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Anaerobic biotransformation of hexachlorocyclohexane isomers by Dehalococcoides species and an enrichment culture

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Abstract

The biotransformation of hexachlorocyclohexane isomers (HCH) by two Dehalococcoides mccartyi strains (195 and BTF08) and an enrichment culture was investigated and compared to conversion by the obligate anaerobic strain Clostridium pasteurianum strain DSMZ 525. The D. mccartyi strains preferentially transformed γ-HCH over α-HCH and δ-HCH isomers while β-HCH biotransformation was not significant. In case of the enrichment culture, γ-HCH was preferentially transformed over the δ-HCH, β-HCH and α-HCH isomers. Major observed metabolites in both cases were tetrachlorocyclohexene and as end products monochlorobenzene (MCB) and benzene. Dechlorination of the γ-HCH isomer was linked to an increase in cell numbers for strain 195. γ-HCH transformation was linked to considerable carbon stable isotope fractionation with the enrichment factor εc = − 5.5 ± 0.8‰ for D. mccartyi strain 195, εc = − 3.1 ± 0.4‰ for the enrichment culture and εc = − 4.1 ± 0.6‰ for co-metabolic transformation by C. pasteurianum.

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References

  • Adrian L, Hansen SK, Fung JM, Görisch H, Zinder SH (2007) Growth of Dehalococcoides strains with chlorophenols as electron acceptors. Environ Sci Technol 41:2318–2323

    Article  PubMed  CAS  Google Scholar 

  • Bachmann A, De Bruin W, Jumelet J, Rijnaarts H, Zehnder A (1988) Aerobic biomineralization of alpha-hexachlorocyclohexane in contaminated soil. Appl Environ Microbiol 54:548–554

    PubMed  PubMed Central  CAS  Google Scholar 

  • Badea SL, Vogt C, Weber S, Danet AF, Richnow HH (2009) Stable isotope fractionation of gamma-hexachlorocyclohexane (Lindane) during reductive dechlorination by two strains of sulfate-reducing bacteria. Environ Sci Technol 43:3155–3161

    Article  PubMed  CAS  Google Scholar 

  • Badea SL, Vogt C, Gehre M, Fischer A, Danet AF, Richnow HH (2011) Development of an enantiomer-specific stable carbon isotope analysis (ESIA) method for assessing the fate of α-hexachlorocyclohexane in the environment. Rapid Commun Mass Spectrom 25:1363–1372

    Article  PubMed  CAS  Google Scholar 

  • Bashir S, Fischer A, Nijenhuis I, Richnow H-H (2013) Enantioselective carbon stable isotope fractionation of hexachlorocyclohexane during aerobic biodegradation by Sphingobium spp. Environ Sci Technol 47:11432–11439

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bashir S, Hassan W, Niazi NK, Bibi I, Ahmad N (2017) Current approaches for the assessment of in situ remediation of xenobiotics. In: Hashmi M, Kumar V, Varma A (eds) Xenobiotics in the soil environment, vol. 49. Springer, Cham, pp 171–196

    Chapter  Google Scholar 

  • Boyle AW, Häggblom 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

    CAS  Google Scholar 

  • Bradley AE, Shoenfelt JL, Durda JL (2016) Carcinogenicity and mode of action evaluation for alphahexachlorocyclohexane: implications for human health risk assessment. Regul Toxicol Pharmacol 76:152–173

    Article  PubMed  CAS  Google Scholar 

  • Buser H-R, Mueller MD (1995) Isomer and enantioselective degradation of hexachlorocyclohexane isomers in sewage sludge under anaerobic conditions. Environ Sci Technol 29:664–672

    Article  PubMed  CAS  Google Scholar 

  • Cichocka D, Nikolausz M, Haest PJ, Nijenhuis I (2010) Tetrachloroethene conversion to ethene by a Dehalococcoides-containing enrichment culture from Bitterfeld. FEMS Microbiol Ecol 72:297–310

    Article  PubMed  CAS  Google Scholar 

  • Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560

    Article  PubMed  CAS  Google Scholar 

  • Doesburg V, 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

    Article  PubMed  CAS  Google Scholar 

  • Elango V, Kurtz HD Jr, 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

    Article  PubMed  CAS  Google Scholar 

  • Elsner M (2010) Stable isotope fractionation to investigate natural transformation mechanisms of organic contaminants: principles, prospects and limitations. J Environ Monit 12:2005–2031

