Perspectives of lindane (γ-hexachlorocyclohexane) biodegradation from the environment: a review

Abstract

This review describes the biodegradation of Lindane (γ-hexachlorocyclohexane, γ-HCH) from the diverse sources. Environmental degradation of γ-HCH has been described in terms of integrated biological approaches such as metagenomics, cloning, phytoremediation, nanobiodegradation, and biosrfactants, genes and enzymes responsible for γ-HCH degradation and exploration of new strains of γ-HCH-degrading microbes from different environmental sources. Metagenomics-based approaches help in the identification and isolation of new genes from the uncultivable sources and provide insights for future research. There is potential in the elucidation of pathways of degradation of persistent organic pollutants (POPs) from environment by the microorganisms. This is possible by means of new/improved microbial species. The behavior of isolated strains and the microorganisms when present in community is altogether different. Therefore, there is a need to develop new technology which will identify the minor component of the microbial community involved in degradation because the minor part might have profound effect on degradation. This is mediated by the biological activity of the microbial system.

Keywords

Microbial degradation / Metagenomics / Phytoremediation / Microbial community / Lindane (γ-hexachlorocyclohexane, γ-HCH)

References

[1] Abhilash PC, Srivastava S, Singh N. Comparative bioremediation potential of four rhizospheric microbial species against lindane. Chemosphere, 2011, 82(1): 56-63.

[2] Alexander M. Biodegradation and bioremediation, 1994, San Diego: Academic Press.

[3] Alexander M. Biodegradation and bioremediation. 2nd ed. San Diego, American Chemical Society. Biosciences, 1999, 36: 86-91.

[4] Alvarez A, Yanez ML, Benimeli CS, Amoroso MJ. Maize plants (Zea mays) root exudates enhance lindane removal by native Streptomyces strains. Int Biodeterior Biodegrad, 2012, 66: 14-18.

[5] Anacleto P, van den Heuvel FHM, Oliveira C, Rasmussen RR, Fernandes JO, Sloth JJ, Barbosa V, Alves RN, Marques A, Cunha SC. Exploration of the phycoremediation potential of Laminaria digitata towards diflubenzuron, lindane, copper and cadmium in a multitrophic pilot-scale experiment. Food Chem Toxicol, 2017, 104: 95-108.

[6] Anupama KS, Paul S. Ex situ and in situ biodegradation of lindane by Azotobacter chroococcum. J Environ Sci Health, Part B, 2010, 45: 58-66.

[7] Aresta A, Nonnis Marzano C, Lopane C, Corriero G, Longo C, Zambonin C, Stabili L. Analytical investigations on the lindane bioremediation capability of the demosponge Hymeniacidon perlevis. Mar Pollut Bull, 2015, 90(1–2): 143-149.

[8] Asemoloye MD, Ahmad R, Jonathan SG. Synergistic rhizosphere degradation of γ-hexachlorocyclohexane (lindane) through the combinatorial plant-fungal action. PLoS ONE, 2017, 12(8): e0183373.

[9] Assaf-Anid N, Kun-Yu L. Carbon tetrachloride reduction by Fe2C, S2 K, and FeS with vitamin B-12 as organic amendment. J Environ Eng, 2002, 128: 94-99.

[10] Awasthi N, Ahuja R, Kumar A. Factors influencing the degradation of soil applied endosulfan isomers. Soil Biol Biochem, 2000, 32: 1697-1705.

[11] Bajaj S, Sagar S, Khare S, Singh DK. Biodegradation of γ-hexachlorocyclohexane (lindane) by halophilic bacterium Chromohalobacter sp. LD2 isolated from HCH dumpsite. Int Biodeterior Biodegrad, 2017, 122: 23-28.

[12] Barnhoorn IEJ, van Dyk JC, Genthe B, Harding WR, Wagenaar GM, Bornman MS. Organochlorine pesticide levels in Clarias gariepinus from polluted fresh water impoundments in South Africa and associated human health risks. Chemosphere, 2015, 120: 391-397.

[13] Bashir S, Hitzfeld KL, Gehre M, Richnow HH, Fischer A. Evaluating degradation of hexachlorcyclohexane (HCH) isomers within a contaminated aquifer using compound-specific stable carbon isotope analysis (CSIA). Water Res, 2015, 71: 187-196.

[14] Becerra-Castro C, Kidd PS, Rodríguez-Garrido B, Monterroso C, Santos-Ucha P, Prieto-Fernández A. Phytoremediation of hexachlorocyclohexane(HCH) contaminated soils using Cytisusstriatus and bacterial inoculants in soils with distinctorganic matter content. Env Pollut, 2013, 178: 202-210.

[15] Benezet HJ, Matsumura F. Isomerization of γ-BHC to α-BHC in the environment. Nature, 1973, 243: 480-481.

[16] Benimeli CS, Castro GR, Chaile AP, Amoroso MJ. Lindane removal induction by Streptomyces sp. M7. J Basic Microbiol, 2006, 46: 348-357.

[17] Benimeli CS, González AJ, Chaile AP, Amoroso MJ. Temperature and pH effect on lindane removal by Streptomyces sp. M7 in soil extract. J Basic Microbiol, 2007, 47: 468-473.

[18] Benimeli CS, Fuentes MS, Abate CM, Amoroso MJ. Bioremediation oflindane-contaminated soil by Streptomyces sp. M7 and its effects on Zea mays growth. Int Biodeterior Biodegrad, 2008, 61: 233-239.

[19] Berger M, Löffler D, Ternes T, Heininger P, Ricking M, Schwarzbauer J. Hexachlorocyclohexane derivatives in industrial waste and samples from a contaminated riverine system. Chemosphere, 2016, 150: 219-226.

[20] Beyer A, Matthies M. Long-range transport potential of semivolatile organic chemicals in coupled air–water systems. Environ Sci Pollut Res, 2001, 8(3): 173-179.

