Abstract
Assessment of biotic and abiotic degradation reactions by studying the variation in stable isotopic compositions of organic contaminants in contaminated soil and aquifers is being increasingly considered during the last two decades with development of Compound specific stable isotope analysis (CSIA) technique. CSIA has been recognized as a potential tool for evaluating both qualitative and quantitative degradation with measurement of shifts in isotope ratios of contaminants and their degradation products as its basis. Amongst a wide variety of environmental pollutants including monoaromatics, chlorinated ethenes and benzenes etc., it is only recently that its efficacy is being tested for assessing biodegradation of a noxious pollutant namely hexachlorocyclohexane (HCH), by pure microbial cultures as well as directly at the field site. Anticipating the increase in demand of this technique for monitoring the microbial degradation along with natural attenuation, this review highlights the basic problems associated with HCH contamination emphasizing the applicability of emerging CSIA technique to absolve the major bottlenecks in assessment of HCH. To this end, the review also provides a brief overview of this technique with summarizing the recent revelations put forward by both in vitro and in situ studies by CSIA in monitoring HCH biodegradation.
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References
Weber R, Aliyeva G, Vijgen J (2013) The need for an integrated approach to the global challenge of POPs management. Environ Sci Pollut Res Int 20:1901–1906. doi:10.1007/s11356-012-1247-8
Fang GD, Dionysiou DD, Wang Y, Al-Abed SR, Zhou DM (2012) Sulfate radical-based degradation of polychlorinated biphenyls: effects of chloride ion and reaction kinetics. J Hazard Mat 227:394–401. doi:10.1016/j.jhazmat.2012.05.074
Lal R, Pandey G, Sharma P, Kumari K, Malhotra S, Pandey R, Raina V, Kohler HP, Holliger C, Jackson C, Oakeshott JG (2010) Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol Mol Biol Rev 74:58–80. doi:10.1128/MMBR.00029-09
López Ó, Fernández-Bolaños JG (2011) Green trends in insect control (No. 11). Royal Society of Chemistry
Nolan K, Kamrath J, Levitt J (2012) Lindane toxicity: a comprehensive review of the medical literature. Pediatr Dermatol 29:141–146. doi:10.1111/j.1525-1470.2011.01519.x
Perry AS, Yamamoto I, Ishaaya I, Perry RY (2013) Insecticides in agriculture and environment: retrospects and prospects. Springer, Berlin
Akoto O, Oppong-Otoo J, Osei-Fosu P (2015) Carcinogenic and non-carcinogenic risk of organochlorine pesticide residues in processed cereal-based complementary foods for infants and young children in Ghana. Chemosphere 132:193–199. doi:10.1016/j.chemosphere.2015.02.056
Wöhrnschimmel H, Tay P, von Waldow H, Hung H, Li YF, MacLeod M, Hungerbuhler K (2012) Comparative assessment of the global fate of α-and β-hexachlorocyclohexane before and after phase-out. Environ Sci Technol 46:2047–2054. doi:10.1021/es203109q
Phillips Theresa M, Seech AG, Lee H, Trevors JT (2005) Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation 16:363–392. doi:10.1007/s10532-004-2413-6
Vijgen J, Abhilash PC, Li YF, Lal R, Forter M, Torres J, Singh N, Yunus M, Tian C, Schäffer A, Weber R (2011) Hexachlorocyclohexane (HCH) as new Stockholm Convention POPs—a global perspective on the management of Lindane and its waste isomers. Environ Sci Pollut R 18:152–162. doi:10.1007/s11356-010-0417-9
Vijgen J, Aliyeva G, Weber R (2013) The Forum Of The International HCH and Pesticides Association—a platform for international cooperation. Environ Sci Pollut Res 20:2081–2086. doi:10.1007/s11356-012-1170-z
Vijgen, J, Yi LF, Forter M, Lal R, Weber R (2006) The legacy of lindane and technical HCH production. Organohalog Comp 68:899–904. (https://www.researchgate.net/profile/Rup_Lal/publication/267410840_The_legacy_of_lindane_and_technical_HCH_production_Organohalog_Compd/links/54ab68b30cf25c4c472f773f.pdf)
