Abstract
Lindane (γ-HCH) is a pesticide that has mainly been used in agriculture. Lindane and the other HCH isomers are highly chlorinated hydrocarbons. The presence of a large number of electron withdrawing chlorine groups makes some of the HCH isomers rather recalcitrant in oxic environments. Especially β-HCH is poorly degraded by aerobic bacteria. The chlorine groups make HCH isomers more accessible for an initial reductive attack, a common mechanism in anoxic environments. Among the HCH isomers, γ-HCH is degraded most easily while β-HCH is most persistent. Little is known about the diversity of the microorganisms involved in anaerobic HCH degradation. Thus far, species within the genera Clostridium and Bacillus, two Desulfovibrio species, and one species each of Desulfococcus, Desulfobacter, Citrobacter and Dehalobacter have been found to metabolize lindane and other HCH isomers. Benzene and monochlorobenzene are the end products of anaerobic degradation, while in some studies pentachlorocyclohexane, tetrachlorocyclohexene, chlorobenzenes and chlorophenols have been detected as intermediates. Enzymes and coding genes involved in the reductive dechlorination of HCH isomers are largely unknown. Recently, a metagenomic analysis has indicated the presence of numerous putative reductive dehalogenase genes in the genome of β-HCH degrading Dehalobacter sp. High-throughput omics techniques can help to explore the key players and enzymes involved in the reductive dehalogenation of lindane and other HCH isomers.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bachmann A, de Bruin W, Jumelet JC, Rijnaarts HHM, Zehnder AJB (1988a) Aerobic biomineralization of alphahexachlorocyclohexane in contaminated soil. Appl Environ Microbiol 54:548–554
Bachmann A, Wijnen P, de Bruin W, Huntjens JLM, Roelofsen W, Zehnder AJB (1988b) Biodegradation of alpha- and beta-hexachlorocyclohexane in a soil slurry under different redox conditions. Appl Environ Microbiol 54:143–149
Baczynski TP, Pleissner D, Grotenhuis T (2010) Anaerobic biodegradation of organochlorine pesticides in contaminated soil-significance of temperature and availability. Chemosphere 78:22–28
Badea S-L, Vogt C, Weber S, Danet A-F, Richnow H-H (2009) Stable isotope fractionation of γ-hexachlorocyclohexane (lindane) during reductive dechlorination by two strains of sulfate-reducing bacteria. Environ Sci Technol 43:3155–3161
Baker MT, Nelson RM, van Dijke RA (1985) The formation of chlorobenzene and benzene by the reductive metabolism of lindane in rat liver microsomes. Arch Biochem Biophys 236:506–514
Benezet HJ, Matsumura F (1973) Isomerization of γ-BHC to α -BHC in the environment. Nature 243:480–481
Berg T, Kallenborn R, Manø S (2004) Challenges in arctic-alpine environmental research. Arct Antarct Alp Res 36:284–291
Beurskens JEM, Stams AJM, Zehnder AJB, Bachmann A (1991) Relative biochemical reactivity of three hexachlorocyclohexane isomers. Ecotoxicol Environ Safety 21:128–136
Bhat P, Kumar MS, Mudliar SN, Chakrabarti T (2006) Biodegradation of tech-hexachlorocyclohexane in a upflow anaerobic sludge blanket (UASB) reactor. Bioresour Technol 97:824–830
Bhatt P, Kumar MS, Mudliar SN, Chakrabarti T (2008) Enhanced biodegradation of hexachlorocyclohexane in upflow anaerobic sludge blanket reactor using methanol as an electron donor. Bioresour Technol 99:2594–2602
Boyle AW, Haggblom MM, Young LY (1999) Dehalogenation of lindane (γ-hexachlorocyclohexane) by anaerobic bacteria from marine sediments and by sulfate-reducing bacteria. FEMS Microbiol Ecol 29:379–387
Breitenstein A, Wiegel J, Haertig C, Weiss N, Andreesen JR, Lechner U (2002) Reclassification of Clostridium hydroxybenzoicum as Sedimentibacter hydroxybenzoicus gen. nov., comb. nov., and description of Sedimentibacter saalensis sp. nov. Int J Sys Evol Microbiol 52:801–807
Breivik K, Pacyna JM, Munch J (1999) Use of α, β and γ-hexachlorocyclohexane in Europe, 1970–1996. Sci Total Environ 239:151–163