[21] Bezama A, Navia R, Mendoza G, Barra R. Remediation technologies for organochlorine- contaminated sites in developing countries. Rev Environ Contam Toxicol, 2008, 193: 1-29.

[22] Blondel C, Khelalfa F, Reynaud S, Fauvelle F, Raveton M. Effect of organochlorine pesticides exposure on the maize root metabolome assessed using high-resolution magic-angle spinning (1)H NMR spectroscopy. Environ Pollut, 2016, 214: 539-548.

[23] Böltner D, Moreno-Morillas S, Ramos JL. 16S rDNA phylogeny and distribution of lin genes in novel hexachlorocyclohexane-degrading Sphingomonas strains. Environ Microbiol, 2005, 7(9): 1329-1338.

[24] Boyle AW, Haggblom MM, Young LY. Dehalogenation of lindane (γ-hexachlorocyclohexane) by anaerobic bacteria from marine sediments and by sulfate-reducing bacteria. FEMS Microbiol Ecol, 1999, 29: 379-387.

[25] Brown HM, Kearney PC. Plant biochemistry, environmental properties and global impact of the sulfonylurea herbicides, 1991, Washington DC: ACS Publication, 32-49.

[26] Caicedo P, Schroder A, Ulrich N, Schroter U, Schuurmann G, Paschke A. Determination of lindane leachability in soil–biosolid systems and its bioavailability in wheat plants. Chemosphere, 2011, 84: 397-402.

[27] Camacho-Pérez B (2010a) Biorrestauración de suelos agrícolas contaminados conagroquímicos utilizando reactores de suelos activados convencionales y electrobioquímico de nuevo tipo. Bioremediation of agricultural soils polluted with lindane using slurry bioreactors and a novel bioelectrochemical reactor. Sc D Thesis, Interim Report. CINVESTAV del IPN, México D.F., México

[28] Camacho-Pérez B, Ríos-Leal E, Barrera-Cortés J, Esparza-García F, Rinderknecht- Seijas N, Poggi-Varaldo HM. Treatment of soils contaminated with γ-hexachlorocyclohexane in sequential methanogenic-aerobic slurry bioreactors. J Biotechnol, 2010, 150: 559-561.

[29] Camacho-Pérez B, Ríos-Leal E, Rinderknecht-Seijas N, Poggi-Varaldo HM. Enzymes involved in the biodegradation of hexachlorocyclohexane: A mini review. J Environ Manage, 2011, 95(Suppl): S306-S318.

[30] Carrillo-Pérez E, Ruiz-Manríquez A, Yeomans-Reina H. Isolation, identification and evaluation of a mixed culture of microorganisms capable of degrading DDT (in Spanish). Revista Internacional de Contaminación Ambiental, 2004, 20: 69-75.

[31] Ceci A, Pierro L, Riccardi C, Pinzari F, Maggi O, Persiani AM, Gadd GM, Petrangeli Papini M. Biotransformation of β-hexachlorocyclohexane by the saprotrophic soil fungus Penicillium griseofulvum. Chemosphere, 2015, 137: 101-107.

[32] Ceremonie H, Boubakri H, Mavingui P, Simonet P, Vogel TM. Plasmid-encoded gamma-hexachlorocyclohexane degradation genes and insertion sequences in Sphingobium francense (ex-Sphingomonas paucimobilis Sp +). FEMS Microbiol Lett, 2006, 257: 243-252.

[33] Chaves R, López D, Macías F, Casares J, Monterroso C. Application of system dynamics technique to simulate the fate of persistent organic pollutants in soils. Chemosphere, 2013, 90(9): 2428-2434.

[34] Chouychai W, Kruatrachue M, Lee H. Effect of plant growth regulators on phytoremediation of hexachlorocyclohexane contaminated soil. Int J Phytoremediation, 2015, 17(11): 1053-1059.

[35] Concha-Graña E, Turnes-Carou MI, Muniategui-Lorenzo S, López-Mahia P, Prada-Rodriguez D, Fernández-Fernández E. Evaluation of HCH isomers and metabolites in soils, leachates, river water and sediments of a highly contaminated area. Chemosphere, 2006, 6: 588-595.

[36] Crowley DE, Alvey S, Gilbert ES. Kruger EL, Anderson TA, Coats JR. Rhizosphere ecology of xenobiotic-degrading microorganisms. Phytoremediation of soil and water contaminants, 1997, Washington, DC: American Chemical Society, 20-36.

[37] Dadhwal M, Jit S, Kumari H, Lal R. Sphingobium chinhatense sp. nov., a hexachlorocyclohexane (HCH)-degrading bacterium isolated from an HCH dumpsite. Int J Syst Evol Microbiol, 2009, 59(12): 3140-3144.

[38] Datta J, Maiti AK, Modak DP, Chakrabartty PK, Bhattacharyya P, Ray KR. Metabolism of γ-hexachlorocyclohexane by Arthrobacter citreus strain BI-100: identification of metabolites. J Gen Appl Microbiol, 2000, 46: 59-67.

[39] Dogra C, Raina V, Pal R, Suar M, Lal S, Gartemann KH, van der Meer JR, Lal R. Organization of lin genes and IS6100 among different strains of hexachlorocyclohexane degrading Sphingomonas paucimobilis: evidence for horizontal gene transfer. J Bacteriol, 2004, 186: 2225-2235.

[40] De Paolis MR, Lippi D, Guerriero E, Polcaro CM, Donati E. Biodegradation of a-, b-, and c-Hexachlorocyclohexane by Arthrobacter fluorescens and Arthrobacter giacomelloi. Appl Biochemis Biotechnol, 2013, 170: 514-524.

[41] Dubey RK, Tripathi V, Singh N, Abhilash PC. Phytoextraction and dissipation of lindane by Spinacia oleracea L. Ecotoxicol Environ Saf, 2014, 109: 22-26.

