Sarker 2021

Environmental Technology & Innovation 23 (2021) 101777
Contents lists available at ScienceDirect
Environmental Technology & Innovation

journal homepage: www.elsevier.com/locate/eti
Remediation of chemical pesticides from contaminated sites

through potential microorganisms and their functional
enzymes: Prospects and challenges
∗ ∗∗
Aniruddha Sarker a,c , Rakhi Nandi a,d , Jang-Eok Kim a , , Tofazzal Islam b ,
a
School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University, Daegu 41566, Republic of
Korea
b
Institute of Biotechnology and Genetic Engineering, Bangabandhu Sheikh Mujibur Rahman Agricultural
University, Gazipur, Bangladesh
c
Department of Soil Science, EXIM Bank Agricultural University Bangladesh (EBAUB), Chapainawabganj, Bangladesh
d
Bangladesh Academy for Rural Development (BARD), Kotbari, Cumilla, Bangladesh
article info a b s t r a c t
Article history: In modern agriculture, chemical pesticides are widely used to protect crop plants from
Received 20 June 2021 insects and microbial pests, but the improper application of synthetic chemicals is
Received in revised form 28 June 2021 hazardous for non-targeted organisms and the environment of the applied sites. The
Accepted 5 July 2021
disposition mechanism of applied pesticides is highly variable in global farmlands; there-
Available online 7 July 2021
fore, the sustainable remediation of pesticide-contaminated sites is a priority research
Keywords: area for the ecofriendly management of these pollutants. Furthermore, researchers
Pesticide discourage the physical and chemical remediation of pesticides and their metabolites
Disposition because of issues related to time consumption, cost effectiveness, and sustainability
Bioremediation compared to microbial and enzymatic remediation. Microorganisms from diverse tax-
Microorganisms onomic groups, such as bacteria, fungi, and algae, are known to effectively metabolize
Enzyme pesticides and/or alter the chemical structures facilitating their degradation and making
the contaminated environment free from harmful pesticide residues. Similarly, catalytic
enzymes, such as laccase and peroxidase, can also efficiently remediate most organic and
chemical pesticides. The elite strains of microorganisms, singly or as a mixed consortium,
can be used for compelling biological pesticide remediation. However, several research
uncertainties, including inconsistent performance, adaptation under varying weather
conditions, and application difficulties, may limit the wider practical application of these
potential ecofriendly bioremediation approaches. This study reviews recent literature on
the prospect and challenges of ecofriendly bioremediation approaches for the reclama-
tion of pesticide-contaminated sites. This study also discusses the underlying mechanism
of the microbe- and enzyme-mediated bioremediation of pesticides with a sustainable
research prospective.
© 2021 Elsevier B.V. All rights reserved.
Contents
1. Introduction............................................................................................................................................................................................... 2
∗ Corresponding author.
∗∗ Correspondence to: Institute of Biotechnology and Genetic Engineering, Bangabandhu Sheikh Mujibur Rahman Agricultural
University, Gazipur 1706, Bangladesh.
E-mail addresses: jekim@knu.ac.kr (J.-E. Kim), tofazzalislam@bsmrau.edu.bd (T. Islam).
https://doi.org/10.1016/j.eti.2021.101777
2352-1864/© 2021 Elsevier B.V. All rights reserved.
A. Sarker, R. Nandi, J.-E. Kim et al. Environmental Technology & Innovation 23 (2021) 101777
2. Review methodology................................................................................................................................................................................ 3
3. Biological remediation of pesticides — A green and prospective approach...................................................................................... 3
3.1. Bacterial degradation of pesticides............................................................................................................................................ 4
3.2. Fungi- and algae-mediated pesticide degradation................................................................................................................... 4
4. Enzymatic pesticide biodegradation....................................................................................................................................................... 6
4.1. Application of laccase and peroxidase in pesticide biotransformation................................................................................. 7
5. Potentials of plant growth-promoting rhizobacteria in pesticide degradation ................................................................................ 9
6. Underlying mechanism and molecular advancement of pesticide bioremediation ......................................................................... 9
7. Challenges and prospective of pesticide biodegradation..................................................................................................................... 12
8. Conclusion ................................................................................................................................................................................................. 14
CRediT authorship contribution statement ........................................................................................................................................... 14
Declaration of competing interest.......................................................................................................................................................... 14
Acknowledgment ...................................................................................................................................................................................... 14
References ................................................................................................................................................................................................. 14
1. Introduction
Chemical pesticides are commonly used to protect crops from infestations by pests, including insects, pathogens, and
weeds, to enhance agricultural production (Lindley, 1976; Liu et al., 2001; Gavrilescu, 2005). Consequently, potential
hazards associated with human health, beneficial insects, animals, and birds have been reported due to the inappropriate
handling of these chemicals (Verger and Boobis, 2003; Naqqash et al., 2016; Baron et al., 2017; Ali et al., 2019).
Approximately ≤5% of the total applied pesticides practically inhibit the target pests, whereas the remaining >95% of
these pesticides never reach the target pest organisms rather deposited in the surrounding environments, including soil
and water resources (Nawaz et al., 2011; Niti et al., 2013). The resulting environmental and human food adulteration by
the applied pesticides also poses a serious threat to the food safety of agricultural commodities (Niti et al., 2013; Kumar
et al., 2018a). Likewise, the bioaccumulation and the biomagnification of pesticides in food chains primarily cause several
health hazards in human beings (Chen et al., 2015a). These pesticides and their metabolites have damaging effects on
ecology and biodiversity (Bilal et al., 2019; Barbieri et al., 2019). Early reports confirmed that residual pesticides may
cause neurotoxicity (Pereira et al., 2015) and serious health hazards, including the death of humans and other animals
(Simonelli et al., 2007).
Obsolete pesticides (e.g., organochlorine, organophosphate, carbamate, pyrethroids, and some broad-spectrum her-
bicides) have been banned or not recommended for field applications. Some of the recently used pesticides have
exhibited persistence in the applied sites (IRAC, 2020; Sparks and Nauen, 2015). Obsolete pesticides can also contaminate
the applied farmlands and the surrounding soil ecosystems, even after years of application. Improper landfilling and
uncertain residual pesticides can accelerate this unexpected contamination (IRAC, 2020; Rani et al., 2019). Thus, certain
banned pesticides (e.g., DDT, endosulfan, and BHC) could also contribute to the uncertainty of the sustainable and
future management of pesticides in applied sites (Sun et al., 2018). Considering the longer residence in applied sites
and the harmful effects of the applied pesticides to the off-target of the surrounding ecosystem, the higher pesticide
concentration from pesticide-contaminated sites and environmental matrices must be reduced, eliminated, or stabilized by
applying physical, chemical, or biological processes (Morillo and Villaverde, 2017; Kumar et al., 2018b; Saleh et al., 2020).
Physical and chemical pesticide remediation is largely discouraged because of unsustainability in terms of application
difficulties, high cost, and poor environmental safety (Zeng et al., 2017; Sun et al., 2020). Alternatively, the prospective
and potent microorganisms derived from the environment and their biocatalytic enzymes are effective bio-degraders for
the ecofriendly biodegradation of residual chemical pesticides and their toxic metabolites (Cycon et al., 2017; Kumar
et al., 2018b; Bilal et al., 2019; Tarla et al., 2020). The microbiomes and their enzymatic potency could function as robust
biological weapons to fight against toxic agrochemicals (Ortiz-Hernandez et al., 2013; Maqbool et al., 2016; Tarla et al.,
2020). A single type of microbe could be effective for pesticide bioremediation (Amani et al., 2019). Furthermore, a
mixed consortium could be used for the potential bioremediation of a specific chemical pesticide (Lopes et al., 2012).
In addition, biological remediation through efficient biodegraders and plant species is effective for the remediation of
emerging pollutants, including heavy metal degradations (Kaur et al., 2018; Dhaliwal et al., 2020).
Although a large body of literature on the classifications of pesticides and their toxicities and the application of the
elite strains of microorganisms and their enzymes in the bioremediation of various pesticides is available (Maqbool
et al., 2016; Huang et al., 2018; Cycon et al., 2017; Tarla et al., 2020), an unexplored avenue still exists in terms of
the efficient screening of the best biodegraders through molecular toolkits and practical applications to these biologics.
Additionally, sustainability with respect to cost effectiveness and performance stability must be meticulously addressed
through the expedition of the underlying molecular mechanisms of bioremediation (Ortiz-Hernandez et al., 2013; Bhat
et al., 2020). Therefore, the present study performs a review with a critical meta-analysis for updating our understanding
of the contemporary microbial and enzymatic biodegradation approaches for the ecofriendly remediation of pesticides
and their associated metabolites along with the prospective and practical challenges of these novel approaches toward
the commercial and sustainable reclamation of pesticide-contaminated sites or farmlands. Furthermore, a roadmap
of the prospective and biotechnological advancements for the sustainable commercial application of microbe-based
bioremediation of pesticides is also a focus herein.
2
Fig. 1. Types of pesticides studied for bioremediations and the associated elite strains of biodegraders summarized through the meta-analysis of the
reviewed 166 literatures.
2. Review methodology