Buser H-R, Müller MD (1995) Isomer and enantioselective degradation of hexachlorocyclohexane isomers in sewage sludge under anaerobic conditions. Environ Sci Technol 29:664–672
Camacho-Pérez B, Ríos-Leal E, Esparza-García F, Cortes JB, Fava F, Poggi-Varaldo HM (2010) Bioremediation of an agricultural soil polluted with lindane in triphasic, sequential methanogenic-sulfate reducing slurry bioreactors. J Biotechnol 150:S561–S562
Camacho-Pérez B, Ríos-Leal E, Rinderknecht-Seijas N, Poggi-Varaldo HM (2012) Enzymes involved in the biodegradation of hexachlorocyclohexane: a mini review. J Environ Manag 95:S306–S318
Castro TF, Yoshida T (1974) Effect of organic matter on the biodegradation of some organochlorine insecticides in submerged soils. Soil Sci Plant Nutr 20:363–370
Cui Z, Meng F, Hong J, Li X, Ren X (2012) Effects of electron donors on the microbial reductive dechlorination of hexachlorocyclohexane and on the environment. J Biosci Bioeng 113:765–770
Deo PG, Karanth NG, Karanth NGK (1994) Biodegradation of hexachlorocyclohexane isomers in soil and food environment. CRC Crit Rev Microbiol 20:57–78
Doelman P, Haanstra L, deRuiter E, Slange J (1985) Rate of microbial degradation of high concentrations of a-hexachlorocyclohexane in soil under aerobic and anaerobic conditions. Chemosphere 14:565–570
Doelman P, Haanstra L, Vos A (1988) Microbial degradation by the autochthonous soil population of alpha and beta HCH under anaerobic field conditions in temperate regions. Chemosphere 17:481–487
Dogra C, Raina V, Pal R, Suar M, Lal S, Gartemann KH, van der Meer JR, Holliger C, Lal R (2004) Organization of lin genes and IS6100 among different strains of hexachlorocyclohexane degrading Sphingomonas paucimobilis: evidence for natural horizontal transfer. J Bacteriol 186:2225–2235
Elango V, Kurtz HD, Anderson C, Freedman DL (2011) Use of γ-hexachlorocyclohexane as a terminal electron acceptor by an anaerobic enrichment culture. J Hazard Mater 197:204–210
Feldmann RJ, Maibach HI (1974) Percutaneous penetration of some pesticides and herbicides in man. Toxicol Appl Pharmacol 28:126–132
Field JA, Stams AJM, Kato M, Schraa G (1995) Enhanced biodegradation of aromatic pollutants in cocultures of anaerobic and aerobic bacterial consortia. Antonie Van Leeuwenhoek 67:47–77
Geyer HJ, Scheunert I, Korte F (1987) Correlation between the bioconcentration potential of organic environmental chemicals in humans and their n-octanol/water partition coefficients. Chemosphere 16:239–252
Haider K (1979) Degradation and metabolization of lindane and other hexachlorocyclohexane isomers by anaerobic and aerobic soil microorganisms. Z Naturforsch 34c:1066–1069
Haider K, Jagnow G (1975) Abbau von 14C-, 3H- und 36Cl-markierten γ-Hexachlorcyclohexan durch anaerobe Bodenmikroorganismen. Arch Microbiol 104:113–121
Heritage AD, MacRae IC (1977a) Degradation of lindane by cell-free preparations of Clostridium sphenoides. Appl Environ Microbiol 34:222–224
Heritage AD, MacRae IC (1977b) Identification of intermediates formed during the degradation of hexachlorocyclohexanes by Clostridium sphenoides. Appl Environ Microbiol 33:1295–1297
Heritage AD, MacRae IC (1979) Degradation of hexachlorocyclohexanes and structurally related substance by Clostridium sphenoides. Appl Environ Microbiol 33:1295–1297
Hill DW, McCarty PL (1967) Anaerobic degradation of selected chlorinated hydrocarbon pesticides. JWPCF 39:1259–1277
Jagnow G, Haider K, Ellwardt P (1977) Anaerobic dechlorination and degradation of hexachlorocyclohexane isomers by anaerobic and faculative anaerobic bacteria. Arch Microbiol 115:285–292
Jung D, Becher H, Edler L, Flesch-Janys D, Gurn P, Konietzko J, Manz A, Papke O (1997) Elimination of beta-hexachlorocyclohexane in occupationally exposed persons. J Toxicol Environ Health 51:23–34