[42] Elcey CD, Kunhi AAM. Substantially enhanced degradation of hexachlorocyclohexane isomers by a microbial consortium on acclimation. J Agric Food Chem, 2010, 58: 1046-1054.

[43] Elliott DW, Zhang WF. Field assessment of nanoscale bimetallic particles for groundwater treatment. Environ Sci Technol, 2001, 35: 4922-4926.

[44] Fan X, Liu X, Huang R, Liu Y. Identification and characterization of a novel thermostable pyrethroid-hydrolyzing enzyme isolated through metagenomic approach. Microb Cell Fact, 2011, 13: 11-33.

[45] Fang H, Cai L, Yang Y, Ju F, Li X, Yu Y, Zhang T. Metagenomic analysis reveals potential biodegradation pathways of persistent pesticides in freshwater and marine sediments. Sci Total Environ, 2014, 1(470–471): 983-992.

[46] Francis AJ, Spanggord RJ, Ouchi GI. Degradation of lindane by Escherichia coli. Appl Microbiol, 1975, 29: 567-568.

[47] Fuentes MS, Benimeli CS, Cuozzo SA, Amoroso MJ. Isolation of pesticide-degrading actinomycetes from a contaminated site: bacterial growth, removal and dechlorination of organochlorine pesticides. Int  Biodeterior Biodegrad, 2010, 64: 434-441.

[48] Fuentes MS, Saez JM, Benimeli CS, Motoso MJ. Lindane biodegradation by defined consortia of indigenous Streptomyces strains. Water Air Soil Poll, 2011, 222: 217-231.

[49] García-Rivero M, Peralta-Pérez MR. Co-metabolism in the biodegradation of hydrocarbons. Revista Mexicana de Ingeniería Biomédica, 2008, 7: 1-12.

[50] Garg N, Lata P, Jit S, Sangwan N, Singh AK, Dwivedi V, Niharika N, Kaur J, Saxena A, Dua A, Nayyar N, Kohli P, Geueke B, Kunz P, Rentsch D, Holliger C, Kohler HP, Lal R. Laboratory and field scale bioremediation of hexachlorocyclohexane (HCH) contaminated soils by means of bioaugmentation and biostimulation. Biodegradation, 2016, 7(2–3): 179-193.

[51] Gianfreda L, Rao M. Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzyme Microb Technol, 2004, 35: 339-354.

[52] Girish K, Afsar M, Radha S, Manonmani HK, Kunhi AAM (2000) Effect of induction and acclimation of a microbial consortium on its ability to degrade isomeric hexachlorocyclohexane (HCH). In: Modern trends and perspectives in food packaging for 21st century, Souvenir, 14th Indian convection of food scientists and technologists (ICFOST 2000). Central Food Technological Research Institute (CFTRI), Mysore

[53] Golfinopoulos SK, Nikolaou AD, Kostopoulou MN, Xilourgidis NK, Vagi MC, . Organochlorine pesticides in the surface waters of Northern Greece. Chemosphere, 2003, 50: 507-516.

[54] Gong T, Liu R, Zuo Z, Che Y, Yu H, Song C, Yang C. Metabolic Engineering of Pseudomonas putida KT2440 for Complete Mineralization of Methyl Parathion and γ-Hexachlorocyclohexane. ACS Synth Biol, 2016, 5(5): 434-442.

[55] Guillén-Jiménez FM, Cristiani-Urbina E, Cancino-Díaz JC, Flores-Moreno JL, Barragán-Huerta BE. Lindane biodegradation by the Fusarium verticillioides AT-100 strain, isolated from Agave tequilana leaves: kinetic study and identification of metabolites. Int  Biodeterior Biodegrad, 2012, 74: 36-47.

[56] Gupta A, Kaushik CP, Kaushik A. Degradation of hexacholorocyclohexane (HCH; α, β, γ and δ) by Bacillus circulans and Bacillus brevis isolated from soil contaminated with HCH. Soil Biol Biochem, 2000, 32: 1803-1805.

[57] Gupta A, Kaushik CP, Kaushik A. Degradation of hexachlorocyclohexane isomers by two strains of Alcaligenes faecalis isolated from a contaminated site. Bull Environ Contam Toxicol, 2001, 66: 794-800.

[58] Haby PA, Crowley DE. Biodegradation of 3-chlorobenzoate as affected by rhizodeposition and selected carbon substrates. J Environ Qual, 1996, 25: 304-310.

[59] Herrero-Mercado M, Waliszewski SM, Valencia-Quintana R, Caba M, Hernández-Chalate F, García-Aguilar E, . Organochlorine pesticide levels in adipose tissue of pregnant women in Veracruz, Mexico. Bulletin Environ Cont Toxicol, 2010, 84: 652-656.

[60] Hoagland RE, Zablotowicz RM. Hall JC, Hoagland RE, Zablotowicz RM. The role of plant and microbial hydrolytic enzymes in pesticide metabolism. Pesticide biotransformation in plants and microorganisms: similarities and divergences, 2001, Washington, DC: American Chemical Society, 58-88.

[61] Homolková M, Hrabák P, Kolář M, Černík M. Degradability of hexachlorocyclohexanes in water using ferrate (VI). Water Sci Technol, 2015, 71(3): 405-411.

[62] Huntjens JLM, Brouwer W, Grobben K, Jansma O, Scheffer F, Zehnder AJB. Wolf K, van der Brink WJ, Colon FJ. Biodegradation of alpha-hexachlorocyclohexane by a bacterium isolated from polluted soil. Contaminated Soil 88, 1988, Dordrecht: Kluwer Academic Publishers, 733-737.

[63] Imai R, Nagata Y, Senoo K, Wada H, Fukuda M, Takagi M, Yano K. Dehydrochlorination of g-hexachlorocyclohexane (g-BHC) by γ-BHC-assimilating Pseudomonas paucimobilis. Agric Biol Chem, 1989, 53: 2015-2017.