A meticulous web surfing coupled with a screening of printed reference papers was performed to scrutinize studies
from peer-reviewed articles (e.g., research and review articles) to arrange the major features of biodegradation of
pesticides through biological drivers. The keywords for the search engine were ‘‘uncertainty of residual pesticide’’,
‘‘bioremediation of pesticides’’, ‘‘bacterial remediation of pesticide’’, ‘‘fungal remediation of pesticide’’, ‘‘mechanism of
pesticide bioremediation’’, ‘‘enzymatic degradation of pesticides’’, ‘‘challenges of microbial degradation of pesticide’’,
‘‘biotechnological advancement for pesticide bioremediation’’, and ‘‘prospective of pesticides bioremediation’’. However,
scholarly search-derived approximately 250 articles, including original research, systematic, and critical review on
pesticide contamination, and related microbe-derived bioremediation studies were gathered from frequently used, and
worldwide recognized sources (i.e., Google Scholar, Science Direct, Scopus, Springer, PubMed, and ResearchGate). A vigilant
skimming of the collected articles was performed with a positive correlation of pesticide biodegradation, a roadmap
of commercial applications, and proposed advocacy toward sustainable applications. We follow the standard review
methodology (e.g., identification, screening, eligibility, and interpretation for inclusion) to provide a chronological order of
the review story deciphering the problem identification related to pesticides, existing biological approaches for combating
the pesticide pollution, research uncertainty, existing knowledge gap, and the prospective concerning the sustainable
management of pesticide contamination. Moreover, we excluded irrelevant articles with respect to our study goal and
chose 166 referral articles for this review study followed by a critical discussion of studied pesticides and associated
biodegraders (Fig. 1). In summary, this study critically addresses the existing and well-documented biological approaches
for the sustainable management of pesticide-contaminated sites and provides future suggestions for the rectification of
pesticide bioremediation toward a green bio-cleanup of the contaminated sites.
3. Biological remediation of pesticides — A green and prospective approach
Pesticide bioremediation is a greener, and ecofriendly approach for the complete degradation, or transformation of
pesticides into nontoxic metabolites using living agents as the potential degraders (e.g., elite strains of microorganisms
and derived functional enzymes, effective species of earthworm for vermiremediation, and potential plant species for
phytoremediation) (Ortiz-Hernandez et al., 2013; Morillo and Villaverde, 2017; Bhat et al., 2020; Tarla et al., 2020). Among
microbial drivers, bacteria, fungi, algae, and mixed consortia including potential microbes are the chief transformers or
mediators for effective bioremediation due to their biocatalytic activities (Ortiz-Hernandez et al., 2013; Huang et al., 2018;
Bilal et al., 2019). Meanwhile, vermiremediation, which is a vital approach for remediating chemical pollutants, including
pesticides from contaminated sites, can function as both ex-situ and in-situ bioremediation utilizing potential earthworm
species either by direct remediation or stimulating associated bacteria or fungi to enhance the bioremediation process
(Zeb et al., 2020; Lin et al., 2019). The key mechanisms of vermiremediation may include ingestion by earthworms,
transformation into metabolites, and vermicast-derived microbial depletion of obsolete pesticides, including DDT and
metolachlor (Zeb et al., 2020; Sun et al., 2019; Xu et al., 2021). In addition, the pesticide bioremediation using potential
plant species through various mechanisms (e.g., phytoextraction, phytostabilization, phytoaccumulation, and rhizoreme-
diation) are effective in situ phytoremediation approaches (Singh and Singh, 2017; Bhat et al., 2020; Tarla et al., 2020).
Although bioremediation of pesticides is a natural phenomenon in agricultural farmlands, these processes are relatively
slow and insignificant in the contaminated sites (Singh and Singh, 2017). Thus, in particular, the bioremediation process
could be significantly accelerated by applying genetically engineered microorganisms (Niti et al., 2013; Bhat et al., 2020;
3
Tarla et al., 2020; Huang et al., 2018). Therefore, this study focuses on the prospect and challenges of potential microbes
(e.g., Bacteria, Fungi, and Microbial consortia), and their functional enzymes with respect to the bioremediation of obsolete
and problem pesticides under the sub-headings below.
3.1. Bacterial degradation of pesticides
Bacteria-mediated pesticide bioremediation is a major approach for the decontamination of pesticide-polluted sites
or samples. Several potential bacterial genera, such as Pseudomonas, Bacillus, Actinobacter, Acinetobacter, Burkholderia,
and Klebsiella, are effective for the pesticide bioremediation of diverse chemical classes (Matsumoto et al., 2008; Ajaz
et al., 2012; Mandal et al., 2013; Phugare et al., 2013). Over the past decades, these potential bacterial genera have been
effectively used in bioaugmentation and biotransformation approaches for the ecofriendly remediation of pesticides and
their toxic metabolites (Qu et al., 2015; Bilal et al., 2019) (Table 1).
A few early reports have suggested the potential of the Novosphingobium sp. bacteria for the biotransformation of
carbofuran (Liu et al., 2019) and the degradation (by up to 95%) of the 2,4-D herbicide using the bioaugmentation approach
(Dai et al., 2015). Endosulfan bioremediation by Pseudomonas sp. was conducted during a five-day lab experiment (Zaffar
et al., 2018). The study findings suggested that up to 80% endosulfan removal can be reached by applying Pseudomonas
species. Similarly, one of the chlorinated POPs, namely DDT, was remediated by approximately 80% in a pilot-phase trial
using the Chryseobacterium sp. bacterial strain (Qu et al., 2015). In another study, approximately 68% DDT remediation
was achieved when a mixture of Pseudomonas stutzeri, P. aeruginosa, and Bacillus firmus was used in a week-long lab
assay (Powthong et al., 2016). Approximately 85% degradation of three triazole fungicides was attained by applying
some effective Bacillus strains (Salunkhe et al., 2015). Approximately 88% diazinon degradation was also revealed by
Acinetobacter in a 20-day-long batch trial experiment (Amani et al., 2019). Interestingly, most of these potential bacterial
strains were isolated from the rhizosphere or soils (Morillo and Villaverde, 2017; Rani et al., 2019), indicating the cost
effectiveness of the bacterial bioremediation for pesticide remediation.
The ineffective and inconsistent performance of single bacterial strains can be recovered by the microbial mixed con-
sortium as a holistic solution for the sustainable pesticide bioremediation (McLellan et al., 2019). A bacterial consortium
comprising Pseudomonas, Klebsiella, Stenotrophomonas, Ochrobactrum, and Bacillus sp. remediated 82% of chlorpyrifos in a
10-day lab trial (Singh et al., 2016). The bacterial consortium of Pseudomonas spp. strains GA07, GA09, and GC04 exhibited
an excellent degradation capacity in a batch lab trial to remediate glyphosate herbicide (Zhao et al., 2015). Velázquez-
Fernández et al. (2012) described endosulfan degradation using a potential bacterial consortium of Pseudomonas spinose,
P. aeruginosa, and Burkholderia sp. A microbial consortium can be an economically and environmentally friendly approach
considering multifunctional features compared to conventional bioremediation techniques using a single effective strain
(Velázquez-Fernández et al., 2012). The mechanisms of the bacterial pesticide bioremediation are complex and versatile.
The elucidation of such a complex biochemical breakdown and further development are an interesting subject for further
study. Chen et al. (2015b) proposed one of the degradation pathways of pesticide cyhalothrin and identified metabolites
through Bacillus thuringiensis strain ZS-19. The authors demonstrated that hydrolysis may degrade cyhalothrin by the
cleavage of the ester linkage of the studied pesticide. The resulting cleavage of the diaryl bond was followed by the
aromatic ring degradation and a subsequent metabolism (Fig. 2A). The key mechanistic approaches can be merged with
the microbial genetic advancement to scrutinize the most effective bacterial strains or bacterial consortia for enhancing
sustainable pesticide bioremediation.
3.2. Fungi- and algae-mediated pesticide degradation
Although bacterial remediation is predominant over other microbial remediations, certain fungi and algae are con-
sidered as potential weapons for the degradation of notorious agrochemicals in soils (Harms et al., 2011; Zhang et al.,
2012; Kumar et al., 2018b; Spina et al., 2018). For example, a pure isolate of the white-rot fungus, Trametes versicolor, is
effective in remediating a mixture of imiprothrin and cypermethrin (Mir-Tutusaus et al., 2014). Similarly, the fungal strain
Phanerochaete can successfully remediate a mixture of atrazine and alachlor (Chrinside et al., 2011) and clothianidin (Mori
et al., 2017). The application of a novel Penicillium sp. strain leads to the efficient remediation of bensulphuron-methyl
(Peng et al., 2012). In addition, a fungal strain of Aspergillus sp. facilitates the bioremediation of oxyfluorfen herbicide
(Mohamed et al., 2011).
Maqbool et al. (2016) described several potential fungal strains triggering the processes, including hydroxyla-
tion, demethylation, dechlorination, dioxygenation, esterification, dehydrochlorination, and oxidation, during pesticide
biodegradation from varying chemical classes. The authors suggested that fungi use organic materials (pesticides) as
their carbon sources, and their long mycelial network covers a significant rhizospheric area to biodegrade various
pesticides. However, the enzymatic catalysis of pesticides by fungal enzymes is a significant bioremediation mechanism
(Ali et al., 2019). In a recent study, the biodegradation ability of the Cunninghamella elegans fungus in planktonic form
was much faster than that in biofilm form for the cyhalothrin degradation (Palmer-Brown et al., 2019). The co-cultures
of bacteria and fungi in a consortium have received priority for overcoming the limitations of the reaction optimization
for specific microorganisms. A consortium of fungi and bacteria was reported to mineralize the phenyl urea herbicide,
diuron (Ellegaard-Jensen et al., 2014). Using various types of microbes in the consortium can synergistically assist in the
4
Table 1
Pesticide biodegradation through elite bacteria strains.
Organism Pesticide Experiment type Reaction Result Reference
conditions
Acinetobacter Diazinon Batch trial 20-day batch 88.27% Amani et al.
experiment remediation (2019)
Actinobacteria Methoxychlor Lab trial 12 h in a slurry >60% biodegraded Fuentes et al.
(herbicide) bioreactor after 12 h (2014)
Alcaligenes Dieldrin and Microcosm Seven- and 14-day 39% and 74% Matsumoto et al.
endrin incubation removal (2008)
Arthrobacter sp. Atrazine In vitro lab trial Two-day in vitro 99.9% removal Cai et al. (2003)
incubation
Fipronil Sequential batch 42-day batch assay 73% removal Mandal et al.
trial (2013)
Bacillus sp. (B. Imidacloprid In vitro lab trial 25-day batch assay 25.36%–45.48% Sabourmoghaddam
thuringiensi, B. remediation et al. (2015)
subtilis, B. firmus;
Bacillus strains, DDT In vitro lab Seven-day 67.55% Powthong et al.
namely, DR-39, experiment bioassay remediation (2016)