Krishna KR, Philip L (2008) Biodegradation of lindane, methyl parathion and carbofuran by various enriched bacterial isolates. J Environ Sci Health B 43:157–171
Kurihara N, Ohisa N, Nakajima M, Kakutani T, Senda M (1981) Relation between microbial degradation and polarographic half-wave potential of polychlorocyclohexenes and BHC isomers. Agric Biol Chem 45:1229–1235
Lal R, Pandey G, Sharma P et al (2010) Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol Mol Bio Rev 74:58–80
Langenhoff AAM (2009) Bioremediation of areas polluted with chlorinated and non-chlorinated hydrocarbons. Land Contam Recl 17:295–302
Langenhoff AAM, Staps JJM, Pijls C, Alphenaar A, Zwiep G, Rijnaarts HHM (2002) Intrinsic and stimulated in situ biodegradation of hexachlorocyclohexane (HCH). Water, Air, Soil Poll Focus 2:171–181
Law SA, Bidleman TF, Martin MJ, Ruby MV (2004) Evidence of enantioselective degradation of α-hexachlorocyclohexane in groundwater. Environ Sci Technol 38:1633–1638
Li YF (1999) Global technical hexachlorocyclohexane usage and its contamination consequences in the environment: from 1948 to 1997. Sci Total Environ 232:121–158
Lichtenstein EP, Polivka JB (1959) Persistence of some chlorinated hydrocarbon insecticides in turf soils. J Econ Ent 52:289–293
Lichtenstein EP, Schulz KR, Skrentny RF, Tsukano Y (1966) Toxicity and fate of insecticide residues in water. Arch Environ Health 12:199–212
Lodha B, Bhat P, Kumar SM, Vaidya AN, Mudliar S, Killedar DJ, Chakrabarti T (2007) Bioisomerization kinetics of γ-HCH and biokinetics of Pseudomonas aeruginosa degrading technical HCH. Biochem Eng J 35:12–19
MacRae IC, Raghu K, Castro TF (1967) Persistence and biodegradation of four common isomers of benzene hexachloride in submerged soils. J Agric Food Chem 15:911–914
MacRae IC, Raghu K, Bautista EM (1969) Anaerobic degradation of the insecticide lindane by Clostridium sp. Nature 221:859–860
MacRae IC, Yamaya Y, Yoshida T (1984) Persistence of hexachlorocyclohexane isomers in soil suspensions. Soil Biol Biochem 16:285–286
Malaiyandi M, Shah SM, Lee P (1982) Fate of alpha- and gamma-hexachlorocyclohexane isomers under simulated environmental conditions. J Environ Sci Health A A17:283–297
Maphosa F (2010) Chasing organohalide respirers: ecogenomics approaches to assess the bioremediation capacity of soils. PhD dissertation, Wageningen University, The Netherlands
Marks TS, Allpress JD, Maule A (1989) Dehalogenation of lindane by a variety of porphyrins and corrins. Appl Environ Microbiol 55:1258–1261
Mathur SP, Saha JG (1975) Microbial degradation of lindane-C14 in a flooded sandy loam soil. Soil Sci 120:301–307
Maule A, Plyte S, Quirk AV (1987) Dehalogenation of organochlorine insecticides by mixed anaerobic microbial populations. Pestic Biochem Physiol 27:229–236
Mehboob F, Weelink S, Saia FT, Junca H, Stams AJM, Schraa G (2010) Microbial degradation of aliphatic and aromatic hydrocarbons with (per)chlorate as electron acceptor. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg
Metcalf RL (1955) Organic insecticides, their chemistry and mode of action. Interscience, New York
Middeldorp PJ, Jaspers M, Zehnder AJB, Schraa G (1996) Biotransformation of α-, β-, γ-, δ-hexachlorocyclohexane under methaonogenic conditions. Environ Sci Technol 30:2345–2349
Middeldorp PJ, van Doesburg W, Schraa G, Stams AJ (2005) Reductive dechlorination of hexachlorocyclohexane (HCH) isomers in soil under anaerobic conditions. Biodegradation 16:283–290
Miyauchi K, Adachi Y, Nagata Y, Takagi M (1999) Cloning and sequencing of a novel meta-cleavage dioxygenase gene whose product is involved in degradation of γ-hexachlorocyclohexane in Sphingomonas paucimobilis. J Bacteriol 181:6712–6719
Nagasawa S, Kikuchi R, Nagata Y, Takagi M, Matsuo M (1993) Aerobic mineralization of gamma-HCH by Pseudomonas paucimobilis UT26. Chemosphere 26:1719–1728
Nagata YT, Hatta IR, Kimbara K, Fukuda M, Yano K, Takagi M (1993) Purification and characterization of γ-hexachlorocyclohexane (γ-HCH) dehydrochlorinase (LinA) from Pseudomonas paucimobilis. Biosci Biotechnol Biochem 59:1582–1583