[64] Ito M, Prokop Z, Klvana M, Otsubo Y, Tsuda M, Damborsky J, Nagata Y. Degradation of beta-hexachlorocyclohexane by haloalkane dehalogenase LinB from gamma-hexachlorocyclohexane-utilizing bacterium Sphingobium sp. MI1205. Arch Microbiol, 2007, 188: 313-325.

[65] Ivdra N, Fischer A, Herrero-Martin S, Giunta T, Bonifacie M, Richnow HH. Carbon, hydrogen and chlorine stable isotope fingerprinting for forensic investigations of hexachlorocyclohexanes. Environ Sci Technol, 2017, 51(1): 446-454.

[66] Jagnow G, Haider K, Ellwardt PC. Anaerobic dechlorination and degradation of hexachlorocyclohexane isomers by anaerobic and facultative anaerobic bacteria. Arch Microbiol, 1977, 115: 285-292.

[67] Janssen DB, Oppentocht JE, Poelarends GJ. Microbial dehalogenation. Curr Opin Biotechol, 2001, 12: 254-258.

[68] Jit S, Dadhwal M, Kumari H, Jindal S, Kaur J, . Evaluation of hexachlorocyclohexane contamination from the last lindane production plant operating in India. Environ Sci Pollut Res Int, 2011, 18(4): 586-597.

[69] Jürgens HJ, Roth R. Case study and proposed decontamination steps of the soil and groundwater beneath a closed herbicide plant in Germany. Chemosphere, 1989, 18: 1163-1169.

[70] Kaur J, Moskalikova H, Niharika N, Sedlackova M, Hampl A, Damborsky J, . Sphingobium baderi sp. nov, isolated from a hexachlorocyclohexane dump site. Int J Syst Evolut Microbiol, 2013, 63: 673-678.

[71] Kaur H, Kapoor S, Kaur G. Application of ligninolytic potentials of a white-rot fungus Ganoderma lucidum for degradation of lindane. Environ Monit Assess, 2016, 188(10): 588.

[72] Khan F, Husain T, Hejazi R. An overview and analysis of site remediation technologies. J Environ Manage, 2004, 71: 95-122.

[73] Kiran GS, Selvin J, Manilal A, Sujith S. Biosurfactants as green stabilizers for the biological synthesis of nanoparticles. Crit Rev Biotechnol, 2011, 31(4): 354-364.

[74] Kumar M, Chaudhary P, Dwivedi M, Kumar R, Paul D, Jain RK, Garg SK, Kumar A. Enhanced biodegradation of β- and δ-hexachlorocyclohexane in the presence of α- and γ-isomers in contaminated soils. Environ Sci Technol, 2005, 39: 4005-4011.

[75] Kumar M, Gupta SK, Garg SK, Kumar A. Biodegradation of hexachlorocyclohexane isomers in contaminated soils. Soil Biol Biochem, 2006, 38: 2318-2327.

[76] Kumar D, Kumar A, Sharma J. Degradation study of lindane by novel strains Kocuria sp. DAB-1Y and Staphylococcus sp. DAB-1W. Bioresour Bioprocess, 2016, 3: 53-60.

[77] Kumar D, Jaswal S, Chopra S. Co-degradation study of Lindane and Chlorpyrifos by novel bacterial isolates. Int J Environ Waste Manage, 2017, 20(4): 283-299.

[78] Kumari R, Subudhi S, Suar M, Dhingra G, Raina V, Dogra C, Lal S, Van der Meer JR, Holliger C, Lal R. Cloning and characterization of lin genes responsible for the degradation of hexachlorocyclohexane isomers by Sphingomonas paucimobilis strain B90. Appl Environ Microbiol, 2002, 68: 6021-6028.

[79] Kuritz T, Wolk CP. Use of filamentous cyanobacteria for biodegradation of organic pollutants. Appl Environ Microbiol, 1995, 61: 234-238.

[80] Lal R, Pandey G, Sharma P, Kumari K, Malhotra S, Pandey R, Raina V, Kohler HP-E, Holliger C, Jackson C, Oakeshott JG. The biochemistry of microbial degradation of hexachlorocyclohexane (HCH) and prospects for bioremediation. Microbiol Mol Biol Rev, 2010, 74: 58-80.

[81] Lal D, Jindal S, Kumari H, Jit S, Nigam A, Sharma P, Kumari K, Lal R. Bacterial diversity and real-time PCR based assessment of linA and linB gene distribution at hexachlorocyclohexane contaminated sites. J Basic Microbiol, 2015, 55(3): 363-373.

[82] Lamoureux GL, Rusness DG. Pentachloronitrobenzene metabolism in peanut. 1. Mass spectral characterization of seven glutathione- related conjugates produced in vivo or in vitro. Agric Food Chem, 1980, 28: 1057-1070.

[83] Laquitaine L, Durimel A, de Alencastro LF, Jean-Marius C, Gros O, Gaspard S. Biodegradability of HCH in agricultural soils from Guadeloupe (French West Indies): identification of the lin genes involved in the HCH degradation pathway. Environ Sci Pollut Res Int, 2016, 23(1): 120-127.

[84] Li YF, Scholtz MT, Van Heyst BJ. Global gridded emission inventories of beta-hexachlorocyclohexane. Environ Sci Technol, 2003, 37: 3493-3498.

[85] Lima TM, Procópio LC, Brandão FD, Carvalho AM, Tótola MR, Borges AC. Biodegradability of bacterial surfactants. Biodegradation, 2011, 22: 585-592.

[86] Lodha B, Bhat P, Kumar MS, Vaidya AN, Mudliar S, Killedar DJ, Chakrabarti T. Bioisomerization kinetics of γ-HCH and biokinetics of Pseudomonas aeruginosa degrading technical HCH. Biochem Eng J, 2007, 35: 12-19.

[87] Loredana S, Graziano P, Antonio M, Carlotta NM, Caterina L, Maria AA, Carlo Z, Giuseppe C, Pietro A. Lindane bioremediation capability of bacteria associated with the demosponge Hymeniacidon perlevis. Mar Drugs, 2017, 15(4): E108.