Schaap MM, Zwart EP, Wackers PF, Huijskens I, van de Water B, Breit TM, van Steeg H, Jonker MJ, Luijten M (2012) Dissecting modes of action of non-genotoxic carcinogens in primary mouse hepatocytes. Arch Toxicol 86:1717–1727. doi:10.1007/s00204-012-0883-6
Alavanja MC, Ross MK, Bonner MR (2013) Increased cancer burden among pesticide applicators and others due to pesticide exposure. CA Cancer J Clin 63:120–142. doi:10.3322/caac.21170
Mrema EJ, Rubino FM, Brambilla G, Moretto A, Tsatsakis AM, Colosio C (2013) Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicology 307:74–88. doi:10.1016/j.tox.2012.11.015
Heeb NV, Zindel D, Geueke B, Kohler HP, Lienemann P (2012) Biotransformation of Hexabromocyclododecanes (HBCDs) with LinB- An HCH-Converting Bacterial Enzyme. Environ Sci Technol 46:6566–6574. doi:10.1021/es2046487
Odukkathil G, Vasudevan N (2013) Toxicity and bioremediation of pesticides in agricultural soil. Rev Environ Sci Biotechnol 12:421–444. doi:10.1007/s11157-013-9320-4
Wycisk P, Stollberg R, Neumann C, Gossel W, Weiss H, Weber R (2013) Integrated methodology for assessing the HCH groundwater pollution at the multi-source contaminated mega-site Bitterfeld/Wolfen. Environ Sci Pollut Res Int 20:1907–1917. doi:10.1007/s11356-012-0963-4
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. doi:10.1016/j.watres.2014.12.033
Jit S, Dadhwal M, Kumari H, Jindal S, Kaur J, Lata P, Niharika N et al (2011) Evaluation of hexachlorocyclohexane contamination from the last lindane production plant operating in India. Environ Sci Pollut Res Int 18:586–597. doi:10.1007/s11356-010-0401-4
Kallenborn R, Halsall C, Dellong M, Carlsson P (2012) The influence of climate change on the global distribution and fate processes of anthropogenic persistent organic pollutants. J Environ Monit 14:2854–2869. doi:10.1039/C2EM30519D
IARC (1979) Hexachlorocyclohexane (technical HCH and lindane). In: Some halogenated hydrocarbons. IARC monographs on the evaluation of carcinogenic risk of chemicals to humans, vol 20. Lyon, France, International Agency for Research on Cancer. pp 195–239
Hazardous Substances Data Bank (HSDB) (2003). A database of the National Library of Medicine’s TOXNET system
US Department of Health and Human Services. Toxicological profile for alpha-, beta-, gamma-, and delta-hexachlorocyclohexane. Atlanta, GA: Public Health Service Agency for Toxic Substances and Disease Registry. 2005. (http://www.atsdr.cdc.gov/toxprofiles/tp43.pdf)
Lide DR (1991) CRC handbook of chemistry and physics, 72nd edn. CRC Press, Boca, pp 3–241
Hollifield HC (1979) Rapid nephelometric estimate of water solubility of highly insoluble organic chemicals of environmental interest. Bull Environ Contam Toxicol 23:579–586. doi:10.1007/BF01770007
Clayton G, Clayton F (1981) Patty’s industrial hygiene and toxicology, 3rd edn. John Wiley, New York, pp 2786–2788
Rippen G, Ilgenstein M, Klöpffer W, Poremski HJ (1982) Screening of the adsorption behavior of new chemicals: natural soils and model adsorbents. Ecotox Environ Safety 6:236–245. doi:10.1016/0147-6513(82)90014-8
Weiss G (1986) Hazardous chemicals data book, 2nd edn. Noyes Data Corporation, Park Ridge, p 153
Alvarez A, Benimeli CS, Saez JM, Fuentes MS, Cuozzo SA, Polti MA, Amoroso MJ (2012) Bacterial bio-resources for remediation of hexachlorocyclohexane. Intern J Mol Sci 13:15086–15106. doi:10.3390/ijms131115086
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. doi:10.1016/j.jenvman.2011.06.047
Chen H, Gao B, Wang S, Fang J (2015) Microbial Degradation of Hexachlorocyclohexane (HCH) Pesticides. Advances in Biodegradation and Bioremediation of Industrial Waste
