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Anish Kumar Sharma and Jyotsana Pandit,Biodegradation of Chlorpyrifos by Microbes - A Review,Discovery Biotechnology, 2016, 7(18), 1-10,www.discoveryjournals.com © 2016 Discovery Publication. All Rights Reserved

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Anish Kumar Sharma1*, Jyotsana Pandit2

1. Assistant Professor (Biotechnology), School of Biotechnology, P P Savani Knowledge City, Kosamba, Surat - 394125, India2. Research Scholar, Department of Environmental Sciences, Dr Y S Parmar University of Horticulture and Forestry, Nauni, Solan -

173 230, India

*Corresponding author: School of Biotechnology, P P Savani Knowledge City, Kosamba, Surat - 394125, India, [email protected]

Publication HistoryReceived: 2 September 2016Accepted: 20 September 2016Online First: 22 September 2016Published: October-December 2016

CitationAnish Kumar Sharma, Jyotsana Pandit. Biodegradation of Chlorpyrifos by Microbes - A Review. Discovery Biotechnology, 2016, 7(18),1-10

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This work is licensed under a Creative Commons Attribution 4.0 International License.

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ABSTRACTChlorpyrifos is a broad spectrum organ phosphorus compound, with anti-cholinesterase enzyme activity against a variety ofchewing, sucking and boring insects/pests and used worldwide. Continuous and excessive uses of chlorpyrifos for agricultural as well

Discovery Biotechnology, Vol. 7, No. 18, October-December, 2016 REVIEW

Biodegradation of Chlorpyrifos by Microbes - A Review

Discovery BiotechnologyAn International Journal

ISSN2319–7773

EISSN2319–7781


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as other purpose have resulted in environmental pollution, human and animal adverse health effects. Biodegradation of chlorpyrifosby microbes is a cost effective technique for environmental clean-up of this toxic pesticide. Microorganisms including bacteria, fungiand actinomycetes alone as well as together have been reported to efficiently degrade chlorpyrifos. The present review article dealswith the isolated chlorpyrifos degrading microorganisms and enzyme systems probably playing active role in chlorpyrifosdegradation.

Keywords: Chlorpyrifos, Biodegradation, Organophosphorous, Bioremediation

Abbreviations: OPH-Organophosphorus Hydrolase, OPD- O-Phenylenediamine Dihydrochloride, MPH- Methyl Parathion Hydrolase,Mevalonate Pyrophosphate Decarboxylase

1. INTRODUCTION

Pesticide is a chemical or biological agent that kills or incapacitates target pests including insects, plant pathogens, weeds, mollusks,

birds, nematodes which lead to destruction of agricultural crops. Pesticides have been classified on the basis of their chemicalstructure, target organism, biological mechanism etc. and are broadly classified as: organochlorines, organophosphates, carbamates,pyrethroids and triazines. Chlorpyrifos [O, O – diethyl O - (3, 5, 6 – trichloro – 2 - pyridyl phosphorothioate)] is one of the most usedorganophosphate insecticide against broad spectrum of insects and pests of economically important crops (Cho et al., 2002).Organophosphorus compounds belong to a class of highly toxic neurotoxins that are commonly used as insecticides and chemicalwarfare agents. They inhibit acetylcholine esterase (AchE) in the central nervous system synapses, leading to a subsequent loss ofnerve function and eventual death (Donarski et al., 1989). Chlorpyrifos, an organophosphorous pesticide, is sold under various tradenames such as Lorsban and Dursban. Chlorpyrifos is effective in controlling a variety of insects, including cutworms, corn rootworms,cockroaches, grubs, flea beetles, flies, termites, fire ants and lice (US EPA 1986). In India, chlorpyrifos usage is mainly for controllinginsect pests of apples, pears, rice, tobacco, cotton and Chinese cabbage as foliar treatments. Chlorpyrifos is commonly available informulations which includes emulsifiable concentrates, granulars and wettable powder (Meister, 1992).