[88] Loredana S, Graziano P, Antonio M, Carlotta NM, Caterina L, Maria AA, Carlo Z, Corriero Giuseppe C, Pietro A. Lindane bioremediation capability of bacteria associated with the demosponge Hymeniacidon perlevis. Mar Drugs, 2017, 15(108): 1-15.

[89] Lu Y, Yu Y, Zhou R, Sun W, Dai C, Wan P, Zhang L, Hao D, Ren H. Cloning and characterisation of a novel 2,4-dichlorophenol hydroxylase from a metagenomic library derived from polychlorinated biphenyl-contaminated soil. Biotechnol Lett, 2011, 33(6): 1159-1167.

[90] MacRae IC, Raghu K, Bautista EM. Anaerobic degradation of the insecticide lindane by Clostridium sp. Nature, 1969, 221: 859-860.

[91] Manickam N, Mau M, Schlo¨mann M. Characterization of the novel HCH-degrading strain, Microbacterium sp. ITRC1. Appl Microbiol Biotechnol, 2006, 69: 580-588.

[92] Manickam N, Reddy MK, Saini HS, Shanker R. Isolation of hexachlorocyclohexane-degrading Sphingomonas sp. by dehalogenase assay and characterization of genes involved in c-HCH degradation. J Appl Microbiol, 2008, 104: 952-960.

[93] Manickam N, Pathak A, Saini HS, Mayilraj S, Shanker R. Metabolic profiles and phylogenetic diversity of microbial communities from chlorinated pesticides contaminated sites of different geographical habitats of India. J Appl Microbiol, 2010, 109(4): 1458-1468.

[94] Maqbool Z, Hussain S, Imran M, Mahmood F, Shahzad T, Ahmed Z, Azeem F, Muzammil S. Perspectives of using fungi as bioresource for bioremediation of pesticides in the environment: a critical review. Environ Sci Pollut Res Int, 2016, 23(17): 16904-16925.

[95] Math RK, Asraful Islam SM, Cho KM, Hong SJ, Kim JM, Yun MG, Cho JJ, Heo JY, Lee YH, Kim H, Yun HD. Isolation of a novel gene encoding a 3,5,6-trichloro-2-pyridinol degrading enzyme from a cow rumen metagenomic library. Biodegradation, 2010, 21(4): 565-573.

[96] Mertens B (2006) Microbial Monitoring and Degradation of Lindane in Soil. Ph.D. thesis, Ghent University, Belgium, ISBN 90-5989-126-0. Pp. 187

[97] Milun V, Lušić J, Despalatović M. Polychlorinated biphenyls, organochlorine pesticides and trace metals in cultured and harvested bivalves from the eastern Adriatic coast (Croatia). Chemosphere, 2016, 153: 18-27.

[98] Miyauchi K, Suh SK, Nagata Y, Takagi M. Cloning and sequencing of a 2,5-dichlorohydroquinone reductive dehalogenase gene whose product is involved in degradation of hexachlorocyclohexane by Sphingomonas paucimobilis. J Bacteriol, 1998, 180: 1354-1359.

[99] Mohapatra S, Pandey M. Biodegradation of hexachlorocyclohexane (HCH) isomers by white rot fungus, Pleurotus florida. J Bioremed Biodeg, 2015, 6: 280-286.

[100] Mohn WW, Garmendia J, Galvao TC, de Lorenzo V. Surveying biotransformations with a la carte genetic traps: translating dehydrochlorination of lindane (γ-hexachlorocyclohexane) into lacZ-based phenotypes. Environ Microbiol, 2006, 8: 546-555.

[101] Moldes AB, Paradelo R, Rubinos D, Devesa-Rey R, Cruz JM, Barral MT. Ex-situ treatment of hydrocarbon-contaminated soil using biosurfactants from Lactobacillus pentosus. J Agric Food Chem, 2011, 59: 9443-9447.

[102] Mougin C, Pericaud C, Malosse C, Laugero C, Asther M. Biotransformation of the insecticide lindane by the white rot basidiomycete Phanerochaete chrysosporium. Pestic Sci, 1996, 47: 51-59.

[103] Mougin C, Pericaud C, Dubroca J, Asther M. Enhanced mineralization of lindane in soils supplemented with the white rot basidiomycete Phanerochaete chrysosporium. Soil Biol Biochem, 1997, 29: 1321-1324.

[104] Mrema EJ, Rubino FM, Brambilla G, Moretto A, Tsatsakis AM, Colosio C. Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicology, 2013, 10(307): 74-88.

[105] Mugin CP, Corio-Costet MF, Werck-Reichhart D. Plant and fungal cytochrome P-450 s: their role in pesticide transformation, 2001, Washington DC: ACS Publication, 166-182.

[106] Muñiz S, Gonzalvo P, Valdehita A, Molina-Molina JM, Navas JM, Olea N, Fernández-Cascán J, Navarro E. Ecotoxicological assessment of soils polluted with chemical waste from lindane production: use of bacterial communities and earthworms as bioremediation tools. Ecotoxicol Environ Saf, 2017, 145: 539-548.

[107] Murthy HMR, Manonmani HK. Aerobic degradation of technical hexachlorocyclohexane by a defined microbial consortium. J Hazard Mat, 2007, 149(1): 18-25.

[108] Nagata Y, Miyauchi K, Takagi M. Complete analysis of genes and enzymes for γ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. J Ind Microbiol Biotechnol, 1999, 23: 380-390.

[109] Nagata Y, Prokop Z, Sato Y, Jerabek P, Kumar A, Ohtubo Y, Tsuda M, Damborsky J. Degradation of beta-hexachlorocyclohexane by haoloalkane dehydrogenase Lin B from Sphingomonas paucimobilis UT26. App Env Microbiol, 2005, 71: 2183-2185.