Usman M, Tascone O, Faure P, Hanna K (2014) Chemical oxidation of hexachlorocyclohexanes (HCHs) in contaminated soils. Sci Total Environ 476:434–439. doi:10.1016/j.scitotenv.2014.01.027
Kolvenbach BA, Helbling DE, Kohler HP, Corvini PF (2014) Emerging chemicals and the evolution of biodegradation capacities and pathways in bacteria. Curr Opin Biotechnol 27:8–14. doi:10.1016/j.copbio.2013.08.017
Sangwan N, Lata P, Dwivedi V, Singh A, Niharika N, Kaur J, Anand S, Malhotra J, Jindal S, Nigam A, Lal D et al (2012) Comparative metagenomic analysis of soil microbial communities across three hexachlorocyclohexane contamination levels. PLoS ONE 7(9):e46219. doi:10.1371/journal.pone.0046219
Verma H, Kumar R, Oldach P, Sangwan N, Khurana JP, Gilbert JA, Lal R (2014) Comparative genomic analysis of nine Sphingobium strains: insights into their evolution and hexachlorocyclohexane (HCH) degradation pathways. BMC Genom 15:1. doi:10.1186/1471-2164-15-1014
Anand S, Sangwan N, Lata P, Kaur J, Dua A, Singh AK, Verma M, Kaur J, Khurana JP, Khurana P, Mathur S (2012) Genome sequence of Sphingobium indicum B90A, a hexachlorocyclohexane-degrading bacterium. J Bacteriol 194:4471–4472. doi:10.1186/1471-2164-15-1014
Garg N, Bala K, Lal R (2012) Sphingobium lucknowense sp. nov., a hexachlorocyclohexane (HCH)-degrading bacterium isolated from HCH-contaminated soil. Int J Syst Evol Microbiol 62:618–623. doi:10.1099/ijs.0.028886-0
Niharika N, Sangwan N, Ahmad S, Singh P, Khurana JP, Lal R (2013) Draft genome sequence of Sphingobium chinhatense strain IP26T, isolated from a hexachlorocyclohexane dumpsite. Genome Announc 1:e00680. doi:10.1128/genomeA.00680-13
Mukherjee U, Kumar R, Mahato NK, Khurana JP, Lal R (2013) Draft genome sequence of Sphingobium sp. strain HDIPO4, an avid degrader of hexachlorocyclohexane. Genome Announc 1:e00749–13. doi: 10.1128/genomeA.00749-13
Kohli P, Dua A, Sangwan N, Oldach P, Khurana JP, Lal R (2013) Draft genome sequence of Sphingobium ummariense strain RL-3, a hexachlorocyclohexane-degrading bacterium. Genome Announc 1:e00956. doi:10.1128/genomeA.00956-13
Garg N, Lata P, Jit S, Sangwan N, Singh AK, Dwivedi V, Niharika N, Kaur J, Saxena A, Dua A, Nayyar N, Kohli P et al (2016) Laboratory and field scale bioremediation of hexachlorocyclohexane (HCH) contaminated soils by means of bioaugmentation and biostimulation. Biodegradation 27:179–193. doi:10.1007/s10532-016-9765-6
Tabata M, Ohtsubo Y, Ohhata S, Tsuda M, Nagata Y (2013) Complete genome sequence of the γ-hexachlorocyclohexane-degrading bacterium Sphingomonas sp. strain MM-1. Genome Announc 1(3):e00247-13. doi: 10.1128/genomeA.00247-13
Nagata Y, Miyauchi K, Takagi M (1999) Complete analysis of genes and enzymes forγ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. J Ind Microbiol Biotechnol 23:380–390. doi:10.1038/sj.jim.2900736
Nagata Y, Endo R, Ito M, Ohtsubo Y, Tsuda M (2007) Aerobic degradation of lindane (γ-hexachlorocyclohexane) in bacteria and its biochemical and molecular basis. Appl Microbiol Biotechnol 76:741–752. doi:10.1007/s00253-007-1066-x
Mehboob F, Langenhoff AA, Schraa G, Stams AJ (2013) Anaerobic degradation of lindane and other HCH Isomers. In: Management of microbial resources in the environment. Springer, Netherlands. pp. 495–521
Langenhoff AA, Staps SJ, Pijls C, Rijnaarts HH (2013) Stimulation of hexachlorocyclohexane (HCH) biodegradation in a full scale in situ bioscreen. Environ Sci Technol 47:11182–11188. doi:10.1021/es4024833
Bombach P, Richnow HH, Kästner M, Fischer A (2010) Current approaches for the assessment of in situ biodegradation. Appl Microbiol Biotechnol 86:839–852. doi:10.1007/s00253-010-2461-2
Meckenstock RU, Morasch B, Griebler C, Richnow HH (2004) Stable isotope fractionation analysis as a tool to monitor biodegradation in contaminated auquifers. J Contam Hydrol 75:215–255. doi:10.1016/j.jconhyd.2004.06.003