CS-126, TL-171, Myclobutanil, Pilot (vineyard 20-day >85% biodegraded Salunkhe et al.
and TS-204; and B. tetraconazole, and plots) bioaugmentation after 20 days (2015)
s megaterium flusilazole
Mes11) (fungicide)
Mesotrione Lab assay 5 h incubation 99% remediation Carles et al. (2018)
Carbofuran Field study 60-day experiment Fivefold decrease Plangklang and
of immobilized Reungsang (2011)
Burkholderia sp. (B. supports
cepacia)
Dieldrin and Microcosm Seven- and 14-day 39% and 74% Matsumoto et al.
Chryseobacterium DDT Pilot-scale trial 45-day experiment 80.3% removal Qu et al. (2015)
sp.
Cupriavidus Dieldrin and Microcosm Seven- and 14-day 39% and 74% Matsumoto et al.
Klebsiella Imidacloprid Lab trial Seven-day lab 78% re Phugare et al.
pneumoniae incubation mediation (2013)
Novosphingobium, 2,4-D (herbicide) Lab trial Seven-day 50%–95% Dai et al. (2015)
strain DY4 bioaugmentation biodegraded after
3 and 7 days,
respectively
Chlorpyrifos Lab trial Six-day incubation 65% remediation Ajaz et al. (2012)
to attain
bioaugmentation
Imidacloprid In vitro lab trial 25-day batch assay 25.36%–45.48% Sabourmoghaddam
Pseudomonas sp.
remediation et al. (2015)
(P. putida MAS-1,
putida, P. stutzeri, DDT In vitro lab Seven-day 67.55% Powthong et al.
P. aeruginosa) experiment bioassay remediation (2016)
Atrazine In vitro lab trial Two-day in vitro 99.9% removal Cai et al. (2003)
incubation
Endosulfan In vitro lab assay Five-day 70%–80% removal Zaffar et al. (2018)
incubation
Rhizobium sp. Imidacloprid In vitro lab trial 25-day batch assay 25.36%–45.48% Sabourmoghaddam
remediation et al. (2015)
Sphingomonas sp. Chlorpyrifos In vitro bioassay Six-day incubation 78.6% remediation Feng et al. (2017)
strain HJY
Stenotrophomonas Methyl parathion, In vitro lab trial Two-day trial for 37.8%–59.7% Shen et al. (2010)
sp. SMSP-1 fenthion, and bioaugmentation removal
phoxim
complete transformation or degradation of toxic agrochemicals (Ali et al., 2019; Maqbool et al., 2016). The pathways
and mechanisms of the fungi-mediated bioremediation of pesticides are in research infancy. An encouraging approach
by Deng et al. (2015) elaborated on the cypermethrin biodegradation and the conversion of its toxic intermediates
into nontoxic products by Aspergillus niger (Fig. 2B). Lindane-tolerant fungal strains, including Aspergillus, can effectively
5
Fig. 2. Mechanism of the cyhalothrin biodegradation in Bacillus thuringiensis (A) adapted from Chen et al. (2015b) and cypermethrin biodegradation
by fungi Aspergillus niger (B) adapted from Deng et al. (2015).
deplete the lindane concentration in contaminated soils with the help of the root chemistry of rhizosphere through a
mutual understanding of the plant–fungus interaction (Asemoloye et al., 2017).
Microalgae and cyanobacteria can convert organic substances into highly economical and valuable new molecules. This
mechanism remediates pesticides in aquatic and terrestrial ecosystems using selective potential algal species (McLellan
et al., 2019) (Table 2). Green algal species, including Chlorococcum and Scenedesmus sp., efficiently remediate endosulfan
isomers and their toxic metabolite, endosulfan sulfate (Sethunathan et al., 2004). Approximately, 75%–98% of the pesticide
lindane biodegradation was achieved by a microalgal species Scenedesmus intermedius in a lab assay (González et al.,
2012). Glyphosate was inhibited using a mixed algal strain in a previous lab trial (Wang et al., 2016). The green algae
or cyanobacterial strain, Anabaena azotica, was used to degrade hexachlorocyclohexane (HCH) (Zhang et al., 2012). Lopes
et al. (2012) depicted the herbicide molinate mineralizing the microbial consortium of G. molinativorx ON4T, two strains
of Pseudomonas, Stenotrophomonas, and Achromobacter sp. for 63% mineralization of the studied agrochemical in a 42-day
batch incubation.
A consortium of several fungi–bacteria was described for an efficient pesticide bioremediation (Maqbool et al., 2016;
Ellegaard-Jensen et al. 2014). Microalgae and bacteria are prominent candidates for pesticide bioremediation (McLellan
et al., 2019). A potential microalgae–bacterial consortium was reported for the bioremediation of hexachlorocyclohexane
(lindane), DDT, and endosulfan (Zhang et al., 2012; Sethunathan et al., 2004; González et al., 2012) (Table 3). This type
of co-metabolism can be feasible in terms of the economical and ecofriendly sustainability of pesticide bioremediation.
Various factors influence the remediation rate of agrochemicals by algae, including algal strains, nature of pollutants,
and environmental factors, such as nutrients, water, pH, salinity, oxygen tension, temperature, and light intensity (Bhat
et al., 2020; Varsha et al., 2011). The most effective microalgae–bacterial consortium can be encouraged to accelerate the
co-metabolism for the effective bioremediation of several pesticides (McLellan et al., 2019; Amin et al., 2012). Therefore,
the mixed consortia or synergistic effect of the rhizosphere can enhance the fungal bioremediation of pesticides compared
to single strain degradation.
4. Enzymatic pesticide biodegradation
Bacteria and fungi produce and secrete various functional enzymes during the biodegradation approach. Various fungi
species secrete biocatalytic enzymes that can be effective in the bioremediation of pesticides and their toxic metabolites
(Maqbool et al., 2016; Spina et al., 2018). Many bacterial and fungal extracellular and lignin-degrading enzymes are
effective for the bioremediation of several pesticides (Rao et al., 2010; Bilal et al., 2019). The green catalytic degradation
of pesticides and their toxic metabolites is preferable to microbial degradation because of its simplicity in application
and prompt effectiveness (Sarker et al., 2020; Fan et al., 2013). Thus, enzymatic biodegradation is emerging as a ‘‘white
biotechnology’’ toolkit for the degradation of environmental pollutants, including pesticides.
Common biocatalytic enzymes, such as monooxygenases, oxidoreductases, dehalogenases, phosphotriesterase, es-
terases, and dioxygenases, are effective for the bioremediation of diverse chemical pesticides (Thakur et al., 2019; Riya and
6
Table 2
Fungi- and algae-mediated pesticide biodegradation.
Organism Pesticide Experiment type Reference
Fungi
Endosulfan 12-day lab incubation (100% Bhalerao and Puranik
degradation) (2007)
Aspergillus sp. (A. niger,
A. sydowii CBMAI 935) Methyl parathion 100% degradation by A. sydowii Alvarenga et al.
(20-day trial) and by P. (2014)
decanturense (30-day trial)
Boletus edulis DDT 15-day incubation (100% Huang et al. (2007)
degradation by all fungal
strains)
Chlorpyrifos 100% degradation in a five-day Silambarasan and
lab trial Abraham (2014)
Ganoderma sp. JAS4, G.
viscidus DDT 15-day incubation (100% Huang et al. (2007)
degradation by all fungal
strains)
Laccaria sp. (L. bicolor, L. DDT 15-day incubation (100% Huang et al. (2007)
scaburm) degradation by all fungal
strains)
Penicillium decanturense Methyl parathion 100% degradation by A. sydowii Alvarenga et al.
CBMAI 1234 (fungal (20-day trial) and by P. (2014)
strains) decanturense (30-day trial)
Phanerochaete sordida Clothianidin 37% degradation of the studied Mori et al. (2017)
(White-rot fungus) chlothianidin into nontoxic
metabolite TZMU within a
20-day lab trial
Trametes versicolor (pure Imiprothin + >90% degradation in 2 days Mir-Tutusaus et al.
fungal isolate) cypermethrin (mixture) for imiprothrin and 15 days for (2014)
cypermethrin
Algae
Scenedesmus intermedius Lindane 75%–98% degradation efficiency González et al. (2012)
(microalgae) at lab assay
Skeletonema costatum, Glyphosate Inhibit or use tested Wang et al. (2016)
Emiliania huxleyi (algae) glyphosate as the sole P source
in the lab assay
Isochrysis galbana Glyphosate Inhibit or use tested Wang et al. (2016)
glyphosate as the sole P source
in the lab assay
Anabaena azotica γ- Enhanced the countable Zhang et al. (2012)
(cyanobacterium) Hexachlorocyclohexane decrease in the HCH
(HCH) concentration after a five-day
exposure
Chlorococcum sp., α -Endosulfan and >90% remediation at 20-day Sethunathan et al.
Scenedesmus sp. (green endosulfan sulfate incubation for both pesticide (2004)
algae) (metabolite) and metabolite
Chlamydomonas Prometryne Nearly 100% cellular Jin et al. (2012)
reinhardtii (green algae) accumulation of pesticide at a
six-day batch assay
Jagatpati, 2012; Ortiz-Hernandez et al., 2013) (Table 4). The monooxygenases (Ese) derived from Arthrobacter sp. are ef-
fective in the bioremediation of aldrin, endosulfan, and malathion (Riya and Jagatpati, 2012; Scott et al., 2008). Glyphosate
was also successfully biodegraded by the Agrobacterium strain T10-originated enzyme oxidoreductases (Ortiz-Hernandez
et al., 2013). Malathion and methyl parathion can be effectively degraded by esterase, whereas phenylurea pesticides
can be degraded using acylamidases (Nannipieri and Bollag, 1991). However, enzymatic pesticide biodegradation may
emerge as a sustainable alternative to conventional biodegradation strategies because of its simplicity in application and
comparatively stable performance.
4.1. Application of laccase and peroxidase in pesticide biotransformation
Laccases are an important class of enzymes that can be derived from many bacterial and fungal species. Their
unique structures assist the catalysis of various toxic pollutants, such as humic acids, xenobiotics, polycyclic aromatic
hydrocarbons, pesticides, and polyphenol compounds (Bilal et al., 2019). The bacterial laccases derived from diverse
7
Table 3
Microbial mixed consortium in pesticide remediation.
Microbial consortium Pesticide Experiment type Reaction condition Result Reference
Bacterial consortium Chlorpyrifos Lab batch trial 10-day incubation 82% remediation Singh et al. (2016)
(Pseudomonas, Klebsiella,
Stenotrophomonas,
Ochrobactrum, and Bacillus and
their mixed culture)
Soil inhabiting microbial Fipronil Lab bioassay (field 19–21-day – Tan et al. (2008)
consortium (undefined) soils) incubation
Microbial consortium (G. Molinate Lab trial (paddy 42-day batch 63% mineralized Lopes et al. (2012)
molinativorx ON4T, (herbicide) field soils) incubation after 42 days
Pseudomonas (two strains),
Stenotrophomonas, and
Achromobacter)
Bacterial consortium Diuron (herbicide) Lab assay 120-day 45% mineralized Villaverde et al.
(Arthrobacter sp. N2 , Variovorax (agricultural soils) incubation after 120 days (2012)
sp. SRS16)
Mixed consortium Malathion In vitro lab assay 28 ◦ C incubation 99% removal Paris et al. (1975)
(Pseudomonas cepacian, experiment
Xanthomonas sp., Commomonas
terrigera, and Flavobacterium
meningosepticum)
Soil inhabiting mixed Monocrotophos Slurry experiment 28 ◦ C incubation 96%–98% removal Gundi and Reddy
consortium (undefined) for 20 days (2006)
Mixed consortium of soil Atrazine Site study 160-day batch 48% remediation Chirnside et al.
microbes (population density assay (2009)
1.10 × 108 CFU/mL)
Bacterial consortium Glyphosate Lab assay 18-day batch Two to three Zhao et al. (2015)
(Pseudomonas spp. strains study times of
GA07, GA09, and GC04) degradation than
non-inoculated
treatment
Bacterial consortium Endosulfan Lab trial – – Velázquez-
(Pseudomonas spinose, P. Fernández et al.
aeruginosa, and Burkholderia) (2012)
Table 4
Enzymes involved in pesticide remediation.
Enzyme Source/microorganism Pesticide Reference
Monooxygenases (Ese) Arthrobacter sp. Aldrin, endosulfan, and Riya and Jagatpati
malathion (2012), Scott et al.
(2008)
Oxidoreductases (Gox) Agrobacterium strain T10 Glyphosate Ortiz-Hernandez et al.
(2013)
Dehalogenases Sphingomonas sp. Hexachloro-cyclohexane Riya and Jagatpati