[110] Nagata Y, Endo R, Ito M, Ohtsubo Y, Tsuda M. Aerobic degradation of lindane (γ-hexachlorocyclohexane) in bacteria and its biochemical and molecular basis. Appl Microbiol Biotechnol, 2007, 76: 741-752.

[111] Nagpal V, Paknikar KM. Integrated approach for the enhanced degradation of lindane. Indian J Biotechnol, 2006, 5: 400-405.

[112] Nalin R, Simonet P, Vogel TM, Normand P. Rhodanobacter lindaniclasticus gen. nov., sp. nov., a lindane-degrading bacterium. Int J Syst Bacteriol, 1999, 49: 19-23.

[113] Nanasato Y, Namiki S, Oshima M, Moriuchi R, Konagaya K, Seike N, Otani T, Nagata Y, Tsuda M, Tabei Y. Biodegradation of γ-hexachlorocyclohexane by transgenic hairy root cultures of Cucurbita moschata that accumulate recombinant bacterial LinA. Plant Cell Rep, 2016, 35(9): 1963-1974.

[114] Nandavaram A, Sagar AL, Madikonda AK, Siddavattam D. Proteomics of Sphingobium indicum B90A for a deeper understanding of hexachlorocyclohexane (HCH) bioremediation. Rev Environ Health, 2016, 31(1): 57-61.

[115] Nawab A, Aleem A, Malik A. Determination of organochlorine pesticides in agricultural soil with special reference to c-HCH degradation by Pseudomonas strains. Biores Technol, 2003, 88: 41-46.

[116] Nichols TD, Wolf DC, Roders HB, Beyrouty CA, Renolds CM. Rhizosphere microbial populations in contaminated soils. Water Air Soil Pollut, 1997, 95: 165-178.

[117] Ohisa N, Yamaguchi M. Gamma-BHC degradation accompanied by the growth of Clostridium rectum isolated from paddy field soil. Agric Bio Chem, 1978, 42: 1819-1823.

[118] Okeke BC, Siddique T, Arbestain MC, Frankenberger WT. Biodegradation of c-hexachlorocyclohexane (Lindane) and a-hexachlorocyclohexane in water and a soil slurry by a Pandoraea species. J Agric Food Chem, 2002, 50: 2548-2555.

[119] Osterreicher-Cunha P, Langenbach T, Torres JP, Lima AL, de Campos TM. HCH distribution and microbial parameters after liming of a heavily contaminated soil in Rio de Janeiro. Environ Resource, 2003, 93: 316-327.

[120] Pacwa-Plociniczak M, Plaza GA, Piotrowska-Seget Z, Cameotra SS. Environmental applicatications of biosurfactants: recent advances. Int J Mol Sci, 2011, 12(1): 633-654.

[121] Paknikar KM, Nagpal V, Pethkar AV, Rajwade JM. Degradation of lindane from aqueous solutions using iron sulfide nanoparticles stabilized by biopolymers. Sci Technol Adv Mat, 2005, 6: 370-374.

[122] Pal R, Bala S, Dadhwal M, Kumar M, Dhingra G, Prakash O, Prabagaran SR, Shivaji S, Cullum J, Holliger C, Lal R. Hexachlorocyclohexane- degrading bacterial strains Sphingomonas paucimobilis B90A, UT26 and Sp_, having similar lin genes, represent three distinct species, Sphingobium indicum sp. nov., Sphingobium japonicum sp. nov. and Sphingobium francense sp. nov., and reclassification of [Sphingomonas] chungbukensis as Sphingobium chungbukense comb. nov. Int J Syst Evol Microbiol, 2005, 55: 1965-1972.

[123] Pannu R, Kumar D. Process optimization of γ- Hexachlorocyclohexane degradation using three novel Bacillus sp. strains. Biocatal Agric Biotechol, 2017, 11: 97-107.

[124] Pearce SL, Oakeshott JG, Pandey G. Insights into ongoing evolution of the hexachlorocyclohexane catabolic pathway from comparative genomics of ten Sphingomonadaceae strains. G3 (Bethesda), 2015, 5(6): 1081-1094.

[125] Pesce SF, Wunderlin DA. Biodegradation of lindane by a native bacterial consortium isolated from contaminated river sediment. Int  Biodeterior Biodegrad, 2004, 54: 255-260.

[126] Pesce SF, Cazenave J, Monferrán MV, Frede S, Wunderlin DA. Integratedsurvey on toxic effects of lindane on neotropical fish: Corydoraspaleatus and Jenynsiamultidentata. Environ Pollut, 2008, 156: 775-783.

[127] Phillips TM, Seech AG, Lee H, Trevors JT. Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation, 2005, 16: 363-392.

[128] Phillips TM, Lee H, Trevors JT, Seech AG. Full-scale in situ bioremediationof hexachlorocyclohexane-contaminated soil. J Chem Technol Biotech, 2006, 81: 289-298.

[129] Pino NJ, Domínguez MC, Penuela GA. Isolation of a selected microbialconsortium capable of degrading methyl parathion and p-nitrophenol from a contaminated soil site. J Environ Sci Health, 2011, 46: 173-180.

[130] Polti MA, Aparicio JD, Benimeli CS, Amoroso MJ. Simultaneous bioremediation of Cr(VI) and lindane in soil by actinobacteria. Int  Biodeterior Biodeg, 2014, 88: 48-55.

[131] Prakash O, Suar M, Raina V, Dogra C, Pal R, Lal R. Residues of hexachlorocyclohexane isomers in soil and water samples from Delhi and adjoining areas. Curr Sci, 2004, 87: 73-77.

[132] Quintero JC, Moreira MT, Feijoo G, Lema JM. Anaerobic degradation of hexachlorocyclohexane isomers in liquid and soil slurry systems. Chemosphere, 2005, 61: 528-536.

[133] Raymond J, Rogers T, Shonnard D, Kline A. A review of structure based biodegradation estimation methods. J Hazard Mater, 2001, 84: 189-215.