Chlorpyrifos is considered to have a high potential for adverse effects in occupational applications (Aponso, 2002). The primarytarget organ for chlorpyrifos toxicity is the central and peripheral nervous systems, since its metabolite, chlorpyrifos-oxon is anacetylcholinesterese inhibitor, this may cause death and have adverse sub-lethal effects in humans. Low-level exposure tochlorpyrifos has caused interference with the development of the mammalian nervous system during pregnancy (Slotkin et al.,2006). Developmental effects such as low birth weight and reduced head circumference were found in human epidemiologicalstudies on pregnant women exposed to chlorpyrifos (Whyatt and Barr, 2004). Chlorpyrifos is also considered to be an endocrinedisrupting compound (Rawling et al., 1998). Exposure to chlorpyrifos has reportedly caused death by respiratory failure or cardiacarrest or disability in humans (Environmental Research Laboratory, 1984). Lesser exposures may cause headache, dizziness, unsteadymovements, anemia, bronchitis, fluids in lungs and sweating (EXTONET, 1993). Agricultural activities are considered a primary sourceof exposure to chlorpyrifos (Alexander et al., 2006 ; Curwin et al., 2007). In developing countries, small-scale farmers were found tohave a high risk of adverse health effects from chlorpyrifos when mixing, loading and spraying chlorpyrifos using back-pack sprayers(Rodriguez et al., 2006 ; Panuwet et al., 2008 ; Aponso, 2002). Farmers are at high risk of pesticide exposure due to the use of back-pack reservoirs for pesticide application, low safety knowledge, and limited use of personal protection equipment (Dung, 2006).However, the exposure assessment and evaluation of adverse health effects of chlorpyrifos with these farmers has not beenevaluated. The potential damage by chlorpyrifos to non-target organisms is high because acetyl cholinesterase is present in allvertebrates (Sogorb et al., 2004).

Chlorpyrifos is toxic to a variety of beneficial non-target arthropods including bees, ladybird beetles and parasitic wasps.Prolonged exposure to chlorpyrifos results in delayed seedling emergence, fruit deformities and abnormal cell division in plants(NCAP, 2000). Microbial degradation of organophosphates is of particular interest because of the high mammalian toxicity of suchcompounds and their widespread and extensive use (Singh et al., 2004). Biodegradation is considered to be a reliable cost-effectivetechnique for pesticide removal. There have been many reports where different bacterial species were found effective in degradationof chlorpyrifos. Few reports confirm that algae, fungi and yeast are also capable of degrading chlorpyrifos. The potential r isksassociated with the use of this pesticide have provoked the scientists to find out the ways based on biological and biotechnologies


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approaches to mitigate the ill-effects of Chlorpyrifos on environmental quality and public health (Harish et al., 2013). Keeping in viewthe human health and ecological risks associated with chlorpyrifos and its widespread use in agriculture, prompted us to investigateand review chlorpyrifos degradation by different microorganisms, so that possible cost effective bioremediation technologies for theenvironmental clean-up of this toxic pesticide may be developed.

2. MICROBIAL DEGRADATION OF PESTICIDESMicrobial degradation occurs when bacteria, fungi and other micro-organisms in soil use pesticides or other organic materials ascarbon or energy source, or consume them along with other sources co-metabolites of food or energy. Organic matter content,moisture, temperature, aeration and pH of soil all affect degradation. Microbes that are present in pesticide contaminated sites forlong duration, develops the ability to degrade/ tolerate such contaminant. Such microbes with advanced/new traits can be used forpesticide degradation (Farhan et al., 2012).

Microorganisms generally demonstrate considerable capacity for the metabolism of many pesticides. There are two major typesof microbial degradation of organic chemicals. The first, termed catabolism is a type of degradation in which the organic chemical ora portion thereof is completely degraded (e.g. mineralized) and the energy or nutrient gained contributes to cell growth. Thesecond, incidental metabolism or co-metabolism, involves the partial degradation of an organic chemical with no net benefit to theorganism, the compound being merely caught up in some metabolic pathway during the normal metabolic activities of themicroorganisms (Racke 1993). Bacterial species like Pseudomonas sp., Flavobacterium sp., Bacillus sp. etc. fungi species likeAspergillus sp., Cladosporium sp., Penicillium sp., Phanerochaete sp. etc. plays a significant role in degradation of various pesticidesdegradation.