Nagata YT, Ohtomo R, Miyauchi K, Fukuda M, Yano K, Takagi M (1994) Cloning and sequencing of a 2,5-dichloro-2,5-cyclohexadiene-1,4-diol dehydrogenase gene involved in the degradation of γ-hexachlorocyclohexane in Pseudomonas paucimobilis. J Bacteriol 176:3117–3125
Nagata K, Huang CS, Hamilton BJ, Carter DB, Narahashi T (1996) Differential effects of hexachlorocyclohexane on the GABA receptor subunits expressed in human embryonic kidney-cell line. Brain Res 738:131–137
Nagata YT, Miyauchi K, Takagi M (1999) Complete analysis of genes and enzymes for γ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. J Ind Microbiol Biotechnol 23:380–390
Nagata YT, Prokop Z, Sato Y, Jerabek P, Kumar A, Ohtsubo Y, Tsuda M, Damborsky J (2005) Degradation of γ-hexachlorocyclohexane by haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26. Appl Environ Microbiol 71:2183–2185
Neujahr HY, Rossi-Ricci G (1960) On vitamins in sewage sludge XII. Production of vitamin B12 by certain Clostridia. Acta Chem Scand 14:43–47
Newland LW, Chesters G, Lee GB (1969) Degradation of γ-BHC in simulated lake impoundments as affected by aeration. JWPCF 41:R174–R188
Ohisa N, Yamaguchi M (1978a) Degradation of gamma-BHC in flooded soils enriched with peptone. Agric Biol Chem 42:1983–1987
Ohisa N, Yamaguchi M (1978b) Gamma-BHC degradation accompanied by the growth of Clostridium rectum isolated from paddy field soil. Agric Biol Chem 42:1819–1823
Ohisa N, Yamaguchi M (1979) Clostridium species and γ-BHC degradation in paddy soil. Soil Biol Biochem 11:645–649
Ohisa N, Yamaguchi M, Kurihara N (1980) Lindane degradation by cell-free extracts of Clostridium rectum. Arch Microbiol 125:221–225
Ohisa N, Kurihara N, Yamaguchi M (1982) ATP synthesis associated with the conversion of hexachlorocyclohexane related compounds. Arch Microbiol 131:330–333
Okey RW, Bogan RH (1965) Apparent involvement of electron mechanism in limiting metabolism of pesticides. JWPCF 37:692–712
Panda S, Sharmila M, Ramanand K, Panda D, Sethunathan N (1988) Persistence of hexachlorocyclohexane isomers and carbofuran applied to surface and sub-surface layers of a flooded soil. Pestic Sci 23:199–207
Phillips TM, Seech AG, Lee H, Trevors JT (2005) Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation 16:363–392
Quintero JC, Moreira MT, Feijoo G, Lema JM (2005) Anaerobic degradation of hexachlorocyclohexane isomers in liquid and soil slurry systems. Chemosphere 61:528–536
Quintero JC, Moreira MT, Lema JM, Feijoo G (2006) An anaerobic bioreactor allows the efficient degradation of HCH isomers in soil slurry. Chemosphere 63:1005–1013
Raghu K, MacRae IC (1966) Biodegradation of the gamma isomer of benzene hexachloride in submerged soils. Science 154:263–264
Rijnaarts HHM, Bachmann A, Jumelet JC, Zehnder AJB (1990) Effect of desorption and intraparticle mass transfer on the aerobic biomineralization of α-hexachlorocyclohexane in a contaminated calcareous soil. Environ Sci Technol 24:1349–1354
Rodriguez-Garrido B, Lu-Chau TA, Feijoo G, Macias F, Monterrroso MC (2010) Reductive dechlorination of α, β-, γ-, δ-hexachlorocyclohexane isomers with hydroxocobalamin, in soil slurry systems. Environ Sci Technol 44:7063–7069
Sagelsdorff P, Lutz WK, Schlatter S (1983) The relevance of covalent binding to mouse liver DNA to the carcinogenic action of hexachlorocyclohexane isomers. Carcinogenesis 4:1267–1273
Sahu SK, Patnaik KK, Sharmila M, Sethunathan N (1990) Degradation of alpha-, beta-, and gamma-hexachlorocyclohexane by a soil bacterium under aerobic conditions. Appl Environ Microbiol 56:3620–3622
Sahu SK, Patnaik KK, Bhuyan S, Sreedharan B, Kurihara N, Adhya TK, Sethunathan N (1995) Mineralization of α-, γ-, and β-isomers of hexachlorocyclohexane by a soil bacterium under aerobic conditions. J Agric Food Chem 43:833–837