[134] Rigas F, Papadopoulou K, Philippoussis A, Papadopoulou M, Chatzipavlidis J. Bioremediation of lindane contaminated soil by Pleurotus ostreatus in non sterile conditions using multilevel factorial design. Water Air Soil Pollut, 2009, 197: 121-129.

[135] Rijnaarts HMM, Bachmann A, Jumelet JC, Zehnder AJB. Effect of desorption and intraparticle mass transfer on the aerobic biomineralization of ã-hexachlorocyclohexane in a calcerous soil. Environ Sci Technol, 1990, 24: 1349-1354.

[136] Robles-Gonzalez IV, Fava F, Poggi-Varaldo HM. A review on slurry bioreactors for bioremediation of soils and sediments. Microb Cell Factories, 2008, 7: 1-16.

[137] Roh Y, Cho KS, Lee S. Electrochemical reduction of trichloroethene contaminated groundwater using palladized iron oxides. J Environ Sci Health A, 2001, 36: 923-933.

[138] Romano ML, Stephenson GR, Tal A, Hall JC. The effect of monooxygenase and glutathione S-transferase inhibitors on the metabolism of diclofop-methyl and fenoxaprop-ethyl in barley and wheat. Pesti Biochem Physiol, 1993, 46: 181-189.

[139] Roy C, Gaillardon P, Montfort F. The effect of soil moisture content on the sorption of five sterol biosynthesis inhibiting fungicides as a function of their physicochemical properties. Pest Manag Sci, 2000, 56: 795-803.

[140] Saez JM, Alvarez A, Benimeli CS, Amoroso MJ. Enhanced lindane removal from soil slurry by immobilized Streptomyces consortium. Int  Biodeterior Biodeg, 2014, 93: 63-69.

[141] Sahu SK, Patnaik KK, Sharmila M, Sethunathan N. Degradation of alpha-, beta-, and gamma-hexachlorocyclohexane by a soil bacterium under aerobic conditions. Appl Environ Microbiol, 1990, 56: 3620-3622.

[142] Sahu SK, Patnaik KK, Bhuyan S, Sreedharan B, Kurihara N, Adhya TK, Sethunathan N. Mineralization of α-, γ- and β-isomers of hexachlorocyclohexane by a soil bacterium under aerobic conditions. J Agric Food Chem, 1995, 43: 833-837.

[143] Sáinz MJ, González-Penalta B, Vilariño A. Effects of hexachlorocyclohexane onrhizosphere fungal propopagules and root colonization by arbuscular mycorrhizal fungi in Plantago lanceolata. Eur J Soil Sci, 2006, 57: 83-90.

[144] Salam JA, Das N. Lindane degradation by Candida VITJzN04, a newly isolated yeast strain from contaminated soil: kinetic study, enzyme analysis and biodegradation pathway. World J Microbiol Biotechnol, 2014, 30: 1301-1311.

[145] Salam JA, Das N. Degradation of lindane by a novel embedded bio-nano hybrid system in aqueous environment. Appl Microbiol Biotechnol, 2015, 99(5): 2351-2360.

[146] Salam JA, Hatha MAA, Das N. Microbial-enhanced lindane removal by sugarcane (Saccharum officinarum) in doped soil-applications in phytoremediation and bioaugmentation. J Environ Manag, 2017, 193: 394-399.

[147] Salem JA, Das N. Remediation of lindane from environment-an overview. Int J Adv Biol Res, 2012, 2: 9-15.

[148] Salem JAA, Lakshmi V, Das D, Das N. Biodegradation of lindane using a novel yeast strain, Rhodotorula sp. VITJzN03 isolated from agricultural soil. World J Microbiol Biotechnol, 2013, 29(3): 475-4873.

[149] Sangwan N, Lata P, Dwivedi V, Singh A, Niharika N. Comparative metagenomic analysis of soil microbial communities across three hexachlorocyclohexane contamination levels. PLoS ONE, 2012, 7(9): e46219.

[150] Sangwan N, Verma H, Kumar R, Negi V, Lax S, Khurana P, Khurana JP, Gilbert JA, Lal R. Reconstructing an ancestral genotype of two hexachlorocyclohexane-degrading Sphingobium species using metagenomic sequence data. ISME J, 2014, 8(2): 398-408.

[151] Schrick B, Hydutsky BW, Blough JL, Mallouk TE. Delivery vehicles for zerovalent metal nanoparticles in soil and groundwater. Chem Mater, 2004, 16: 2187-2193.

[152] Senoo K, Wada H. Isolation and identification of an aerobic gamma-HCH-decomposing bacterium from soil. Soil Sci Plant Nutr, 1989, 35: 79-87.

[153] Shong J, Jimenez Diaz MR, Collins CH. Towards synthetic microbialconsortia forbioprocessing. Curr Opi Biotechnol, 2012, 23: 798-802.

[154] Sineli PE, Tortella G, Dávila Costa JS, Cuozzo SA. Evidence of α-, β- and γ-HCH mixture aerobic degradation by the native actinobacteria Streptomyces sp. M7. World J Microbiol Biotechnol, 2016, 32: 81-90.

[155] Singh BK, Kuhad RC. Biodegradation of lindane (ã-hexachlorocyclohexane) by the white- rot fungus Trametes hirsustus. Lett Appl Microbiol, 1999, 28: 238-241.

[156] Singh R, Manickam N, Mudiam MKR, Murthy RC, Misra V. An integrated (nano-bio) technique for degradation of γ-HCH contaminated soil. J Hazard Mat, 2013, 258–259: 35-41.

[157] Stomp AM, Han KH, Wilbert S, Gordon MP. Genetic improvement of tree species for remediation of hazardous wastes. In Vitro Cell Dev Biol Plant, 1993, 29: 227-232.