(2012), Scott et al.
(2008)
Organophosphate hydrolase Agrobacterium Methyl-paraoxon Yang et al. (2003)
(OpdA) radiobacter
Phosphotriesterase (PTE) Brevundimonas diminuta Malathion, OP substances Bigley et al. (2019)
Diisopropylfluorophosphatase Loligo vulgaris Sarin and cyclosarin Zhang et al. (2018)
(DFPase)
Esterases – Malathion and methyl Nannipieri and Bollag
parathion (1991)
Acylamidases – Phenylureas (linuron, Nannipieri and Bollag
monalide, and carboxin) (1991)
Dioxygenases (E3) Lucilia cuprina Insecticide Riya and Jagatpati (2012)
phosphodiester
Paraoxonase (PON1) Human liver Paraoxon Purg et al. (2017)
genera, such as Bacillus, Marinomonas, Azospirillum, Streptomyces, and Streptomyces, are vital for morphogenesis, spore
formation, and copper homeostasis (Fernández-Fernández et al., 2013). However, commonly used laccases are obtained
8
from saprotrophic and ligninolytic fungal species of ascomycetes, deuteromycetes, and basidiomycetes. The most common
laccase producers are Trametes versicolor, T. ochracea, T. hirsuta, T. gallica, T. villosa, Coriolopsis polizona, Cerena maxima,
Pleurotus enryngii, and Lentinus tigrinus (Madhavi and Lele, 2009; Fernández-Fernández et al., 2013).
The laccase-mediated biotransformation of xenobiotics and organic pollutants was reported in a decade-long study.
Herbicide bentazon and its metabolites can be effectively degraded using the oxidoreductive catalysis of laccase (Kim
et al., 1998). Oxidoreductase catalysts have effectively biotransformed chlorinated phenols and anilines (Park et al., 1999).
The most common coupling of laccase with chemical pollutants is followed by C–C and C–O couplings for transforming
pollutants into nontoxic metabolites, binding together by a covalent bond, or crosslinking by these couplings (Zeng et al.,
2017; Sarker et al., 2020). Laccase from Trametes versicolor showed an efficient degradation of the isoproturon pesticide
in a laccase-1-hydroxybenzotriazole (HBT) mediator catalysis (Zeng et al., 2017). Sarker et al. (2020) also reported the
degradation of 3,5-dichloroaniline, a procymidone metabolite, in laccase-catechol mediator-based catalysis. This laccase
can be used as a free enzyme or immobilized with many support materials for the remediation of various organic
pollutants (Bilal et al., 2019). A comparative study reported the reclamation of soil polluted with 2,4-dichlorophenol
by free and immobilized laccase. Laccase immobilization with suitable support materials will be more effective for the
repeated use of the laccase-based degradation of the tested 2,4-dichlorophenol (Ahn et al., 2002). The bacterial laccase
from Pseudomonas sp. with/without phenolic mediators showed an improved degradation of chlorpyrifos, dichlorvos, and
monocrotophos at 6 h of incubation in a laboratory experiment (Chauhan and Jha, 2018).
Lignin peroxidase derived from diverse microbes, including bacteria and fungi, can be used as a potential bio-degrader
(Maqbool et al., 2016). Pesticide removal by oxidoreductase catalysts that originate from a consortium of bacteria and
fungi was reported (Hai et al., 2012; Maqbool et al., 2016). Another peroxidase source is the horseradish plant root. The
horseradish-derived peroxidase is effective in glyphosate (Pizzul et al., 2009) and 1-naphthol (a carbamate metabolite)
(Islam et al., 2014) bioremediation. The peroxidase activities from Shepherd’s purse root crude extract with an H2 O2
activator reported 78% removal of 2,4-dichlorophenol in a 30-min laboratory assay (Park et al., 2006). Table 5 presents
the selected laccase- and peroxidase-based pesticide bioremediation.
5. Potentials of plant growth-promoting rhizobacteria in pesticide degradation
The plant growth-promoting rhizobacteria (PGPR) are a group of bacteria that effectively colonize the plant rhizosphere
and enhance the plant growth and development (Rani et al., 2019; Islam and Hossain, 2012). Certain PGPR can fix
atmospheric nitrogen for the nitrogen nutrition of plants. They also promote the nutrition of phosphorous, potassium,
and zinc by solubilizing these essential elements from soils (Islam and Hossain, 2012; Sarker et al., 2014). Bacteria
from the diverse genera, such as Bacillus, Pseudomonas, Paraburkholderia, Enterobacter, Sphingomonas, Serratia, Klebsiella,
Arthrobacter, Azotobacter, and Rhizobium have been reported as PGPR (Islam et al., 2016, 2019; Khan et al., 2016; Rahman
et al., 2018).
Further, PGPR can be used as a driver of the bioremediation for pesticide-contaminated sites (Rani et al., 2019).
Pyrethroid pesticides can be hydrolyzed by PGPR, such as the Klebsiella sp. strain ZD112-derived esterase, in a batch
experiment (Wu et al., 2006). Two PGPR strains, namely Serratia sp. and Pseudomonas sp., were effectively used in a four-
day trial for 80%–92% diazinon degradation (Cycoń et al., 2009). Endosulfan was degraded by Staphylococcus equorum,
Enterobacter sp., and Bacillus subtilis in a 21-day batch trial experiment (Bhattacharjee et al., 2014). Fig. 3 illustrates
the proposed metabolic pathways of endosulfan biodegradation by Bacillus subtilis and Pseudomonas sp. (Kumar et al.,
2014; Bajaj et al., 2010). Giri and Rai (2012) showed the potentiality of Pseudomonas fluorescens for the endosulfan isomer
biodegradation. The potential strains of Arthrobacter sp. DNS10 co-cultured with Enterobacter sp. P1 was a significantly
remediated pesticide atrazine in a 60 h batch experiment (Jiang et al., 2019a). The DDT biodegradation was achieved
by Bacillus sp. in a five-day lab experiment (Pant et al., 2013). Table 6 presents the use of various PGPR in pesticide
bioremediation. Zhang et al. (2020) documented the biotransformation of residual herbicide, including nicosulfuron,
through a climate chamber study using Bacillus subtilis strains. Thus, a countable number of PGPR has been found to
exhibit prospective for pesticide biodegradation. Another study also noticed the soil pH and soil organic matter (SOM) as
the triggering factors for the bioremediation and phytoremediation potentialities along with the adsorption/desorption of
bound atrazine in laterite soils (Lin et al., 2018). However, several research uncertainties, including performance stability
under real field conditions, adaptation in adverse climatic conditions, lack of perfect formulation, and survival of PGPR
strains under infertile soils, may limit extensive field applications (Tarla et al., 2020).
6. Underlying mechanism and molecular advancement of pesticide bioremediation
The basic science of pesticide breakdown comprises three significant stages, namely hydrolysis, oxidation or reduction
(redox), and expansion. The hydrolysis of a pesticide is supported by hydrophilic environmental factors, followed by
oxidation/reduction, adjusting the redox condition of the compound (Scott et al., 2011). The significant chemical group
in the compound chooses whether it will experience oxidation or reduction. The last step is an expansion/addition to
the development of a new reaction product/metabolite (Sun et al., 2020). Most bacteria and fungi can secrete functional
enzymes; therefore, the enzymatic catalysis governs the chief metabolic pathways of pesticide biodegradation (Rao et al.,
2010). The complex and accurate mechanisms of pesticide degradation by microorganisms or their enzymes are still
9
Table 5
Laccase and peroxidase in pesticide biodegradation.
Enzyme Enzyme source Enzyme activity Pesticide Result Reference
name
Laccase Trametes versicolor Free enzyme with HBT Isoproturon 68%–100% Zeng et al. (2017)
mediator degradation at 24 h
incubation
Laccase Trametes versicolor Free optimized enzyme Procymidone and 90%–100% Sarker et al.
with catechol mediator 3,5-DCA (metabolite) degradation at 24 h (2020)
incubation
Laccase Pseudomonas sp. Free enzyme Chlorpyrifos, 45%–83% degradation Chauhan and Jha
with/without mediators dichlorophos, and at 6 h incubation (2018)
monocrotophos
Laccase Trametes versicolor Free enzyme with Glyphosate 40%–90% degradation Pizzul et al. (2009)
various mediators at 24 h incubation
Laccase Trametes versicolor Optimized free enzyme Bentazone, Various degrees of Kupski et al.
with vanillin mediator carbofuran, diuron, degradation in the (2019)
clomazone, batch assay
tebuconazole, and
pyraclostrobin
Laccase Trametes versicolor Free enzyme with Pyrimethanil, 100% degradation at Jin et al. (2016)
violuric acid mediator isoproturon 24 h incubation assay
Laccase Coriollopsis Physical absorption with dichlorophen Efficient oxidation of Vidal-Limon et al.
gallica activated cellulose pesticide with ABTS (2018)
nanofibers mediator
Laccase Trametes versicolor Covalent binding with Chlorpyrifos Degrade >90% Das et al. (2017)
chitosan-coated pesticide at 12 h
nanoparticles incubation
Laccase Aspergillus sp. Crosslinking with 2,4-Dichlorophenol 42.28% removal of Yang et al. (2016)
mesoporous silica pesticide at 24 h
incubation
Peroxidase Horseradish HRP with H2 O2 1-Naphthol 79% transformation of Islam et al. (2014)
(metabolite of 1-naphthol at 3 h
carbamate pesticide) incubation
Peroxidase Shepherd’s purse Peroxidase with H2 O2 2,4-Dichorophenol 78% removal at 30 Park et al. (2006)
activator min incubation
Peroxidase Horseradish Free enzyme with Glyphosate 53% removal without Pizzul et al. (2009)
peroxide activator mediator, 795
removal in presence
of H2 O2 at 5 h
incubation
poorly known. However, based on chemical groups and molecular docking properties, some proposed metabolic pathways
for pesticide biodegradation exist (Bilal et al., 2019). The proposed biodegradation of the isoproturon pesticide and the
metabolic transformation mechanisms by the Tramates versicolor-derived laccase-based HBT mediator system (LMS) are
based on one-electron oxidation through oxidoreductase (Fig. 4) (Zeng et al., 2017). However, a recent study depicted
the degradation pathway for 3,5-dichloroaniline, a prime toxic metabolite of procymidone, by a LMS using catechol
as a mediator while a phenolic mediator may act as a shuttle for the oxidation of aniline products through laccase
active sites (Fig. 5) (Sarker et al., 2020). A previously published study described the laccase-mediated transformation
of herbicide bentazon and its metabolite by the proposed oligomerization and polymerization for a final reaction product.
The formation of a covalent bond between the studied chemicals and metabolites was thought to be cross-coupled among
the intermediate products. The final reaction product was proposed as a dimeric compound with a molecular weight of
510 and two catechol-mediated trimeric isomers with molecular weights of 764 and 728 (Kim and Kim, 2005).
Functional biology coupled with bioinformatics for gene and protein studies through genomics and in silico approach
is a popular strategy for screening contemporary microbe- and enzyme-based bioremediation (Purohit et al., 2018; Sun
et al., 2020). Therefore, the revolution of computer studies in systems biology and informatics could generate new
postgenomic multi-OMIC approaches. Among OMICs, genomics is a popular and emerging field for searching novel genes
for pollutant degradation (Table 7). Microbial genomics and metagenomic strategies are widely used to codify the enzyme
and the genes related to xenobiotic transformation (Rodríguez et al., 2020; Jiang et al., 2019b). Several elite genes,
including ophB, ampA, opdE, opd, opdA, and mpd, are isolated from six organophosphate-degrading bacterial isolates that
are functionally capable of degrading organophosphate insecticides (Jiang et al., 2019b). Likewise, lin genes (i.e., lin, linA,
