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Compound-Specific Isotope Analysis for Studying the Biological Degradation of Hydrocarbons

  • Carsten Vogt
  • Florin Musat
  • Hans-Hermann Richnow
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Compound-specific isotope fractionation analysis (CSIA) has become a promising approach for studying biological degradation of hydrocarbons in the environment. The approach makes use of isotope fractionation processes taking place during enzymatic cleavage of carbon and hydrogen bonds formed by isotopologues due to rate limitations upon the first irreversible step of the reaction mechanism. The magnitude of isotope fractionation is usually expressed by the isotope enrichment factor ε for carbon (εC) and/or hydrogen (εH) using the Rayleigh equation, correlating isotope fractionation with concentration changes of the residual fraction of the substrate. For evaluating the magnitude of biodegradation at environmental sites, εC and/or εH determined from model cultures expressing known biochemical degradation pathways are used. By correlating the magnitude of carbon and hydrogen isotope fractionation (dual or multi-element compound-specific stable isotope analysis (ME-CSIA), resulting in lambda (Λ) values: Λ = Δ(δ2H)/Δ(δ13C) ≈ εHC, distinct (bio)chemical reactions of degradation pathways can be further identified. In this review, we summarize εC, εH, and Λ values of currently known initial enzymatic reaction steps of aerobic and anaerobic hydrocarbon degradation pathways (dioxygenation, monooxygenation, hydroxylation with water, carboxylation, fumarate addition, and reactions by coenzyme M reductase) and discuss the opportunities for using them to identify degradation pathways and to quantify hydrocarbon degradation in environmental studies.

Notes

Acknowledgments

We acknowledge the support by the Helmholtz Centre for Environmental Research – UFZ, the Max Planck Institute for Marine Microbiology, and the Deutsche Forschungsgemeinschaft (DFG) within the framework of the Priority Programme 1319 “Biological transformations of hydrocarbons without oxygen: from the molecular to the global scale,” grants MU 2950/1-1 to F. Musat and RI 903/4-1 & 2 to H.H. Richnow and C. Vogt.