    Article  PubMed  CAS  Google Scholar 

  • Garg N, Lata P, Jit S, Sangwan N, Singh AK, Dwivedi V, Niharika N, Kaur J, Saxena A, Dua A (2016) Laboratory and field scale bioremediation of hexachlorocyclohexane (HCH) contaminated soils by means of bioaugmentation and biostimulation. Biodegradation 27:179–193

    Article  PubMed  CAS  Google Scholar 

  • Heritage A, MacRae I (1977) Degradation of lindane by cell-free preparations of Clostridium sphenoides. Appl Environ Microbiol 34:222–224

  • Jagnow G, Haider K, Ellwardt PCHR (1977) Anaerobic dechlorination and degradation of hexachlorocyclohexane isomers by anaerobic and facultative anaerobic bacteria. Arch Microbiol 115:285–292

    Article  PubMed  CAS  Google Scholar 

  • Kaufhold T, Schmidt M, Cichocka D, Nikolausz M, Nijenhuis I (2013) Dehalogenation of diverse halogenated substrates by a highly enriched Dehalococcoides-containing culture derived from the contaminated mega-site in Bitterfeld. FEMS Microbiol Ecol 83:176–188

    Article  PubMed  CAS  Google Scholar 

  • Krajmalnik-Brown R, Sung Y, Ritalahti KM, Saunders FM, Loffler FE (2007) Environmental distribution of the trichloroethene reductive dehalogenase gene (tceA) suggests lateral gene transfer among Dehalococcoides. FEMS Microbiol Ecol 59:206–214. https://doi.org/10.1111/j.1574-6941.2006.00243.x

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lal R, Pandey G, Sharma P, Kumari K, Malhotra S, Pandey R, Raina V, Kohler HPE, Holliger C, Jackson C, Oakeshott JG (2010) Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol Mol Biol Rev 74:58–80

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Y, Bashir S, Stollberg R, Trabitzsch R, Weiß H, Paschke H, Nijenhuis I, Richnow H-H (2017) Compound specific and enantioselective stable isotope analysis as tools to monitor transformation of hexachlorocyclohexane (HCH) in a complex aquifer system. Environ Sci Technol 51:8909–8916

    Article  PubMed  CAS  Google Scholar 

  • Löffler FE, Ritalahti KM, Zinder SH (2013) Dehalococcoides and reductive dechlorination of chlorinated solvents. In: Stroo H, Leeson A, Ward C (eds) Bioaugmentation for groundwater remediation. SERDP ESTCP Environmental Remediation Technology. Springer, New York, pp 39–88

  • Macrae IC, Raghu K, Bautista EM (1969) Anaerobic degradation of the insecticide lindane by clostridium sp.. Nature 221(5183):859–860

    Article  CAS  Google Scholar 

  • Maymo-Gatell X, Chien Y, Gossett JM, Zinder SH (1997) Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276(5318):1568–1571

    Article  PubMed  CAS  Google Scholar 

  • Meckenstock RU, Morasch B, Griebler C, Richnow HH (2004) Stable isotope fractionation analysis as a tool to monitor biodegradation in contaminated acquifers. J Contam Hydrol 75:215–255

    Article  PubMed  CAS  Google Scholar 

  • Mehboob F, Langenhoff AA, Schraa G, Stams AJ (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, pp 495–521

    Chapter  Google Scholar 

  • Middeldorp PJM, Jaspers M, Zehnder AJB, Schraa G (1996) Biotransformation of alpha-, beta-, gamma-, and delta-hexachlorocyclohexane under methanogenic conditions. Environ Sci Technol 30:2345–2349

    Article  CAS  Google Scholar 

  • Nagasawa S, Kikuchi R, Nagata Y, Takagi M, Matsuo M (1993) Aerobic mineralization of [gamma]-HCH by Pseudomonas paucimobilis UT26. Chemosphere 26:1719–1728

    Article  CAS  Google Scholar 

  • Nijenhuis I, Nikolausz M, Köth A, Felföldi T, Weiss H, Drangmeister J, Großmann J, Kästner M, Richnow H-H (2007) Assessment of the natural attenuation of chlorinated ethenes in an anaerobic contaminated aquifer in the Bitterfeld/Wolfen area using stable isotope techniques, microcosm studies and molecular biomarkers. Chemosphere 67:300–311

    Article  PubMed  CAS  Google Scholar 

  • Ohisa N, Yamaguchi M, Kurihara N (1980) Lindane degradation by cell-free extracts of Clostridium rectum. Arch Microbiol 125:221–225

    Article  PubMed  CAS  Google Scholar 

  • Phillips TM, Seech AG, Lee H, Trevors JT (2005) Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation 16:363–392