linB, and linC) were identified as potential genes from Sphingomonas strains coupled with dehalogenase enzymes for
10
Fig. 3. Proposed metabolic pathways of the endosulfan biodegradation by Bacillus subtilis and Pseudomonas sp. adapted from the previous studies
of Kumar et al. (2014) and Bajaj et al. (2010). The dotted black lines indicate the metabolism pathway by Pseudomonas sp. The solid blue lines
represent the mechanism by Bacillus subtilis.
Fig. 4. Degradation mechanism of isoproturon catalyzed by the laccase-HBT system, initial dimerization processes (A), and subsequent coupling
processes (B).
Source: Reprinted from Zeng et al. (2017), an open-access article published under the CC-BY license.
11
Table 6
Potentials of the PGPR in pesticide bioremediation.
Pesticide PGPR Incubation condition Result Reference
Pyrethroids Klebsiella sp. strain Batch incubation at 7.0 Pyrethroid hydrolysis by Wu et al. (2006)
ZD112 pH, 30 ◦ C PGPR-derived esterase
Diazinon Serratia sp. and Four-day batch trial at 80%–92% degradation by Cycoń et al. (2009)
Pseudomonas sp. 7.0 pH, 30 ◦ C for both in a four-day trial
vitro and soil
experiments
Propoxur (Carbamate) Syntrophic bacterial Four-week trial in a Propoxur is completely Kim et al. (2017)
isolates shaking incubator at 28 degraded through a
◦
(Pseudaminobacter sp. C with optimum syntrophic interaction
SP1a and Nocardioide sp. reaction condition
SP1b)
Atrazine Arthrobacter sp. DNS10 60 h batch trial in a lab >99% degradation of Jiang et al. (2019b)
co-culture with under optimum reaction atrazine with
Enterobacter sp. P1. condition metabolites
Type-II pyrethroids Acinetobacter sp. strain Five-day batch trial at 34%–74% degradation of Jin et al. (2014)
(cypermethrin, JN8 7.0 pH, 35 ◦ C for both in the tested pesticides
fenpropathrin, vitro assay within 5 days
fenvalerate, and
deltamethrin)
Acetaprimid Variovorax 120 h incubation in 41.6% degraded after 120 Sun et al. (2017)
boronicumulans CGMCC shaking incubator at 7.0 h
4969 and its enzymatic pH
mechanism
DDT Bacillus sp. Five-day incubation at 89.3% degradation during Pant et al. (2013)
optimum condition incubation
Staphylococcus equorum, 21-day incubation at 30 81.45% degradation by S. Bhattacharjee et al.
◦
Enterobacter sp. C, pH 8.0 equorum, 82.87% (2014)
Bacillus subtilis degradation by
Enterobacter sp. and
Endosulfan and its 83.69% degradation by B.
isomers subtilis
Pseudomonas fluorescens 15-day batch trial at α -Endosulfan 92.80% and Giri and Rai (2012)
optimum reaction β -endosulfan 79.35%
condition degradation by P.
fluorescens
Pseudomonas aeruginosa 15-day incubation at 28 α - and γ -HCH 98%, Kumar et al. (2006)
◦
C β -HCH 17%, and δ -HCH
Hexachlorocyclohexane 76% degradation
(HCH) and its isomer Bacillus circulans, Bacillus Eight-day incubation for α -HCH 80.7%, β -HCH Gupta et al. (2000)
brevis α - and γ -isomers and 39.7%, and γ -HCH 94.6%
28 days for β -isomers at degradation
optimum condition
the degradation of organochlorine insecticide hexachlorocyclohexane (HCH) (Boltner et al., 2005). The hydrolase enzyme-
mediated genes (i.e., mpd, opd, phnE, glpT, and pdeA) were characterized and screened from Achromobacter for the efficient
degradation of organophosphate insecticides (Somara et al., 2002). Similarly, a biometer assay was conducted to screen
the Atz and Trz pathway catabolic genes during the microbial remediation of atrazine (Douglass et al., 2017), while a
total gene profiling noticed that the variation in the trzN gene numbers was strongly linked to the enhancement of the
atrazine biodegradation (Sagarkar et al., 2013). However, genomic and metagenomic studies were limited to cultivable
and screened biodegraders. To overcome these constraints, stable isotope probing (SIP) using potential stable isotope-
labeled elements (e.g., 13 C, 18 O, or 15 N) can be incorporated into the cellular organelles of potential and uncultivable
biodegraders as a robust in-situ toolkit for scrutinizing and characterizing uncultivable microorganisms concerning
pesticide biodegradation (Jiang et al., 2018). Therefore, these advanced genetic and biotechnological rectifications of
xenobiotic and pesticide bioremediation will open a new avenue for achieving a sustainable and consistent performance
of the biodegradation potentiality.
7. Challenges and prospective of pesticide biodegradation
The major drawback of commercializing microbe-mediated pesticide biodegradation is the inconsistent performance
during field experiments in real growing conditions using screened potential microbial strains from lab trials (Sun et al.,
2020; Tarla et al., 2020). However, most of the potential microbes for the pesticide bioremediation in field conditions
12
Fig. 5. Schematic showing the transformation of 3,5-dichloroaniline (3,5-DCA) through the laccase mediator system (LMS) (a) and the MnO2 -mediator
system (MMS) using catechol as a humic phenolic monomer. The final reaction product should be an oligomer or a polymer of the transformed
intermediates.
Source: Adapted from (Sarker et al., 2020).
Table 7
Selected genome studies of the microorganisms reported for pesticide degradation.
Pesticide chemical class Pesticide name Screened microorganism Genomics method Reference
DDT Stenotrophomonas sp. DDT-1 MiSeq Pan et al. (2016)
Organochlorine Alachlor and Endosulfan Micrococcus sp. strain 2385 HiSeq 2000 Pathak et al. (2016)
Lindane Pseudomonas aeruginosa MTB-1 454 GS-FLX Ohtsubo et al. (2014)
Chlorpyrifos Cupriavidus nantongensis X1 HiSeq 2500 Fang et al. (2016)
Organophosphate Methyl parathion Burkholderia sp. strain MP-1 MiSeq Liu et al. (2014)
Glyphosate Enterobacter sp. E20 HiSeq 2000 Cao et al. (2019)
Anilinopyrimidine Cyprodinil Acinetobacter johnsonii LXL_C1 HiSeq Wang et al. (2019)
Carbamates Carbaryl Pseudomonas putida XWY-1 MiSeq Zhu et al. (2019)
Pyrethroid Deltamethrin Lysinibacillus sp. ZJ6 HiSeq 4000 Hao et al. (2018)
Neonicotinoid Acetaprimid Pigmentiphaga sp. strain D-2 MiSeq Yang et al. (2020)
Triazines Atrazine Arthrobacter sp. ZXY-2 Pacific Biosciences Zhao et al. (2017)
(PacBio RS II)
require some adaptation with environmental factors, such as temperature, pH, humidity, and SOM (Bilal et al., 2019;
Cycon et al., 2017). Most bacterial and fungal strains require optimum growing conditions for their growth and fecundity
(Zeng et al., 2017; Maqbool et al., 2016). Additionally, the competitive action between the biodegraders and the pathogenic
microbes may limit the expected growth of target microbes during the bioremediation process (Goodwin et al., 2017).
Therefore, a compatible microbial consortium for the co-metabolism and transformation of the target pesticides and
agrochemicals has been considered as an alternative to the single strain-mediated bioremediation to compensate for
the single microbe potentiality (McLellan et al., 2019; Morillo and Villaverde, 2017). Furthermore, microbe-originated
enzymes/biomolecules (as a part of white biotechnology) have been used to accelerate bioremediation approaches toward
the sustainable management of pesticide-contaminated sites to resolve the microbial limitations of formulation, pH,
temperature, and application difficulties in the pesticide bioremediation (Rao et al., 2010; Bilal et al., 2019). The enzymatic
catalysis is relatively stable and easy to apply compared to microbial bioremediation (Sarker et al., 2020; Bilal et al., 2019).
The advancement in genetic engineering and biotechnological approaches for the rectification of bio-cleanup tech-
niques for pesticides has been called a revolution in bioremediation (Wang et al., 2012; Sun et al., 2020). Among
the various gene-editing approaches, TALEN, ZNFs, and CRISPR-Cas are popular and widely used as gene-editing tools.
The prime objective of gene editing is to alter the wild genome using a specific target restriction enzyme to build
a new potential target genome complex through multi-OMIC approaches (e.g., transcriptomics, genomics, proteomics,
metagenomics, and metabolomics) (Hussain et al., 2009; Kumar et al., 2015; Manzoni et al., 2016; Jaiswal et al., 2019;
13
Islam et al., 2019). Moreover, SIP is a vital and advanced approach for screening and characterizing the functional yet
uncultivable microbes for pesticide bioremediation (Jiang et al., 2018), which can be coupled with nanotechnology and
omics-driven approaches for a holistic improvement of the microbial pesticide bioremediation (Zhang et al., 2015). The
limiting factors (e.g., pH, temperature, and formulation for long storage) of microbe- and enzyme-based bioremediation
can be stabilized through the immobilization of potential microbial cells and microbe-derived enzymes with compatible
support surfaces for the establishment of a nano-hybrid structure for sustainable and commercial applications.
Another important factor of the sustainability of the microbial biodegradation of pesticides is the comparative assess-
ment for cost effectiveness. In general, bioremediation is mostly performed under in-situ conditions and comparatively
low-cost technology due to no potential expenditure for transportation or excavations (Tarla et al., 2020; Jiang et al., 2018).
A previous study documented that the average cost of commercial chemical treatment for pesticide remediation (250–
500 USD/t) is comparatively higher than the operational cost for general biological remediation (40–70 USD/t) (Eykelbosh,
2014), which is pretty lower than the other conventional and physical approaches, such as incineration and landfills (200–
1000 USD/m3 ) (Anjum et al., 2012). Thus, bioremediation through prospective microbes and their functional enzymes
can reduce substantial costing (60%–80% reduction) compared to conventional approaches (Sun et al., 2020; Tarla et al.,
2020). Hence, microbial pesticide bioremediation is considered a low-cost and sustainable green technology. Despite a
huge advancement in the bioremediation technology in terms of scrutinizing and boosting the genetic make-up have
been achieved for abatement of pesticides, there are still few research uncertainties such as in-situ slowness in real
field conditions, partial degradation leading to uncertain metabolites, mobility, and further ecotoxicology of transferred
metabolites, the stability under adverse climatic conditions, and incompatibility with contemporary approaches are
prevailing, which needs to be explored with meticulous, adaptive, and applied research.
8. Conclusion
The bioremediation of pesticides and other hazardous synthetic agrochemicals using potential microorganisms and
their functional enzymes is a promising sustainable approach for the reclamation of contaminated sites and farmlands.
This approach is comparatively cost-effective, ecofriendly, and non-destructive compared to physical and chemical
remediation techniques. However, the microbial and enzymatic bioremediation of pesticides and their toxic metabolites
has exhibited several limitations, such as optimal growing conditions, inconsistent performance, slow adaptation with the
adverse environment, and specificity to pesticides. Nonetheless, progress has been achieved in numerous biotechnological
and other technical optimizations for the advancement of formulation and consistent performance. The recent progress
in genomics, post-genomics, and gene-editing technologies would facilitate a better understanding of the underlying
molecular mechanisms of bioremediation and their wider practical application reclamation of pesticide-contaminated
sites through bioremediation. This comprehensive review is a critical guide for pinpointing the challenges and research