[158] Sul WJ, Park J, Quensen JF 3rd, Rodrigues JL, Seliger L, Tsoi TV, Zylstra GJ, Tiedje JM. DNA-stable isotope probing integrated with metagenomics for retrieval of biphenyl dioxygenase genes from polychlorinated biphenyl-contaminated river sediment. Appl Environ Microbiol, 2009, 75(17): 5501-5506.

[159] Svrcek J, Marhoul A, Kacer P, Kuzma M, Panek L, Cerveny L. The influence of operating conditions on the efficiency of vapour phase hydrogen peroxide in degradation of 4-(dimethylamino) benzaldehyde. Chemosphere, 2010, 81(5): 617-625.

[160] Thomas JC, Berger F, Jacquier M, Bernillon D, Baud-Grasset F, Truffaut N, Normand P, Vogel TM, Simonet P. Isolation and characterization of a novel c-hexachlorocyclohexane- degrading bacterium. J Bacteriol, 1996, 178: 6049-6055.

[161] Tu CM. Utilization and degradation of lindane by soil microorganisms. Arch Microbiol, 1976, 108: 259-263.

[162] Usman M, Tascone O, Rybnikova V, Faure P, Hanna K. Application of chemical oxidation to remediate HCH-contaminated soil under batch and flow through conditions. Environ Sci Pollut Res Int, 2017, 24(17): 14748-14757.

[163] Van Eerd LL. Pesticide metabolism in plants and microorganisms. Weed Sci, 2003, 51: 472-495.

[164] van Liere H, Staps S, Pijls C, Zwiep G, Lassche R et al. (2003) Full scale case: successful in situ bioremediation of a HCH ontaminated industrial site in central Europe (The Netherlands). In: Forum book, 7th International HCH and Pesticides Forum. Sustainable Development and Ecological Research Center. J Vijgen (ed.) Kiev, Ukraine. pp. 128–132

[165] Venier M, Hung H, Tych W, Hites RA. Temporal trends of persistent organic pollutants: a comparison of different time series models. Environ Sci Technol, 2012, 46(7): 3928-3934.

[166] Verma H, Kumar R, Oldach P, Sangwan N, Khurana JP, Gilbert JA, Lal R. Comparative genomic analysis of nine Sphingobium strains: insights into their evolution and hexachlorocyclohexane (HCH) degradation pathways. BMC Genom, 2014, 15(1): 1014.

[167] Vlčková K, Hofman J. A comparison of POPs bioaccumulation in Eiseniafetida in natural and artificial soils and the effects of aging. Environ Pollut, 2012, 160: 49-56.

[168] Wattanaphon HT, Kerdsin A, Thammacharoen C, Sangvanich P, Vangnai AS. A biosurfactant from Burkholderia cenocepacia BSP3 and its enhancement of pesticide solubilization. J Appl Microbiol, 2008, 23: 1365-2672.

[169] Wiren-Lehr S, Scheunert L, Dorfler U. Mineralisation of plant-incorporated residues of ¹⁴C-isoproturon in arable soils originating from different farming systems. Geoderma, 2002, 105: 351-366.

[170] Wu J, Hong Q, Han P, He J, Li S. A gene linB2 responsible for the conversion of γ-HCH and 2,3,4,5,6-pentachlorocyclohexanol in Sphingomonas sp. BHC-A. Appl Microbiol Biotechnol, 2007, 73: 1097-1105.

[171] Wu J, Hong Q, Sun Y, Hong Y, Yan Q, Li S. Analysis of the role of LinA and LinB in biodegradation of _-hexachlorocyclohexane. Environ Microbiol, 2007, 9: 2331-2340.

[172] Wu BZ, Chen G, Yak H, Liao W, Chiu K, Peng SM. Degradation of lindane and hexachlorobenzene in supercritical carbon dioxide using palladium nanoparticles stabilized in microcellular high-density polyethylene. Chemosphere, 2016, 152: 345-352.

[173] Yamamoto SS, Otsuka Y, Murakami M, Senoo K. Genetic diversity of gamma-hexachlorocyclohexane-degrading sphingomonads isolated from a single experimental field. Lett Appl Microbiol, 2009, 49: 472-477.

[174] Yang C, Yu H, Jiang H, Qiao C, Liu R. An engineered microorganism can simultaneously detoxify cadmium, chlorpyrifos, and γ-hexachlorocyclohexane. J Basic Microbiol, 2016, 56(7): 820-826.

[175] Yang J, Shen F, Qiu M, Qi X. Catalytic dehydrochlorination of lindane by nitrogen-containing multiwalled carbon nanotubes (N-MWCNTs). Sci Total Environ, 2017, 621: 1445-1452.

[176] Yule WN, Chiba M, Morely HV. Fate of insecticide residues. Decomposition of lindane in soil. J Agric Food Chem, 1967, 15: 1000-1004.

[177] Zaprasis A, Liu YJ, Liu SJ, Drake HL, Horn MA. Abundance of novel and diverse tfdA-like genes, encoding putative phenoxyalkanoic acid herbicide-degrading dioxygenases, in soil. Appl Environ Microbiol, 2010, 76(1): 119-128.

[178] Zhang WX. Nanoscale iron particles for environmental remediation: an overview. J Nanopart Res, 2003, 5: 323-332.

[179] Zhao D. Destruction and lindane and atrazine using stabilized iron nanoparticles under aerobic and anaerobic conditions: effect of catalyst and stabilizer. Chemosphere, 2008, 70: 418-425.

[180] Zhu Y, Liu H, Xi Z, Cheng H, Xu X. Organochlorine pesticides (DDTs and HCHs) in soils from the outskirts of Beijing, China. Chemosphere, 2005, 60: 770-778.

[181] Zinovyev SS, Shinkova NA, Perosa A, Tundo P. Dechlorination of lindane in the multiphase catalytic reduction system with Pd/C, Pt/C and Raney-Ni. Appl Catal B, 2004, 47: 27-36.

Funding

University Grants Commission(F.No.42-449/2013 (SR))