3. DEGRADATION OF ORGANOPHOSPHATE PESTICIDESOrganophosphates contain three phosphoester bonds and, hence, are often termed phosphotriesters. Generally, hydrolysis of onlyone of the phosphoester bonds (P-O, P-S, P-F, and P-CN) can significantly reduce the toxicity of an organ phosphorus pesticide, forexample, in parathion; hydrolysis resulted in a 100-fold reduction in toxicity (Lan et al., 2006). The mechanism of degradation oforganophosphates by microorganisms may be hydrolytic, reductive and sometimes, oxidative (Lal, 1982). P=O and P=S containingorganophosphates are degraded by hydrolytic processes in the microbes. For example, phorate is metabolized in Pseudomonas sp.and Thiobacillus thiooxidans by hydrolytic pathways (Ahmed and Casida, 1958). Bacillus sp. inactivates both parathion and parathionmethyl through reduction of the nitro group to an amino (Yasuno et al., 1965). Oxidation reactions involving conversions ofparathion to paraoxon and the opening of the aromatic ring of p-nitrophenol have been reported in microorganisms (Munneckeand Hsieh 1974). Capabilities of various bacterial, fungal and algal species reported for degradation of other Organophosphoruspesticides along with mode of degradation (Table 1) till date can also be checked and utilized for chlorpyrifos degradation.

Table 1Microorganisms isolated for degradation of Organophosphorus compounds

OrganophosphorusCompound

Microorganisms Mode of degradation Reference (Year)

Parathion Flavobacterium sp. ATCC27551 Co-metabolic Sethunathan & Yoshida(1973)

Pseudomonas diminuta Co-metabolic Serdar et al. (1982)Pseudomonas stutzeri Co-metabolic Daughton &Hsieh (1977)Xanthomonas sp. Catabolic Rosenberg & Alexander

(1979)Methyl parathion Pseudomonas putida Catabolic (C) Rani & Latitha-kumari

(1994)Pseudomonas sp. WBC Catabolic (C, N) Yali et al. (2002)Flavobacterium balustinum Catabolic (C) Somara & Siddavattam

(1995)Glyphosate Pseudomonas sp. Catabolic (P) Kertesz et al. (1994a)


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Alcaligene sp. Catabolic (P) Tolbot et al. (1984)Arthrobacter atrocyaneus Catabolic (P) Pike & Amrhein (1988)Penicillium citrinum Co-metabolic Zboinska et al. (1992b)

Coumaphos Pseudomonas monteilli Co-metabolic Horne et al. (2002c)Pseudomonas diminuta Co-metabolic Serder et al. (1982)Nocardia strain-1 Catabolic (C) Mulbry (1992)

Monocrotophos Pseudomonas aeruginosa F10B Catabolic (P) Singh & Singh (2003)Pseudomonas sp. Catabolic (C) Bhadhade et al. (2002)Arthrobacter atrocyaneus Catabolic (C) Bhadhade et al. (2002)

Fenitrothion Flavobacterium sp. Catabolic (P) Sethunathan & Yoshida(1973)

Arthrobacter aurescenes TW 17 Catabolic (C) Ohshiro et al. (1996)Burkholderia sp. NF100 Catabolic (C) Hayatsu et al.(2000)

Diazinon Flavobacterium sp. Catabolic (P) Sethunathan & Yoshida(1973)

Pseudomonas sp. Co-metabolic Rosenberg & Alexander(1979)

Arthrobacter sp. Co-metabolic Barik et al. (1979)