uncertainties concerning the sustainable and green remediation of hazardous pesticide residues in contaminated sites and
farmlands.
CRediT authorship contribution statement
Aniruddha Sarker: Conceptualization, Methodology, Data curation, Writing - review & editing. Rakhi Nandi: Method-
ology, Writing - review & editing. Jang-Eok Kim: Conceptualization, Writing - review & editing, Visualization. Tofazzal
Islam: Conceptualization, Methodology, Writing - review & editing, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgment
Authors are grateful to Kyungpook National University, Republic of Korea and IBGE, BSMRAU, Bangladesh for the
technical supports such as proofreading, data review, and similarity checking during the entire period of writing the
paper.
References
Ahn, M.Y., Dec, J., Kim, J.E., Bollag, J.M., 2002. Treatment of 2, 4-Dichlorophenol polluted soil with free and immobilized laccase. J. Environ. Qual. 31
(5), 1509–1515.
Ajaz, M., Rasool, S.A., Khan Sherwani, S., Ali, T.A., 2012. High profile chlorpyrifos degrading pseudomonas putida MAS-1 from indigenous soil: Gas
chromatographic analysis and molecular characterization. Int. J. Basic Med. Sci. Pharm. 2 (2), 58–61.
Ali, N., Khan, S., Khan, M.A., Waqas, M., Yao, H., 2019. Endocrine disrupting pesticides in soil and their health risk through ingestion of vegetables
grown in Pakistan. Environ. Sci. Pollut. Res. 1–13.
Alvarenga, N., Birolli, W.G., Seleghim, M.H., Porto, A.L., 2014. Biodegradation of methyl parathion by whole cells of marine derived fungi Aspergillus
sydowii and Penicillium decaturense. Chemosphere 117, 47–52.
14
Amani, F., Sinegani, A.A.S., Ebrahimi, F., Nazarian, S., 2019. Biodegradation of chlorpyrifos and diazinon organophosphates by two bacteria isolated
from contaminated agricultural soils. Biol. J. Microorg. 7 (28), 27–39.
Amin, S.A., Parker, M.S., Armbrust, E.V., 2012. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76 (3), 667–684.
Anjum, R., Rahman, M., Masood, F., Malik, A., 2012. Bioremediation of pesticides from soil and wastewater. In: Environmental Protection Strategies
for Sustainable Development. Springer, Dordrecht, pp. 295–328.
Asemoloye, M.D., Ahmad, R., Jonathan, S.G., 2017. Synergistic rhizosphere degradation of γ -hexachlorocyclohexane (lindane) through the combinatorial
plant-fungal action. PLoS One 12 (8), e0183373.
Bajaj, A., Pathak, A., Mudiam, M.R., Mayilraj, S., Manickam, N., 2010. Isolation and characterization of a Pseudomonas sp. strain IITR01 capable of
degrading α -endosulfan and endosulfan sulfate. J. Appl. Microbiol. 109 (6), 2135–2143.
Barbieri, M.V., Postigo, C., Guillem-Argiles, N., Monllor-Alcaraz, L.S., Simionato, J.I., Stella, E., de Alda, M.L., 2019. Analysis of 52 pesticides in fresh
fish muscle by QuEChERS extraction followed by LC-MS/MS determination. Sci. Total Environ. 653, 958–967.
Baron, G.L., Jansen, V.A.A., Brown, M.J.F., et al., 2017. Pesticide reduces bumblebee colony initiation and increases probability of population extinction.
Nat. Ecol. Evol. 1, 1308–1316.
Bhalerao, T.S., Puranik, P.R., 2007. Biodegradation of organochlorine pesticide, endosulfan, by a fungal soil isolate, Aspergillus niger. Int. Biodeterior.
Biodegrad. 59, 315–321.
Bhat, S.A., Qadri, H., Cui, G., Li, F., 2020. Remediation of pesticides through microbial and phytoremediation techniques. In: Fresh Water Pollution
Dynamics and Remediation. Springer Nature Singapore Pte. Ltd., pp. 235–245.
Bhattacharjee, K., Banerjee, S., Bawitlung, L., Krishnappa, D., Joshi, S.R., 2014. A study on parameters optimization for degradation of endosulfan by
bacterial consortia isolated from contaminated soil. Proc. Natl. Acad. Sci. India B 84 (3), 657–667.
Bigley, A.N., Desormeaux, E., Xiang, D.F., Bae, S.Y., Harvey, S.P., Raushel, F.M., 2019. Overcoming the challenges of enzyme evolution to adapt
phosphotriesterase for V-agent decontamination. Biochem 58, 2039–2053.
Bilal, M., Iqbal, H.M.N., Barceló, D., 2019. Persistence of pesticides-based contaminants in the environment and their effective degradation using
laccase-assisted biocatalytic systems. Sci. Total Environ. 695.
Boltner, D., Moreno-Morillas, S., Ramos, J.L., 2005. 16S rDNA phylogeny and distribution of lin genes in novel hexachlorocyclohexane-degrading
Sphingomonas strains. Environ. Microbiol. 7, 1329–1338.
Cai, B., Han, Y., Liu, B., Ren, Y., Jiang, S., 2003. Isolation and characterization of an atrazine- degrading bacterium from industrial wastewater in China.
Lett. Appl. Microbiol. 36, 272–276.
Cao, G., Jia, X., Zheng, Y., 2019. Draft genome sequence of Enterobacter sp. E20, isolated from glyphosate polluted soil. http://dx.doi.org/10.25236/
isafb.2019.036.
Carles, L., Joly, M., Bonnemoy, F., Leremboure, M., Donnadieu, F., Batisson, I., BesseHoggan, P., 2018. Biodegradation and toxicity of a maize herbicide
mixture: Mesotrione, nicosulfuron and S-metolachlor. J. Hazard. Mater. 354, 42–53.
Chauhan, P.S., Jha, B., 2018. Pilot scale production of extracellular thermo-alkali stable laccase from Pseudomonas sp. S2 using agro waste and its
application in organophosphorus pesticides degradation. J. Chem. Technol. Biotechnol. 93 (4), 1022–1030.
Chen, M., Chang, C.-H., Tao, L., Lu, C., 2015a. Residential exposure to pesticide during childhood and childhood cancers: a meta-analysis. Pediatrics
136 (4), 719–729.
Chen, S., Deng, Y., Chang, C., Lee, J., Cheng, Y., Cui, Z., Zhou, J., He, F., Hu, M., Zhang, L.-H., 2015b. Pathway and kinetics of cyhalothrin biodegradation
by Bacillus thuringiensis strain ZS-19. Sci. Rep. 5, 8784.
Chirnside, A.E., Ritter, W.F., Radosevich, M., 2009. Biodegradation of aged residues of atrazine and alachlor in a mix-load site soil. Soil. Biol. Biochem.
41, 2484–2492.
Chrinside, A.E., Ritter, W.F., Radosevich, M., 2011. Biodegradation of aged residues of atrazine and alachlor in a mix-load site soil by fungal enzymes.
Appl. Environ. Soil Sci. 1–10.
Cycon, M., Mrozik, A., Piotrowska-Seget, Z., 2017. Bioaugmentation as a strategy for the remediation of pesticide-polluted soil: A review. Chemosphere
172, 52–71.
Cycoń, M., Wójcik, M., Piotrowska-Seget, Z., 2009. Biodegradation of the organophosphorus diazinon by Serratia sp. and pseudomonas sp. and their
use in bioremediation of contaminated soil. Chemosphere 76 (4), 494–501.
Dai, Y., Li, N., Zhao, Q., Xie, S., 2015. Bioremediation using Novosphingobium strain DY4 for 2, 4-dichlorophenoxyacetic acid-contaminated soil and
impact on microbial community structure. Biodegradation 26, 161–170.
Das, A., Singh, J., Yogalakshmi, K.N., 2017. Laccase immobilized magnetic iron nanoparticles: fabrication and its performance evaluation in chlorpyrifos
degradation. Int. Biodeterior. Biodegrad. 117, 183–189.
Deng, W., Lin, D., Yao, K., Yuan, H., Wang, Z., Li, J., Zou, L., Han, X., Zhou, K., He, L., 2015. Characterization of a novel β -cypermethrin-degrading
Aspergillus niger YAT strain and the biochemical degradation pathway of β -cypermethrin. Appl. Microbiol. Biotechnol. 99 (19), 8187–8198.
Dhaliwal, S.S., Singh, J., Taneja, P.K., Mandal, A., 2020. Remediation techniques for removal of heavy metals from the soil contaminated through
different sources: a review. Environ. Sci. Pollut. Res. 27 (2), 1319–1333.
Douglass, J.F., Radosevich, M., Tuovinen, O.H., 2017. Microbial attenuation of atrazine in agricultural soils: Biometer assays, bacterial taxonomic
diversity, and catabolic genes. Chemosphere 176, 352–360.
Ellegaard-Jensen, L., Knudsen, B.E., Johansen, A., Albers, C.N., Aamand, J., Rosendahl, S., 2014. Fungal–bacterial consortia increase diuron degradation
in water-unsaturated systems. Sci. Total Environ. 466, 699–705.
Eykelbosh, A., 2014. Short- and Long-Term Health Impacts of Marine and Terrestrial Oil Spills. Vancouver Coastal Health.
Fan, B., Zhao, Y., Mo, G., Ma, W., Wu, J., 2013. Co-remediation of DDT-contaminated soil using white rot fungi and laccase extract from white rot
fungi. J. Soils Sediments 13, 1232–1245.
Fang, L.C., Chen, Y.F., Wang, D.S., Sun, L.N., Tang, X.Y., Hua, R.M., 2016. Complete genome sequence of a novel chlorpyrifos degrading bacterium,
Cupriavidus nantongensis X1. J. Biotechnol. 227, 1–2.
Feng, F., Ge, J., Li, Y., Cheng, J., Zhong, J., Yu, X., 2017. Isolation, colonization, and chlorpyrifos degradation mediation of the endophytic bacterium
Sphingomonas Strain HJY in Chinese Chives [Allium tuberosum]. J. Agric. Food Chem. 65 (6), 1131–1138.
Fernández-Fernández, M., Sanromán, M.Á., Moldes, D., 2013. Recent developments and applications of immobilized laccase. Biotechnol. Adv. 31,
1808–1825.
Fuentes, M.S., Alvarez, A., Saez, J.M., Benimeli, C.S., Amoroso, M.J., 2014. Use of Actinobacteria consortia to improve methoxychlor bioremediation in
different contaminated matrices. In: Bioremediation in Latin America. Current Res. Pers.. pp. 267–277.
Gavrilescu, M., 2005. Fate of pesticides in the environment. Eng. Life Sci. 5, 497–526.
Giri, K., Rai, J.P.N., 2012. Biodegradation of endosulfan isomers in broth culture and soil microcosm by Pseudomonas fluorescens isolated from soil.
Int. J. Environ. Stud. 69 (5), 729–742.
González, R., García-Balboa, C., Rouco, M., Lopez-Rodas, V., Costas, E., 2012. Adaptation of microalgae to lindane: a new approach for bioremediation.
Aquat. Toxicol. 109, 25–32.
Goodwin, L., Carra, I., Campo-Moreno, P., Soares, A., 2017. Treatment options for reclaiming wastewater produced by the pesticide industry. Int. J.
Water Wastewater Treat. 4 (1), http://dx.doi.org/10.16966/2381-5299.149.
15
Gundi, V.A., Reddy, B., 2006. Degradation of monocrotophos in soils. Chemosphere 62, 396–403.
Gupta, A., Kaushik, C.P., Kaushik, A., 2000. Degradation of hexachlorocyclohexane (hch; α , β , γ and δ ) by Bacillus circulans and Bacillus brevis isolated
from soil contaminated with HCH. Soil Biol. Biochem. 32 (11–12), 803–1805.
Hai, F.I., Modin, O., Yamamoto, K., Fukushi, K., Nakajima, F., Nghiem, L.D., 2012. Pesticide removal by a mixed culture of bacteria and white rot fungi.
J. Taiwan Inst. Chem. Eng. 43 (3), 459–462.
Hao, X., Zhang, X., Duan, B., Huo, S., Lin, W., Xia, X., Liu, K., 2018. Screening and genome sequencing of deltamethrin-degrading bacterium ZJ6. Curr.
Microbiol. 75, 1468–1476.
Harms, H., Schlosser, D., Wick, L.Y., 2011. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat. Rev. Microbiol. 9 (3),
177–192.
Huang, Y., Xiao, L., Li, F., Xiao, M., Lin, D., Long, X., et al., 2018. Microbial degradation of pesticide residues and an emphasis on the degradation of
cypermethrin and 3-phenoxy benzoic acid: a review. Molecules 23 (2313).
Huang, Y., Zhao, X., Luan, S., 2007. Uptake and biodegradation of DDT by 4 ectomycorrhizal fungi. Sci. Total Environ. 385, 235–241.
Hussain, S., Siddique, T., Arshad, M., Saleem, M., 2009. Bioremediation and phytoremediation of pesticides: Recent advances. Criti. Rev. Environ. Sci.
Technol. 39 (10), 843–907.
IRAC, 2020. The IRAC mode of action classification. https://irac-online.org/modes-of-action/. (Accessed 27 May 2020).
Islam, M.T., Hossain, M.M., 2012. Plant probiotics in phosphorus nutrition in crops, with special reference to rice. In: Bacteria in Agrobiology: Plant
Probiotics. Springer, Berlin Heidelberg, pp. 325–363.
Islam, A.K.M.M., Lee, S.E., Kim, J.E., 2014. Enhanced enzymatic transformation of 1-naphthol in the presence of catechol by peroxidase. J. Kor. Soc.
Appl. Biol. Chem. 57 (2), 209–215.
Islam, M.T., Rahman, M.M., Pandey, P., Boehme, M.H., Haesaert, G. (Eds.), 2019. Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol.
Springer.
Islam, M.T., Rahman, M., Pandey, P., Jha, C.K., Aeron, A. (Eds.), 2016. Bacilli and Agrobiotechnology. Springer, pp. 1–416.