    Article  PubMed  CAS  Google Scholar 

  • Popp P, Brüggemann L, Keil P, Thuß U, Weiß H (2000) Chlorobenzenes and hexachlorocyclohexanes (HCHs) in the atmosphere of Bitterfeld and Leipzig (Germany). Chemosphere 41:849–855

    Article  PubMed  CAS  Google Scholar 

  • Pöritz M, Goris T, Wubet T, Tarkka MT, Buscot F, Nijenhuis I, Lechner U, Adrian L (2013) Genome sequences of two dehalogenation specialists—Dehalococcoides mccartyi strains BTF08 and DCMB5 enriched from the highly polluted Bitterfeld region. FEMS Microbiol Lett 343:101–104. https://doi.org/10.1111/1574-6968.12160

    Article  PubMed  CAS  Google Scholar 

  • Raina V, Suar M, Singh A, Prakash O, Dadhwal M, Gupta SK, Dogra C, Lawlor K, Lal S, van der Meer JR (2008) Enhanced biodegradation of hexachlorocyclohexane (HCH) in contaminated soils via inoculation with Sphingobium indicum B90A. Biodegradation 19:27–40

    Article  PubMed  CAS  Google Scholar 

  • Ricking M, Schwarzbauer J (2008) HCH residues in point-source contaminated samples of the Teltow Canal in Berlin, Germany. Environ Chem Lett 6:83–89

    Article  CAS  Google Scholar 

  • Sahu SK, Patnaik K, Bhuyan S, Sreedharan B, Kurihara N, Adhya T, 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

    Article  CAS  Google Scholar 

  • Schmidt M, Wolfram D, Birkigt J, Ahlheim J, Paschke H, Richnow H-H, Nijenhuis I (2014) Iron oxides stimulate microbial monochlorobenzene in situ transformation in constructed wetlands and laboratory systems. Sci Total Environ 472:185–193

    Article  PubMed  CAS  Google Scholar 

  • Seshadri R, Adrian L, Fouts DE, Eisen JA, Phillippy AM, Methe BA, Ward NL, Nelson WC, Deboy RT, Khouri HM (2005) Genome sequence of the PCE-dechlorinating bacterium Dehalococcoides ethenogenes. Science 307:105–108

    Article  PubMed  CAS  Google Scholar 

  • Van Eekert MH, Van Ras NJ, Mentink GH, Rijnaarts HH, Stams AJ, Field JA, Schraa G (1998) Anaerobic transformation of β-hexachlorocyclohexane by methanogenic granular sludge and soil microflora. Environ Sci Technol 32(21):3299–3304

  • Vijgen J, Abhilash P, Li YF, Lal R, Forter M, Torres J, Singh N, Yunus M, Tian C, Schäffer A (2011) Hexachlorocyclohexane (HCH) as new Stockholm Convention POPs-a global perspective on the management of Lindane and its waste isomers. Environ Sci Pollut Res 18:152–162

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Willett KL, Ulrich EM, Hites RA (1998) Differential toxicity and environmental fates of hexachlorocyclohexane isomers. Environ Sci Technol 32:2197–2207

    Article  CAS  Google Scholar 

  • Zhang N, Bashir S, Qin J, Schindelka J, Fischer A, Nijenhuis I, Herrmann H, Wick LY, Richnow HH (2014) Compound specific stable isotope analysis (CSIA) to characterize transformation mechanisms of α-hexachlorocyclohexane. J Hazard Mater 280:750–757

    Article  PubMed  CAS  Google Scholar 

  • Zinder S (1998) Methanogens. In: Burlage RS, Atlas R, Stahl D, Geesy G, Sayler G (eds) Techniques in microbial ecology. Oxford University Press, New York, pp 113–136

    Google Scholar 

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Acknowledgements

We thank to Ursula Gunther, Stephanie Hinke and Falk Bratfisch for the technical support. Safdar Bashir was supported by University of Agriculture Faisalabad, Pakistan and the Helmholtz Impulse and Networking Fund through Helmholtz Interdisciplinary Graduate School for Environmental Research (HIGRADE). This study was further funded by the Bundesministerium für Bildung und Forschung (Project INTIME 02WU1221), Germany, and Ministry of Science and Technology, Israel (BMBF-MOST).

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Correspondence to Ivonne Nijenhuis.

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Bashir, S., Kuntze, K., Vogt, C. et al. Anaerobic biotransformation of hexachlorocyclohexane isomers by Dehalococcoides species and an enrichment culture. Biodegradation 29, 409–418 (2018). https://doi.org/10.1007/s10532-018-9838-9

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  • DOI: https://doi.org/10.1007/s10532-018-9838-9

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