Table 2Important chlorpyrifos degrading microorganisms

Microorganism Reference (Year)Group1: Bacteria

Micrococcus sp. Guha et al., (1997)Flavobacterium sp. Mallick et al., (1999)Enterobacter strain B-14 Singh et al., (2004)Alcaligenes faecalis DSP3 Yang et al., (2005)Stenotrophomonas YC-1 Yang et al., (2006)Klebsiella sp. Ghanem et al., (2007)Sphingomonas sp. Dsp-2 Li et al., (2007)Paracoccus sp. strain TRP Xu et al., (2008)Pseudomonas putida MAS-1 Ajaz et al., (2009)Bacillus pumillus strain C2A1 Anwar et al., (2009)Pseudomonas sp. (Ch1D) Singh et al., (2009)Bacillus licheniformis ZHU-1 Zhu et al., (2010)Ralstonia sp. strain T6 Li et al., (2010)Cupriavidus sp. DT-1 Lu et al., (2013)Lactobacillus bulgaris Shaker et al., (1988)Streptococcus thermophilus Shaker et al., (1988)Serratia sp. Gangming et al., (2007)Agrobacterium sp. Chishti and Arshad (2013)Enterobacter sp. Chishti and Arshad (2013)Pseudomonas resinovarans AST2.2 Sharma et al., (2016)

Group2: Fungi


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Phanerochaete chrysosporium Bumpus et al., (1993)Coriolus versicolor Bending et al., (2002)Hypholoma fascicularae Bending et al., (2002)Verticillium sp. DSP Hua et al., (2008)Acremonium sp. Strain GFRC-1 Kulshrestha and Kumari (2011)Cladosporium cladosporoides strainHu-01

Chen et al., (2012); Gao et al., (2012)

Ganoderma sp. JAS4 Silambarasan & Abraham (2013)Trichoderma sp. Ivashina (1986); Jayaraman et al., (2012)Trichosporon sp. Gangming et al., (2007)Aspergillus terreus JAS1 Silambarasan & Abraham ( 2013)Isaria Farinosa Karolin et al., (2015)

Group3: CyanobacteriaAnabeana sp. Park and Lee (2010)Phormidium valderianum Palanisami et al., (2009)Synechocystis sp. Singh et al., (2011)

Group4: Bacteria + Fungi in combinationCellulomonas fimi+Phanerochaete chrysosporium

Barathidasan et al., (2014)

Serratia sp. + Trichosporon sp. Gangming et al., (2007)

Table 3Organophosphorus-degrading genes and their enzymesS No. Organism Degrading

EnzymeEnzyme

StructureEncoding

Genes1. Flavobacterium sp. ATCC

27551OPH

(Organophosphorushydrolase)

Dimer opd (organophosphorusdegrading enzyme)

2. Pseudomonas diminuta OPH(Organophosphorus

hydrolase)

Dimer opd (Organophosphorusdegrading enzyme)

3. Agrobacterium radiobacter OPDA Dimer opdA (organophosphorus4. Alteromonas haloplanktis OPAA

(Organophosphorusacid anhydrolase)

Monomer opa (Organophosphorusanhydrolase)

5. Pseudomonas sp. WBC-3 MPH(Methyl parathionhydrolase)

Dimer mpd(methyl parathionhydrolase)


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4. MICROBIAL DEGRADATION OF CHLORPYRIFOSThe microbial bioremediation of chlorpyrifos is a viable option for cleaning up the contaminated sites with its eco-friendliness, highefficiency and cost-effectiveness. Several researchers reported potential many bacterial sp, fungal sp. as well as few cyanobacteriafor chlorpyrifos degradation (Table 2).

5. GENES AND ENZYMES ROLE IN CHLORPYRIFOS BIODEGRADATION:Microbes are capable of utilizing chemical compounds as carbon or phosphorus sources and enzymatic activities in them play vitalrole in degradation of that particular chemical into useable form. Organophosphate degrading enzymes are found to be reportedvarious living organisms ranging from bacteria to human beings like Parathion hydrolases (OPH) in Flavobacterium species,Organophosphorous acid anhydrolase (OAA) in Alteromonas species, Phosphotriesterase homology protein in Escherichia coli,Diisopropyl fluorophosphatase (DFPases) in Squid, Serum Paraoxanases/arylesterases in Mammals and Prolidases in Mammals andother organisms (Salman et al., 2010).