Jaiswal, S., Singh, D.K., Shukla, P., 2019. Gene editing and systems biology tools for pesticide bioremediation: A review. Front. Microbiol. 10, 1–13.
Jiang, B., Jin, N., Xing, Y., Su, Y., Zhang, D., 2018. Unraveling uncultivable pesticide degraders via stable isotope probing (SIP). Crit. Rev. Biotechnol.
38 (7), 1025–1048.
Jiang, Z., Zhang, X., Wang, Z., Cao, B., Deng, S., Bi, M., Zhang, Y., 2019b. Enhanced biodegradation of atrazine by arthrobacter sp. DNS10 during
co-culture with a phosphorus solubilizing bacteria: enterobacter sp. P1. Ecotoxicol. Environ. Safety 172, 159–166.
Jiang, B., et al., 2019a. Microbial degradation of organophosphorus pesticides: novel degraders, kinetics, functional genes, and genotoxicity assessment.
Environ. Sci. Pollut. Res. 26 (21), 21668–21681.
Jin, Z., Guo, Q., Zhang, Z., Yan, T., 2014. Biodegradation of type II pyrethroids and major degraded products by a newly isolated Acinetobacter sp.
strain JN8. Can. J. Microbiol. 60 (8), 541–545.
Jin, Z.P., Luo, K., Zhang, S., Zheng, Q., Yang, H., 2012. Bioaccumulation and catabolism of prometryne in green algae. Chemosphere 87 (3), 278–284.
Jin, X., Yu, X., Zhu, G., Zheng, Z., Feng, F., Zhang, Z., 2016. Conditions optimizing and application of laccase-mediator system (LMS) for the
laccase-catalyzed pesticide degradation. Sci. Rep. 6 (35787).
Kaur, R., Bhatti, S.S., Singh, S., Singh, J., Singh, S., 2018. Phytoremediation of heavy metals using cotton plant: a field analysis. Bull. Environ. Contam.
Toxicol. 101 (5), 637–643.
Khan, M.M.A., Khatun, A., Islam, M.T., 2016. Promotion of Plant Growth By Phytohormone Producing Bacteria. Microbes in Action. Nova Sci. Publishers,
New York, NY, USA.
Kim, J.S., Kim, J.E., 2005. Polymerization of the herbicide bentazon and its metabolite with humic monomers by oxidoreductive catalysts. In:
Environmental Fate and Safety Management of Agrochemicals. In: ACS Symposium Series, vol. 899, American Chemical Society, Washington,
DC.
Kim, H., Kim, D.-U., Lee, H., Yun, J., Ka, J.-O., 2017. Syntrophic biodegradation of propoxur by Pseudaminobacter sp. SP1a and Nocardioides sp. SP1b
isolated from agricultural soil. Int. Biodeterior. Biodegrad. 118, 1–9.
Kim, J.E., Wang, C.J.J., Bollag, J.M., 1998. Interaction of reactive and inert chemicals in the presence of oxidoreductases: reaction of the herbicide
bentazon and its metabolites with humic monomers. Biodegradation 8, 387–392.
Kumar, A., Bhoot, N., Soni, I., John, P.J., 2014. Isolation and characterization of a Bacillus subtilis strain that degrades endosulfan and endosulfan
sulfate. 3 Biotech 4 (5), 467–475.
Kumar, M., Gupta, S.K., Garg, S.K., Kumar, A., 2006. Biodegradation of hexachlorocyclohexane-isomers in contaminated soils. Soil Biol. Biochem. 38
(8), 2318–2327.
Kumar, S., Kaushik, G., Dar, M.A., Nimesh, S., Lopez-Chuken, U.J., Villarreal-Chiu, J.F., 2018b. Microbial degradation of organophosphate pesticides: a
review. Pedosphere 28 (2), 190–208.
Kumar, S., Krishnani, K.K., Bhushan, B., Brahmane, M.P., 2015. Metagenomics: retrospect and prospects in high throughput age. Biotechnol. Res. Int.
13.
Kumar, B., Mishra, M., Verma, V.K., Rai, P., Kumar, S., 2018a. Organochlorines in urban soils from central India: probabilistic health hazard and risk
implications to human population. Environ. Geochem. Health 40 (6), 2465–2480.
Kupski, L., Salcedo, G.M., Caldas, S.S., de Souza, T.D., Furlong, E.B., Primel, E.G., 2019. Optimization of a laccase-mediator system with natural
redox-mediating compounds for pesticide removal. Environ. Sci. Pollut. Res. 26 (5), 5131–5139.
Lin, Z., Zhen, Z., Liang, Y., Li, J., Yang, J., Zhong, L., et al., 2019. Changes in atrazine speciation and the degradation pathway in red soil during the
vermiremediation process. J. Hazard. Mater. 364, 710–719.
Lin, Z., et al., 2018. Rhizospheric effects on atrazine speciation and degradation in laterite soils of Pennisetum alopecuroides (L.) Spreng. Environ. Sci.
Pollut. Res. 25 (13), 12407–12418.
Lindley, M., 1976. Pesticides and the environment. Nature 263, 464.
Liu, Y.Y., Chung, Y.C., Xiong, Y., 2001. Purification and characterization of a dimethoate-degrading enzyme of Aspergillus niger ZHY256 isolated from
sewage. Appl. Environ. Microbiol. 67, 3746–3749.
Liu, L., Helbling, D.E., Kohler, H-P.E., Smets, B.F., 2019. Modelling carbofuran biotransformation by Novosphingobium sp. KN65. 2 in the presence of
coincidental carbon and indigenous microbes. Environ. Sci. Water. Res. Technol. 5, 798–807.
Liu, X.Y., Luo, X.J., Li, C.X., Lai, Q.L., Xu, J.H., 2014. Draft genome sequence of Burkholderia sp. Strain MP-1, a Methyl Parathion (MP)-degrading
bacterium from MP-contaminated soil. Genome Announc. 2, e00344-14.
Lopes, A.R., Danko, A.S., Manaia, C.M., Nunes, O.C., 2012. Molinate biodegradation in soils: natural attenuation versus bioaugmentation. Appl. Microbiol.
Biotechnol. http://dx.doi.org/10.1007/s00253-012-4096-y.
Madhavi, V., Lele, S.S., 2009. Laccase: properties and applications. BioResources 4, 1694–1717.
Mandal, K., Singh, B., Jariyal, M., Gupta, V., 2013. Microbial degradation of fipronil by Bacillus thuringiensis. Ecotoxicol. Environ. Saf. 93, 87–92.
Manzoni, C., Kia, D.A., Vandrovcova, J., Hardy, J., Wood, N.W., Lewis, P.A., et al., 2016. Genome, transcriptome and proteome: the rise of omics data
and their integration in biomedical sciences. Brief Bioinfo. 19, 286–302.
16
Maqbool, Z., Hussain, S., Imran, M., Mahmood, F., Shahzad, T., Ahmed, Z., Azeem, F., Muzammil, S., 2016. Perspectives of using fungi as bioresource
for bioremediation of pesticides in the environment: a critical review. Environ. Sci. Pollut. Res. 23 (17), 16904–16925.
Matsumoto, E., Kawanaka, Y., Yun, S.J., Oyaizu, H., 2008. Isolation of dieldrin-and endrin- degrading bacteria using 1, 2-epoxycyclohexane as a
structural analog of both compounds. Appl. Microbiol. Biotechnol. 80 (6), 1095–1103.
McLellan, J., Gupta, S.K., Kumar, M., 2019. Feasibility of using bacterial-microalgal consortium for the bioremediation of organic pesticides: Application
constraints and future prospects. In: Application of Microalgae in Wastewater Treatment. pp. 341–362.
Mir-Tutusaus, J.A., Masís-Mora, M., Corcellas, C., Eljarrat, E., Barceló, D., Sarrà, M., Caminal, G., Vicent, T., Rodríguez-Rodríguez, C.E., 2014. Degradation
of selected agrochemicals by the white rot fungus Trametes versicolor. Sci. Total Environ. 500, 235–242.
Mohamed, A.T., El-Hussain, A.A., El-Siddig, M.A., Osman, A.G., 2011. Degradation of oxyfluorfen herbicide by soil microorganism biodegradation of
herbicides. Biotechnology 10, 274–279.
Mori, T., Wang, J., Tanaka, Y., Nagai, K., Kawagishi, H., Hirai, H., 2017. Bioremediation of the neonicotinoid insecticide clothianidin by the white-rot
fungus phanerochaete sordida. J. Hazard. Mater. 321, 586–590.
Morillo, E., Villaverde, J., 2017. Advanced technologies for the remediation of pesticide-contaminated soils. Sci. Total Environ. 586, 576–597.
Nannipieri, P., Bollag, J.M., 1991. Use of enzymes to detoxify pesticide-contaminated soils and waters. J. Environ. Qual. 20, 510–517.
Naqqash, M.N., Gökçe, A., Bakhsh, A., Salim, M., 2016. Insecticide resistance and its molecular basis in urban insect pests. Parasitol. Res. 115 (4),
1363–1373.
Nawaz, K., Hussain, K., Choudary, N., Majeed, A., Ilyas, U., Ghani, A., Lin, F., Ali, K., Afghan, S., Raza, G., Lashari, M.I., 2011. Eco-friendly role of
biodegradation against agricultural pesticides hazards. Afr. J. Microbiol. Res. 5 (3), 177–183.
Niti, C., Sunita, S., Kamlesh, K., Rakesh, K., 2013. Bioremediation: An emerging technology for remediation of pesticides. Res. J. Chem. Environ. 17
(4), 88–105.
Ohtsubo, Y., Sato, T., Kishida, K., Tabata, M., Ogura, Y., Hayashi, T., Tsuda, M., Nagata, Y., 2014. Complete genome sequence of Pseudomonas aeruginosa
MTB-1, isolated from a microbial community enriched by the technical formulation of hexachlorocyclohexane. Genome Announc. 2, e01130-13.
Ortiz-Hernandez, M.L., Sanchez-Salinas, E., Dantan-Gonzalez, E., Castrejon-Godınez, M.L., 2013. Pesticide biodegradation: mechanisms, genetics and
strategies to enhance the process. In: Biodegradation-Life of Science. Intech, http://dx.doi.org/10.5772/56098.
Palmer-Brown, W., de Melo Souza, P.L., Murphy, C.D., 2019. Cyhalothrin biodegradation in Cunninghamella elegans. Environ. Sci. Pollut. Res. 26 (2),
1414–1421.
Pan, X., Lin, D., Zheng, Y., Zhang, Q., Yin, Y., Cai, L., Fang, H., Yu, Y., 2016. Biodegradation of DDT by Stenotrophomonas sp. DDT-1: characterization
and genome functional analysis. Sci. Rep. 6, 21332.
Pant, G., Mistry, S.K., Sibi, G., 2013. Isolation, identification and characterization of p, p0-DDT degrading bacteria from soil. J. Environ. Sci. Technol.
6 (3), 130–137.
Paris, D.F., Lewis, D.L., Wolfe, N.L., 1975. Rates of degradation of malathion by bacteria isolated from aquatic systems. Environ. Sci. Technol. 9 (2),
135–138.
Park, J.W., Dec, J., Kim, J.E., Bollag, J.M., 1999. Effect of humic constituents on the transformation of chlorinated phenols and anilines in the presence
of oxidoreductive enzymes or birnessite. Environ. Sci. Technol. 33, 2028–2034.
Park, J.W., Park, B.K., Kim, J.E., 2006. Remediation of soil contaminated with 2, 4-dichlorophenol by treatment of minced shepherd’s purse roots.
Arch. Environ. Contam. Toxicol. 50, 191–195.
Pathak, A., Chauhan, A., Ewida, A.Y., Stothard, P., 2016. Whole genome sequence analysis of an Alachlor and Endosulfan degrading micrococcus sp
strain 2385 isolated from Ochlockonee River. Florida. J. Genom. 4, 42.
Peng, X., Huang, J., Liu, C., Xiang, Z., Zhou, J., Zhong, G., 2012. Biodegradation of bensulphuron-methyl by a novel Penicillium pinophilum strain BP-H-02.
J. Hazard. Mater. 213, 216–221.
Pereira, L.C., de Souza, A.O., Bernardes, M.F.F., Pazin, M., Tasso, M.J., Pereira, P.H., Dorta, D.J., 2015. A perspective on the potential risks of emerging
contaminants to human and environmental health. Environ. Sci. Pollut. Res. 22 (18), 13800–13823.
Phugare, S.S., Kalyani, D.C., Gaikwad, Y.B., Jadhav, J.P., 2013. Microbial degradation of imidacloprid and toxicological analysis of its biodegradation
metabolites in silkworm [Bombyx mori]. Chem. Eng. J. 230, 27–35.
Pizzul, L., Castillo, M.D., Stenström, J., 2009. Degradation of glyphosate and other pesticides by ligninolytic enzymes. Biodegradation 20 (6), 751.
Plangklang, P., Reungsang, A., 2011. Bioaugmentation of carbofuran residues in soil by Burkholderia cepacia PCL3: a small-scale field study. Int.
Biodeterior. Biodegrad. 65, 902–905.
Powthong, P., Jantrapanukorn, B., Suntornthiticharoen, P., 2016. Isolation, identification and analysis of DDT-degrading bacteria for agriculture area
improvements. J. Food Agric. Environ. 14 (1), 131–136.
Purg, M., Elias, M., Kamerlin, S.C.L., 2017. Similar active sites and mechanisms do not lead to cross-promiscuity in organophosphate hydrolysis:
implications for biotherapeutic engineering. J. Am. Chem. Soc. 139, 17533–17546.
Purohit, H.J., Tikariha, H., Kalia, V.C., 2018. Current scenario on application of computational tools in biological systems. In: Soft Computing for
Biological Systems. Springer Nature, Singapore, pp. 1–12.
Qu, J., Xu, Y., Ai, G.-M., Liu, Y., Liu, Z.-P., 2015. Novel Chryseobacterium sp. PYR2 degrades various organochlorine pesticides (OCPs) and achieves
enhancing removal and complete degradation of DDT in highly contaminated soil. J. Environ. Manag. 161, 350–357.
Rahman, M., Rahman, M., Sabir, A.A., Mukta, J.A., Khan, M.M.A., Mohi-Ud-Din, M., Miah, M.G., Islam, M.T., 2018. Plant probiotic bacteria Bacillus and
Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Sci. Rep. 8 (1), 1–11.