Senoo K, Wada H (1989) Isolation and identification of an aerobic gamma-HCH-decomposing bacterium from soil. Soil Sci Plant Nutr 35:79–87
Sharma P, Raina V, Kumari R, Malhotra S, Dogra C, Kumari H, Kohler H-PE, Buser H-R, Holliger C, Lal R (2006) Haloalkane dehalogenase LinB is responsible for beta- and delta-hexachlorocyclohexane transformation in Sphingobium indicum B90A. Appl Environ Microbiol 72:5720–5727
Siddaramappa R, Sethunathan N (1975) Persistence of gamma-BHC and beta-BHC in Indian rice soils under flooded conditions. Pestic Sci 6:395–403
Steinmentz R, Young PCM, Caperellgrant A, Gize EA, Madhukar BV, Benjonathan N, Bigsby RM (1996) Novel estrogenic action of the pesticide residue beta-hexachlorocyclohexane in human breast cancer cells. Cancer Res 56:5403–5409
Stewart DKR, Chisholm D (1971) Long-term persistence of BHC, DDT and Chlordane in a sandy loam soil. Can J Soil Sci 51:379–383
UNEP Stockholm Convention (2008) The new POPs under the Stockholm Convention. http://chm.pops.int. Cited 18 May 2012
Suar M, Hauser A, Poiger T, Buser H-R, Muller MD, Dogra C, Raina V, Holliger C, van der Meer JR, Lal R, Kohler H-PE (2005) Enantioselective transformation of chiral alpha HCH by HCH dehydrochlorinases (LinA1 and LinA2) from Sphingomonas paucimobilis B90A. Appl Environ Microbiol 71:8514–8518
Sugita H, Miyajima C, Deguchi Y (1991) The vitamin B12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 92:267–276
Tsukano Y, Kobayashi A (1972) Formation of γ -BTC in flooded rice field soils treated with γ-BHC. Agric Biol Chem 36:166–167
United States Food and Drug Administration (2009) Lindane shampoo and lindane lotion. http://www.fda.gov. Cited 18 May 2012
van Doesburg W, van Eekert MH, Middeldorp PJ, Balk M, Schraa G, Stams AJ (2005) Reductive dechlorination of β-hexachlorocyclohexane (β-HCH) by a Dehalobacter species in coculture with a Sedimentibacter sp. FEMS Microbiol Ecol 54:87–95
van Eekert MHA, van Ras NJP, Mentink GH, Rijnaarts HHM, Stams AJM, Field JA, Schraa G (1998) Anaerobic transformation of β-hexachlorocyclohexane by methanogenic granular sludge and soil microflora. Environ Sci Technol 32:3299–3304
Vonk JW, Quirijns JK (1979) Anaerobic formation of α-hexachlorocyclohexane from γ- hexachlorocyclohexane in soil and by Escherichia coli. Pest Biochem Physiol 12:68–74
Walker K, Vallero DA, Lewis RG (1999) Factors influencing the distribution of lindane and other hexachlorocyclohexanes in the environment. Environ Sci Technol 33:4373–4378
Willett KL, Ulrich EM, Hites RA (1998) Differential toxicity and environmental fates of hexachlorocyclohexane isomers. Environ Sci Technol 32:2197–2207
Wu WZ, Xu Y, Schramm KW, Kettrup A (1997) Study of sorption, biodegradation and isomerization of HCH in stimulated sediment/water system. Chemosphere 35:1887–1894
Wu J, Hong Q, Sun Y, Hong Y, Yan Q, Li S (2007) Analysis of the role of LinA and LinB in biodegradation of δ-hexachlorocyclohexane. Environ Microbiol 9:2331–2340
Yoshida T, Castro TE (1970) Degradation of γ-BHC in rice soils. Soil Sci Soc Am Proc 34:440–448
Acknowledgements
We would like to thank Wim van Doesburg (WUR) and Dr. Sher (AIOU) for help in making figures. We also thank the Dutch Center for Soil Quality Management and Knowledge Transfer, (SKB; www.skbodem.nl) The Netherlands, and the Wageningen Institute for Environment and Climate Research (WIMEK), The Netherlands for providing funds for the present study.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Mehboob, F., Langenhoff, A.A.M., Schraa, G., Stams, A.J.M. (2013). Anaerobic Degradation of Lindane and Other HCH Isomers. In: Malik, A., Grohmann, E., Alves, M. (eds) Management of Microbial Resources in the Environment. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5931-2_20
Download citation
DOI: https://doi.org/10.1007/978-94-007-5931-2_20
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-5930-5
Online ISBN: 978-94-007-5931-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)