The most widely characterized enzymes are phosphotriesterase (PTEs) or organophosphate hydrolase (OPH) andOrganophosphate degrading (OPDA). The OPDA or OPH enzyme is capable of hydrolyzing a wide range of Organophosphatecompounds (Shimazu et al., 2001). The OPDA enzyme is encoded by the opd gene. The bacterial opd genes have a similar sequencein different bacterial strains (Horne et al., 2002). Sethunathan and Yoshida (1973) reported isolation of the first bacterium to degradeOP compounds from a soil sample from Philippines and was identified as Flavobacterium sp. ATCC 27551. Organophosphorushydrolase (OPH) is a bacterial enzyme capable of degrading a wide range of neurotoxic organophosphorus pesticides. OPHs aremembers of the amidohydrolase superfamily and share the same (α–β) 8 barrel structural folds and an active site with two transitionmetal ions, such as zinc, iron, manganese or cobalt. Bacterial enzymatic detoxification of OPs has attracted considerable interest,because it is economical and effective. Organophosphorus hydrolase (OPH; EC 3.1.8.1) is one of the important hydrolytic enzymeinvolved in detoxification technology that hydrolyze various organophosphate pesticides containing P–O, P–F and P–S bonds (Latifiet al., 2012). Organophosphorus hydrolase (OPH), which is capable of hydrolyzing a wide range of oxon and thion OPs, has beenextensively studied (Dumas et al., 1989; Mulbry and Karns, 1988). OPH has broad substrate specificity and can hydrolyse P–O, P–fand P–S bonds.

The OPH enzymes, including O-Phenylenediamine Dihydrochloride (OPD), Methyl Parathion Hydrolase (MPH) MevalonatePyrophosphate Decarboxylase (MPD) etc., was identified for the hydrolysis for specific classes of organophosphorus compounds(Zheng et al., 2013). The OPH was first isolated from Pseudomonas diminuta MG has the ability to hydrolyse a wide range of OPcompounds (Serdar and Gibson 1985). Cui et al. in 2001 isolated Methyl Parathion Hydrolase (MPH, E.C.3.1.8.1) from Plesiomonas sp.strain M6 and this enzyme was different from organphosphorus hydrolase enzyme as it was capable of hydrolyzing a broadspectrum of OP compounds. High OPH activities have been reported in Pseudomonas pseudoalcaligenes (Ningfeng et al., 2004) andin Pseudomonas resinovorans strain AST2.2 (Sharma et al., 2016). Gao et al., (2012) purified and characterized a novel chlorpyrifoshydrolase from the fungi Cladosporium cladosporioides Hu-01. Few Organophosphorus-degrading genes and their enzymescharacterized are shown in Table 3 (Singh, 2009).

Factors like varying incubation time period, pH, temperature, carbon sources, metal ions and various chemical compoundseffects OPH activities in microbes. Many researchers had reported maximum OPH activity at 35°C and 37°C in Pseudomonas stutzeriS7B4 and Pseudomonas aeruginosa NL01 (Bayoumi et al., 2009 ; Najavand et al., 2012). Many researchers reported alkaline pH to bethe optimum for maximum OPH activity (Najavand et al., 2012 ; DeFrank and Cheng, 1991 ; Chu et al., 2006). Ningfeng et al., (2004)observed highest OPHC2 activity in Pseudomonas pseudoalcaligenes at pH 9.0. Chu et al. (2006) reported that OPHC2 activity wasenhanced by 14.2 % in presence of Co2+ in Pichia pastoris and Najavand et al. (2012) who found OPH enzyme activity enhancementby 1.28 fold in the presence of CoCl2. SDS inhibited strongly the activity of the OPHC2 in Pseudomonas pseudoalcaligenes and Pichiapastoris (Ningfeng et al., 2004; Chu et al., 2006). The OPH enzyme activity was inhibited competitively by dithiothreitol (DTT) inPseudomonas diminuta (Dumas et al., 1989). Most of the genes as well enzymes responsible for chlorpyrifos biodegradation areisolated as well as characterized from bacterial species while there are few report available in literature in case of fungal species.

6. CONCLUSIONHence, it is concluded that different microorganism’s biodegrade chlorpyrifos and these further can be efficiently employed forcleaning up and bioremediation of contaminated sites. Various genes and enzymes actively are responsible for degradingchlorpyrifos as well as other organophosphorus compounds; these can be isolated and characterized further for better


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understanding of the degradation mechanisms. Further, new microbial strains with new traits and better degradation of chlorpyrifosas well as for degradation of other organophosphorus pesticides can be developed.

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