Rani, R., Kumar, V., Gupta, P., Chandra, A., 2019. Application of plant growth promoting rhizobacteria in remediation of pesticides contaminated
stressed soil. In: New and Future Developments in Microbial Biotechnology and Bioengineering: Microbes in Soil, Crop and Environmental
Sustainability. Elsevier B.V., http://dx.doi.org/10.1016/B978-0-12-818258-1.00029-7.
Rao, M.A., Scelza, R., Scotti, R., Gianfreda, L., 2010. Role of enzymes in the remediation of polluted environments. J. Soil Sci. Plant Nutr. 10, 333–353.
Riya, P., Jagatpati, T., 2012. Biodegradation and bioremediation of pesticides in soil: its objectives, classification of pesticides, factors and recent
developments. World J. Sci. Technol. 2, 36–41.
Rodríguez, A., Castrejón-Godínez, M.L., Salazar-Bustamante, E., Gama-Martínez, Y., Sánchez-Salinas, E., et al., 2020. Omics approaches to pesticide
biodegradation. Curr. Microbiol. 77 (4), 545–563.
Sabourmoghaddam, N., Zakaria, M.P., Omar, D., 2015. Evidence for the microbial degradation of imidacloprid in soils of Cameron Highlands. J. Saudi
Soci. Agri. Sci. 14 (2), 182–188.
Sagarkar, S., et al., 2013. Monitoring bioremediation of atrazine in soil microcosms using molecular tools. Environ. Pollut. 172, 108–115.
Saleh, I.A., Zouari, N., Al-Ghouti, M.A., 2020. Removal of pesticides from water and wastewater: Chemical, physical and biological treatment approaches.
Environ. Technol. Innov. 101026.
Salunkhe, V.P., Sawant, I.S., Banerjee, K., Wadkar, P.N., Sawant, S.D., 2015. Enhanced dissipation of triazole and multiclass pesticide residues on grapes
after foliar application of grapevine-associated bacillus species. J. Agric. Food Chem. 63, 10736–10746.
Sarker, A., Lee, S.H., Kwak, S.Y., Nandi, R., Kim, J.E., 2020. Comparative catalytic degradation of a metabolite 3, 5-dichloroaniline derived from
dicarboximide fungicide by laccase and MnO2 mediators. Ecotoxicol. Environ. Safety 196, 110561.
17
Sarker, A., Talukder, N.M., Islam, M.T., 2014. Phosphate solubilizing bacteria promote growth and enhance nutrient uptake by wheat. Plant Sci. Today
1 (2), 86–93.
Scott, C., Begley, C., Taylor, M.J., Pandey, G., Momiroski, V., French, N., et al., 2011. Free enzyme bioremediation of pesticides: a case study for the
enzymatic remediation of organophosphorous insecticide residues. Pesticide Mitig. Strateg. Surf. Water. Qual. 15, 5–174.
Scott, C., Pandey, G., Hartley, C.J., Jackson, C.J., Cheesman, M.J., Taylor, M.C., et al., 2008. The enzymatic basis for pesticide bioremediation. Indian J.
Microbiol. 48, 65–79.
Sethunathan, N., Megharaj, M., Chen, Z.L., Williams, B.D., Lewis, G., Naidu, R., 2004. Algal degradation of a known endocrine disrupting insecticide,
α -endosulfan, and its metabolite, endosulfan sulfate, in liquid medium and soil. J. Agric. Food Chem. 52 (10), 3030–3035.
Shen, Y.J., Lu, P., Mei, H., Yu, H.J., Hong, Q., Li, S.P., 2010. Isolation of a methyl parathion- degrading strain Stenotrophomonas sp. SMSP-1 and cloning
of the ophc2 gene. Biodegradation 21 (5), 785–792.
Silambarasan, S., Abraham, J., 2014. Efficacy of Ganoderma sp. JAS4 in bioremediation of chlorpyrifos and its hydrolyzing metabolite TCP from
agricultural soil. J. Basic Microbiol. 54 (1), 44–55.
Simonelli, A., Basilicata, P., Miraglia, N., Castiglia, L., Guadagni, R., Acampora, A., Sannolo, N., 2007. Analytical method validation for the evaluation
of cutaneous occupational exposure to different chemical classes of pesticides. J. Chromatogr. B 860 (1), 26–33.
Singh, P., Saini, H.S., Raj, M., 2016. Rhamnolipid mediated enhanced degradation of chlorpyrifos by bacterial consortium in soil–water system.
Ecotoxicol. Environ. Saf. 134, 156–162.
Singh, T., Singh, D.K., 2017. Phytoremediation of organochlorine pesticides: Concept, method, and recent developments. Int. J. Phytoremed. 19 (9),
834–843.
Somara, S., Manavathi, B., Tebbe, C.C., Siddavatam, D., 2002. Localisation of identical organophosphorus pesticide degrading (opd) genes on genetically
dissimilar indigenous plasmids of soil bacteria: PCR amplification, cloning and sequencing of opd gene from Flavobacterium balustinum. Indian
J. Exp. Biol. 40 (7), 774–779.
Sparks, T.C., Nauen, R., 2015. IRAC: Mode of action classification and insecticide resistance management. Pest. Biochem. Physiol. 121, 122–128.
Spina, F., et al., 2018. Fungi as a toolbox for sustainable bioremediation of pesticides in soil and water. Plant Biosyst.- Int. J. Deal. All Aspects Plant
Biol. 152 (3), 474–488.
Sun, Y., Kumar, M., Wang, L., Gupta, J., Tsang, D.C.W., 2020. Biotechnology for soil decontamination: opportunity, challenges, and prospects for
pesticide biodegradation. In: Bio-Based Materials and Biotechnologies for Eco-Efficient Construction. Elsevier Ltd., http://dx.doi.org/10.1016/b978-
0-12-819481-2.00013-1.
Sun, S., Sidhu, V., Rong, Y., Zheng, Y., 2018. Pesticide pollution in agricultural soils and sustainable remediation methods: a review. Curr. Pollut. Rep.
4 (3), 240–250.
Sun, S.-L., Yang, W.-L., Guo, J.-J., Zhou, Y.-N., Rui, X., Chen, C., Ge, F., Dai, Y.-J., 2017. Biodegradation of the neonicotinoid insecticide acetamiprid in
surface water by the bacterium Variovorax boronicumulans CGMCC 4969 and its enzymatic mechanism. RSC Adv. 7 (41), 25387–25397.
Sun, Y., Zhao, L., Li, X., Hao, Y., Xu, H., Weng, L., Li, Y., 2019. Stimulation of earthworms (Eisenia fetida) on soil microbial communities to promote
metolachlor degradation. Environ. Pollut. 248, 219–228.
Tan, H., Cao, Y., Tang, T., Qian, K., Chen, W.L., Li, J., 2008. Biodegradation and chiral stability of fipronil in aerobic and flooded paddy soils. Sci. Total
Environ. 407, 428–437.
Tarla, D.N., et al., 2020. Phytoremediation and bioremediation of pesticide-contaminated soil. Appl. Sci. 10 (4), 1217.
Thakur, M., Medintz, I.L., Walper, S.A., 2019. Enzymatic bioremediation of organophosphate compounds—Progress and remaining challenges. Front.
Bioeng. Biotechnol. 7, 1–21.
Varsha, Y.M., Naga, D.C.H., Chenna, S., 2011. An emphasis on xenobiotic degradation in environmental cleanup, review article. J. Bioremed. Biodegrad.
4, 1–10.
Velázquez-Fernández, J.B., Martínez-Rizo, A.B., Ramírez-Sandoval, M., Domínguez-Ojeda, D., 2012. Biodegradation and bioremediation of organic
pesticides. In: Soundararajan, R.P. (Ed.), Pesticides – Recent Trends in Pesticide Residue Assay. InTech, Rijeka.
Verger, P.J.P., Boobis, A.R., 2003. Reevaluate pesticides for food security and safety. Science 341 (6147), 717–718.
Vidal-Limon, A., García Suárez, P.C., Arellano-García, E., Contreras, O.E., Aguila, S.A., 2018. Enhanced degradation of pesticide dichlorophen by laccase
immobilized on nanoporous materials: a cytotoxic and molecular simulation investigation. Bioconjug. Chem. 29 (4), 1073–1080.
Villaverde, J., Posada-Baquero, R., Rubio-Bellido, M., Laiz, L., Saiz-Jimenez, C., Sanchez-Trujillo, M.A., Morillo, E., 2012. Enhanced mineralization of
diuron using a cyclodextrin-based bioremediation technology. J. Agril. Food Chem. 60 (40), 9941–9947.
Wang, W., Chen, X., Yan, H., Hu, J., Liu, X., 2019. Complete genome sequence of the cyprodinil-degrading bacterium Acinetobacter johnsonii LXL_C1.
Microb. Pathog. 127, 246–249.
Wang, X.X., Chi, Z., Ru, S.G., Chi, Z.M., 2012. Genetic surface-display of methyl parathion hydrolase on Yarrowia lipolytica for removal of methyl
parathion in water. Biodegradation 23, 63–774.
Wang, C., Lin, X., Li, L., Lin, S., 2016. Differential growth responses of marine phytoplankton to herbicide glyphosate. PLoS One 11 (3), e0151633.
Wu, P.C., Liu, Y.H., Wang, Z.Y., Zhang, X.Y., Li, H., Liang, W.Q., Luo, N., Hu, J.M., Lu, J.Q., Luan, T.G., 2006. Molecular cloning, purification, and biochemical
characterization of a novel pyrethroid hydrolyzing esterase from Klebsiella sp. strain ZD112. J. Agric. Food Chem. 54 (3), 836–842.
Xu, H.J., Bai, J., Li, W., Murrell, J.C., Zhang, Y., Wang, J., et al., 2021. Mechanisms of the enhanced DDT removal from soils by earthworms: Identification
of DDT degraders in drilosphere and non-drilosphere matrices. J. Hazard. Mater. 404, 124006.
Yang, H., Carr, P.D., McLoughlin, S.Y., Liu, J.W., Horne, I., Qiu, X., et al., 2003. Evolution of an organophosphate-degarding enzyme: a comparison of
natural and directed evolution. PEDS 16, 135–145.
Yang, H., Hu, S., Wang, X., Chuang, S., Jia, W., Jiang, J., 2020. Pigmentiphaga sp. strain D-2 uses a novel amidase to initiate the catabolism of the
neonicotinoid insecticide acetamiprid. Appl. Environ. Microbiol. http://dx.doi.org/10.1128/aem.02425-19.
Yang, Y.X., Pi, N., Zhang, J.B., Huang, Y., Yao, P.P., Xi, Y.J., Yuan, H.M., 2016. USPIO assisting degradation of MXC by host/guest-type immobilized
laccase in AOT reverse micelle system. Environ. Sci. Pollut. Res. 23 (13), 13342–13354.
Zaffar, H., Ahmad, R., Pervez, A., Naqvi, T.A., 2018. A newly isolated pseudomonas sp. can degrade endosulfan via hydrolytic pathway. Pest. Biochem.
Physiol. 152, 69–75.
Zeb, A., Li, S., Wu, J., Lian, J., Liu, W., Sun, Y., 2020. Insights into the mechanisms underlying the remediation potential of earthworms in contaminated
soil: A critical review of research progress and prospects. Sci. Total Environ. 140145.
Zeng, S., Qin, X., Xia, L., 2017. Degradation of the herbicide isoproturon by laccase-mediator systems. Biochem. Eng. J. 119, 92–100.
Zhang, H., Hu, C., Jia, X., Xu, Y., Wu, C., Chen, L., Wang, F., 2012. Characteristics of γ -hexachlorocyclohexane biodegradation by a nitrogen-fixing
cyanobacterium, Anabaena azotica. J. Appl. Phycol. 24 (2), 221–225.
Zhang, H., Yang, L., Ma, Y.Y., Zhu, C., Lin, S., Liao, R.Z., 2018. Theoretical studies on catalysis mechanisms of serum paraoxonase 1 and phosphotriesterase
diisopropyl fluorophosphatase suggest the alteration of substrate preference from paraoxonase to DFP. Molecules 23, E1660.
Zhang, Z., Yang, D., Si, H., Wang, J., Parales, R.E., Zhang, J., 2020. Biotransformation of the herbicide nicosulfuron residues in soil and seven sulfonylurea
herbicides by Bacillus subtilis YB1: A climate chamber study. Environ. Pollut. 263, 114492.
Zhang, D., et al., 2015. Magnetic nanoparticle-mediated isolation of functional bacteria in a complex microbial community. ISME J. 9 (3), 603–614.
18
Zhao, X., Ma, F., Feng, C., Bai, S., Yang, J., Wang, L., 2017. Complete genome sequence of Arthrobacter sp. ZXY-2 associated with effective atrazine
degradation and salt adaptation. J. Biotechnol. 248, 43–47.
Zhao, H., Zhu, J., Liu, S., Gao, H., Zhou, X., Tao, K., 2015. Bioremediation potential of glyphosate degrading pseudomonas spp. strains isolated from
contaminated soil. J. Gen. Appl. Microbiol. 61 (5), 165–170.
Zhu, S., Wang, H., Jiang, W., Yang, Z., Zhou, Y., He, J., Qiu, J., Hong, Q., 2019. Genome analysis of Carbaryl-degrading strain Pseudomonas putida XWY-1.
Curr. Microbiol. 76, 927–929.
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Environmental Technology & Innovation 23 (2021) 101777

Contents lists available at ScienceDirect

Environmental Technology & Innovation

Remediation of chemical pesticides from contaminated sites

3. Biological remediation of pesticides — A green and prospective approach

3.1. Bacterial degradation of pesticides

3.2. Fungi- and algae-mediated pesticide degradation

4. Enzymatic pesticide biodegradation

4.1. Application of laccase and peroxidase in pesticide biotransformation

5. Potentials of plant growth-promoting rhizobacteria in pesticide degradation

6. Underlying mechanism and molecular advancement of pesticide bioremediation

7. Challenges and prospective of pesticide biodegradation

CRediT authorship contribution statement

Declaration of competing interest

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