (Azad target alleles in advanced bioremediation. Among the various genome
et al., 2014; Malik et al., 2022). To investigate the understanding of the editing toolkits, the CRISPR-Cas system is the precise genetic modifi
genome organization of rhizosphere-specific microbial communities and cation procedure that can change multiple genes at the same time by
to screen genes that contribute to bioremediation in various microbial insertion, deletion, or base substitution (Basu and Sachidanandan, 2013;
species, several multi-omics strategies, including the major ones (such as Sarma et al., 2021). However, the conventional metal hyperaccumulator
genomics, metagenomics, metabolomics, and transcriptomics) and the plant was widely used under their pristine conditions for sluggish phy
minor ones (such as proteomics, phenomics, and ionomics), have been toremediation, whereas, the genome editing with the CRISPR-Cas sys
extensively applied (Fig. 5). Fig. 5 indicates that the genomics study will tem will boost metal extraction, metal stabilization, and metal
identify the gene that is most useful for bioremediation and that it can be transformation into non-toxic volatiles or metabolites (Mahar et al.,
combined with metagenomics for a more thorough explanation. For 2016; Ojuederie and Babalola, 2017). Previous studies have docu
determining the most efficient combination technique during sustain mented the enhanced metal tolerance and phytoextraction capability
able bioremediation, metagenomics can also be merged with through the application of altered genetic makeup using CRISPR-Cas9
meta-transcriptomics or the partial or complete genome sequencing of a genome editing (Wang et al., 2014; Sanz-Fernandez et al., 2017).
potential HM-degrading microbial population. (Suenaga et al., 2007; Furthermore, several metal tolerant plants have been sequenced
Meyer et al., 2008; Silva et al., 2012). including potential energy crops for improving the overall performance
According to a prior study (Szewczyk and Kowalski, 2016), the wide of phytoremediation using gene editing biotechnological tools (e.g.,
variation in mRNA expression can restrict the widespread application of Noccaea caerulescens, Arabidopsis juncera) (Estrela and Cate, 2016;
meta-transcriptomics analysis, while meta-proteomics will emerge as a Basharat et al., 2018). The performance of phytoremediation of HM
new technique to identify all expressed proteins in a sample at a contamination using various underlying mechanisms (e.g., phytoex
particular time and under specific circumstances. Metabolomics was traction, phytostabilization, phytovolatilization, and phytodegradation)
also used to explain the processes and pathways of microbial bioreme can be improved by CRISPR-mediated genome editing, while some elite
diation because meta-proteomics alone cannot capture the complexity of enzymes for ligand synthesis (such as metallothionines and phytoche
microbial bioremediation. Metabolomics is the study of transformed latins) will be helpful for transgenic plant-based remediation of HM
metabolites and secreted intermediates through genetically modified (Mani and Kumar, 2014; Basharat et al., 2018). Therefore, the coupling
Fig. 5. Omics-driven approaches for biotechnological advancement of bioremediation strategies during heavy metal remediation.
11
of multi-omics-based bioremediation with transgenic plants will Rakhi Nandi: Writing – original draft, Editing, Review & Editing, Most.
enhance the holistic bioremediation of HM contamination (Sharma Waheda Rahman Ansary: Writing – original draft, Editing, Review &
et al., 2021; Shen et al., 2022). Editing; Abu Reza Md Towfiqul Islam: Conceptualization, Methodol
ogy, Review & Editing, Supervision, Tofazzal Islam: Conceptualization,
9. Conclusion and recommendations Methodology, Review & Editing, Supervision.
In summary, this review updates our understanding regarding the

underlying mechanisms of heavy metal (HM) remediation through po Declaration of competing interest
tential plant species (hyperaccumulating species) and microorganisms
including bacteria, fungi, and algae for the treatment of contaminated The authors declare that they have no known competing financial
soil and wastewater. However, the solitary application of any biological interests or personal relationships that could have appeared to influence
drivers may limit its widespread application during the removal of toxic the work reported in this paper.
metals from contaminated sites. Thus, a combination of phyto- and
microbial-remediation approach seem to augment the magnitude of Data availability
biological remediation of HMs. In particular, biochar, organic manure,
and potential microbes can also be coupled with phytoremediation to No data was used for the research described in the article.
emerge the wondrous options for enhanced bioremediation of toxic
metals. Although, the traditional methods of phytoremediation or mi Acknowledgement
crobial bioremediation alone are the most efficient ones, however, the
process is quite slow, and due to poor performance, complete remedi The authors are grateful to “National Institute of Agricultural Sci
ation may not be achieved. The process can significantly be improved if ences, Rural Development Administration, Jeonju, Republic of Korea”,
the phytoaccumulator is combined with prospective bacteria or other and “Institute of Biotechnology and Genetic Engineering (IBGE), Ban
microbes that promote plant growth. The application of transgenic or gabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur
genome-edited plant species and microorganisms seems a highly 1706, Bangladesh” for continuous support during this manuscript
promising option for the effective bioremediation of HM-contaminated drafting and proofreading.
soils and aquatic environments. The integration of several physical
processes including adsorption and sequestration of HM with contem Appendix A. Supplementary data
porary bioremediation will also be proven as an effective method.
However, several research uncertainties may limit the laboratory-to- Supplementary data to this article can be found online at https://doi.
field transfer of bioremediation approaches, thus further adaptive and org/10.1016/j.chemosphere.2023.138861.
cross-field experiments are recommended for confirming the sustainable
remediation strategy to combat HM contamination. We recommend References
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Chemosphere 332 (2023) 138861

Contents lists available at ScienceDirect

Biological and green remediation of heavy metal contaminated water and

• Heavy metal (HM) reclamation using

1. Introduction combating HM pollution in aquatic environments including wastewater

(Song et al., 2022). attention for the removal/detoxifying/transformation/neutralize the

Ochrobactrum MT180101 Cu 90% removal Biosorption Torres (2020)

A two-stage remediation process was revealed during the et al., 2019).

In summary, this review updates our understanding regarding the

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