Thullner M, Centler F, Richnow HH, Fischer A (2012) Quantification of organic pollutant degradation in contaminated aquifers using compound specific stable isotope analysis—review of recent developments. Org Geochem 42:1440–1460. doi:10.1016/j.orggeochem.2011.10.011
Callaghan AV (2013) Metabolomic investigations of anaerobic hydrocarbon-impacted environments. Curr Opin Biotechnol 24:506–515. doi:10.1016/j.copbio.2012.08.012
Bombach P, Nägele N, Rosell M, Richnow HH, Fischer A (2015) Evaluation of ethyl tert-butyl ether biodegradation in a contaminated aquifer by compound-specific isotope analysis and in situ microcosms. J Hazard Mater 286:100–106. doi:10.1016/j.jhazmat.2014.12.028
Kuder T, Philp P (2013) Demonstration of compound-specific isotope analysis of hydrogen isotope ratios in chlorinated ethenes. Environ Sci Technol 47:1461–1467. doi:10.1021/es303476v
Hatzinger PB, Böhlke JK, Sturchio NC (2013) Application of stable isotope ratio analysis for biodegradation monitoring in groundwater. Curr Opin Biotechnol 24:542–549. doi:10.1016/j.copbio.2012.11.010
Vogt C, Richnow HH (2013) Bioremediation via in situ microbial degradation of organic pollutants. Geobiotechnology II. Springer, Berlin, pp 123–146
Nijenhuis I, Schmidt M, Pellegatti E, Paramatti E, Richnow HH, Gargini A (2013) A stable isotope approach for source apportionment of chlorinated ethene plumes at a complex multi-contamination events urban site. J Cont Hydrol 153:92–105. doi:10.1016/j.jconhyd.2013.06.004
Badea SL, Vogt C, Weber S, Danet AF, Richnow HH (2009) Stable isotope fractionation of γ-hexachlorocyclohexane (lindane) during reductive dechlorination by two strains of sulfate-reducing bacteria. Environ Sci Technol 43:3155–3161. doi:10.1021/es801284m
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-hexachlorocyclo-hexane in the environment. Rapid Commun Mass Spectrom 25:1363–1372. doi:10.1002/rcm.4987
Bashir S, Fischer A, Nijenhuis I, Richnow HH (2013) Enantioselective carbon stable isotope fractionation of hexachlorocyclohexane during aerobic biodegradation by Sphingobium spp. Environ Sci Technol 47:11432–11439. doi:10.1021/es402197s
Wiegert C, Mandalakis M, Knowles T, Hovorková I, Polymenakou P, Aeppli C, Gustafsson Ö (2013) Carbon and Chlorine Stable Isotope Fractionation during Anaerobic Degradation of α-Hexachlorocyclohexane by a Mixed Culture Enriched from a Contaminated Site. Environ Sci Technol. ISSN 0013-936X, E-ISSN 1520-5851 (http://www.diva-portal.org/smash/record.jsf?pid=diva2%3A650015&dswid=article)
Chartrand M, Passeport E, Rose C, Lacrampe Couloume G, Bidleman TF, Jantunen LM, Sherwood Lollar B (2015) Compound specific isotope analysis of hexachlorocyclohexane isomers: a method for source fingerprinting and field investigation of in situ biodegradation. Rapid Commun Mass Spectrom 29:505–514. doi:10.1002/rcm.7146
Greenwood NN, Earnshaw A (2012) Chemistry of the Elements. Elsevier
Reimann C, De Caritat P (2012) Chemical elements in the environment: factsheets for the geochemist and environmental scientist. Springer, Berlin
Brand WA, Coplen TB (2012) Stable isotope deltas: tiny, yet robust signatures in nature. Isot Environ Health S 48:393–409. doi:10.1080/10256016.2012.666977
Creager AN (2013) Life atomic: a history of radioisotopes in science and medicine. University of Chicago Press, Chicago
Schmitz MD, Kuiper KF (2013) High-precision geochronology. Elements 9:25–30. doi:10.2113/gselements.9.1.25
Walker JD, Geissman JW, Bowring SA, Babcock LE (2013) The geological society of America geologic time scale. Geol Soc Am Bull 125:259–272
Elsner M, Jochmann MA, Hofstetter TB, Hunkeler D, Bernstein A, Schmidt TC, Schimmelmann A (2012) Current challenges in compound-specific stable isotope analysis of environmental organic contaminants. Anal Bioanal Chem 403:2471–2491
Rundel P, Ehleringer JR, Nagy KA (eds) (2012) Stable isotopes in ecological research. Springer, Berlin
Matthew DE, Hayes JM (1978) Isotope Ratio Monitoring GC-MS. Anal Chem 50:1465–1473. doi:10.1021/ac50033a022
Cincinelli A, Pieri F, Zhang Y, Seed M, Jones KC (2012) Compound specific isotope analysis (CSIA) for chlorine and bromine: a review of techniques and applications to elucidate environmental sources and processes. Environ Pollut 169:112–127. doi:10.1016/j.envpol.2012.05.006
Yarnes C (2013) δ13C and δ2H measurement of methane from ecological and geological sources by gas chromatography/combustion/pyrolysis isotope-ratio mass spectrometry. Rapid Commun Mass Sp 27:1036–1044. doi:10.1002/rcm.6549
US EPA.2008.A guide for assessing biodegradation and source identification
Eiler JM (2013) The isotopic anatomies of molecules and minerals. Annu Rev Earth Pl Sci 41:411–441. doi:10.1146/annurev-earth-042711-105348
Galimov E (ed) (2012) The biological fractionation of isotopes. Elsevier, Amsterdam
Vogt C, Dorer C, Musat F, Richnow HH (2016) Multi-element isotope fractionation concepts to characterize the biodegradation of hydrocarbons—from enzymes to the environment. Curr Opin Biotechnol 41:90–98. doi:10.1016/j.copbio.2016.04.027
Lord Rayleigh (1902) LIX. On the distillation of binary mixtures. Lond Edinb Dublin Philos Mag J Sci 4:521–537. doi:10.1080/1478644020946287
Zhang N, Bashir S, Qin J, Schindelka J, Fischer A, Nijenhuis I, Richnow HH (2014) Compound specific stable isotope analysis (CSIA) to characterize transformation mechanisms of α-hexachlorocyclohexane. J Hazard Mater 280:750–757. doi:10.1016/j.jhazmat.2014.08.046
Bidleman TF, Jantunen LM, Kurt-Karakus PB, Wong F (2012) Chiral persistent organic pollutants as tracers of atmospheric sources and fate: review and prospects for investigating climate change influences. Atmos Pollut Res 3:371–382. doi:10.5094/APR.2012.043
Renpenning J, Hitzfeld KL, Gilevska T, Nijenhuis I, Gehre M, Richnow HH (2015) Development and validation of an universal unterface for compound-specific stable isotope analysis of chlorine (37Cl/35Cl) by GC-High-Temperature Conversion (HTC)-MS/IRMS. Anal Chem 87:2832–2839. doi:10.1021/ac504232u
Gehre M, Renpenning J, Gilevska T, Qi H, Coplen TB, Meijer HAJ, Brand WA, Schimmelmann A (2015) On-line hydrogen-isotope measurements of organic samples using elemental chromium: an extension for high temperature elemental-analyzer techniques. Anal Chem 87:5198–5205. doi:10.1021/acs.analchem.5b00085
Nijenhuis I, Renpenning J, Kümmel S, Richnow HH, Gehre M (2016) Recent advances in multi-element compound-specific stable isotope analysis of organohalides: achievements, challenges and prospects for assessing environmental sources and transformation. Trends Environ Anal Chem 11:1–8. doi:10.1016/j.teac.2016.04.001
Lin Y, Robert NC, Manfred G (2010) Calibration of δ17O and δ18O of international measurement standards–VSMOW, VSMOW2, SLAP, and SLAP2. Rapid Commun Mass Spectrom 24:773–776. doi:10.1002/rcm.4449
Acknowledgements
We acknowledge the financial support of The German Academic Exchange Service (DAAD) and The Department of Science & Technology (DST) in the personal exchange program DAAD project 57035944 and DST project INT/FRG/DAAD/P-231/2013 and also University of Delhi R&D Grant 2015-16. PK gratefully acknowledges University Grants Commission (UGC) for providing research fellowships. This paper was partly written during the visit by RL and HHR under DST-DAAD exchange program to Germany (Helmholtz Zentrum für Umweltforschung-UFZ, Leipzig).
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Kohli, P., Richnow, H.H. & Lal, R. Compound-Specific Stable Isotope Analysis: Implications in Hexachlorocyclohexane in-vitro and Field Assessment. Indian J Microbiol 57, 11–22 (2017). https://doi.org/10.1007/s12088-016-0630-4
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DOI: https://doi.org/10.1007/s12088-016-0630-4