References

  1. Abu Laban N, Selesi D, Rattei T, Tischler P, Meckenstock RU (2010) Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ Microbiol 12:2783–2796PubMedPubMedCentralGoogle Scholar
  2. Ahad JME, Lollar BS, Edwards EA, Slater GF, Sleep BE (2000) Carbon isotope fractionation during anaerobic biodegradation of toluene: Implications for intrinsic bioremediation. Environ Sci Technol 34:892–896CrossRefGoogle Scholar
  3. Ahn YB, Chae JC, Zylstra GJ, Haggblom MM (2009) Degradation of phenol via phenylphosphate and carboxylation to 4-hydroxybenzoate by a newly isolated strain of the sulfate-reducing bacterium Desulfobacterium anilini. Appl Environ Microb 75:4248–4253CrossRefGoogle Scholar
  4. Aronson D, Howard PH (1997) Anaerobic biodegradation of organic chemicals in groundwater: a summary of field and laboratory studies. Environmental Science Center, Syracuse Research Corporation, North SyracuseGoogle Scholar
  5. Atlas RM (1981) Microbial degradation of petroleum hydrocarbons – an environmental perspective. Microbiol Rev 45:180–209PubMedPubMedCentralGoogle Scholar
  6. Audi G, Bersillon O, Blachot J, Wapstra AH (2003) The NUBASE evaluation of nuclear and decay properties. Nucl Phys A 729:3–128CrossRefGoogle Scholar
  7. Axcell BC, Geary PJ (1975) Purification and some properties of a soluble benzene-oxidizing system from a strain of pseudomonas. Biochem J 146:173–183PubMedPubMedCentralCrossRefGoogle Scholar
  8. van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biot 74:13–21CrossRefGoogle Scholar
  9. Beller HR, Edwards EA (2000) Anaerobic toluene activation by benzylsuccinate synthase in a highly enriched methanogenic culture. Appl Environ Microbiol 66:5503–5505PubMedPubMedCentralCrossRefGoogle Scholar
  10. Beller HR, Spormann AM (1997) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179:670–676PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bergmann FD, Abu Laban NMFH, Meyer AH, Elsner M, Meckenstock RU (2011) Dual (C, H) isotope fractionation in anaerobic low molecular weight (poly)aromatic hydrocarbon (PAH) degradation: potential for field studies and mechanistic implications. Environ Sci Technol 45:6947–6953PubMedCrossRefPubMedCentralGoogle Scholar
  12. Biegert T, Fuchs G, Heider F (1996) Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238:661–668PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bigeleisen J, Wolfsberg M (1958) Theoretical and experimental aspects of isotope effects in chemical kinetics. Adv Chem Phys 1:15–76Google Scholar
  14. Blanksby SJ, Ellison GB (2003) Bond dissociation energies of organic molecules. Acc Chem Res 36:255–263PubMedCrossRefPubMedCentralGoogle Scholar
  15. Bodrossy L, Holmes EM, Holmes AJ, Kovacs KL, Murrell JC (1997) Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov. Arch Microbiol 168:493–503PubMedCrossRefPubMedCentralGoogle Scholar
  16. Boll M, Loffler C, Morris BEL, Kung JW (2014) Anaerobic degradation of homocyclic aromatic compounds via arylcarboxyl-coenzyme A esters: organisms, strategies and key enzymes. Environ Microbiol 16:612–627PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bouchard D, Hunkeler D, Hohener P (2008) Carbon isotope fractionation during aerobic biodegradation of n-alkanes and aromatic compounds in unsaturated sand. Org Geochem 39:23–33CrossRefGoogle Scholar
  18. Brenna JT, Corso TN, Tobias HJ, Caimi RJ (1997) High-precision continuous-flow isotope ratio mass spectrometry. Mass Spectrom Rev 16:227–258PubMedCrossRefPubMedCentralGoogle Scholar
  19. Callaghan AV (2013) Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front Microbiol 4:9.  https://doi.org/10.3389/fmicb.2013.00089CrossRefGoogle Scholar
  20. Colby J, Dalton H (1978) Resolution of methane mono-oxygenase of Methylococcus capsulatus Bath into 3 components – purification and properties of component c, a flavoprotein. Biochem J 171:461–468PubMedPubMedCentralCrossRefGoogle Scholar
  21. Colby J, Dalton H, Whittenbury R (1975) An improved assay for bacterial methane mono-oxygenase: some properties of the enzyme from Methylomonas methanica. Biochem J 151:459–462PubMedPubMedCentralCrossRefGoogle Scholar
  22. Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Sp 25:2538–2560CrossRefGoogle Scholar
  23. Davidova IA, Gieg LM, Duncan KE, Suflita JM (2007) Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME:436–442Google Scholar
  24. Dermer J, Fuchs G (2012) Molybdoenzyme that catalyzes the anaerobic hydroxylation of a tertiary carbon atom in the side chain of cholesterol. J Biol Chem 287:36905–36916PubMedPubMedCentralCrossRefGoogle Scholar
  25. Dorer C, Hohener P, Hedwig N, Richnow HH, Vogt C (2014a) Rayleigh-based concept to tackle strong hydrogen fractionation in dual isotope analysis-the example of ethylbenzene degradation by Aromatoleum aromaticum. Environ Sci Technol 48:5788–5797PubMedCrossRefPubMedCentralGoogle Scholar
  26. Dorer C, Vogt C, Kleinsteuber S, Stams AJM, Richnow HH (2014b) Compound-specific isotope analysis as a tool to characterize biodegradation of ethylbenzene. Environ Sci Technol 48:9122–9132PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dorer C, Vogt C, Neu TR, Stryhanyuk H, Richnow HH (2016) Characterization of toluene and ethylbenzene biodegradation under nitrate-, iron(III)- and manganese(IV)-reducing conditions by compound-specific isotope analysis. Environ Pollut 211:271–281PubMedCrossRefPubMedCentralGoogle Scholar
  28. Elsner M (2010) Stable isotope fractionation to investigate natural transformation mechanisms of organic contaminants: principles, prospects and limitations. J Environ Monit 12:2005–2031PubMedCrossRefPubMedCentralGoogle Scholar
  29. Elsner M, Zwank L, Hunkeler D, Schwarzenbach RP (2005) A new concept linking observable stable isotope fractionation to transformation pathways of organic pollutants. Environ Sci Technol 39:6896–6916PubMedCrossRefPubMedCentralGoogle Scholar
  30. 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 403:2471–2491PubMedCrossRefPubMedCentralGoogle Scholar
  31. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels H, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, den Camp H, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548PubMedCrossRefPubMedCentralGoogle Scholar
  32. Ettwig KF, Zhu BL, Speth D, Keltjens JT, Jetten MSM, Kartal B (2016) Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc Natl Acad Sci U S A 113:12792–12796PubMedPubMedCentralCrossRefGoogle Scholar
  33. Feisthauer S, Vogt C, Modrzynski J, Szlenkier M, Kruger M, Siegert M, Richnow HH (2011) Different types of methane monooxygenases produce similar carbon and hydrogen isotope fractionation patterns during methane oxidation. Geochim Cosmochim Acta 75:1173–1184CrossRefGoogle Scholar
  34. Fischer A, Theuerkorn K, Stelzer N, Gehre M, Thullner M, Richnow HH (2007) Applicability of stable isotope fractionation analysis for the characterization of benzene biodegradation in a BTEX-contaminated aquifer. Environ Sci Technol 41:3689–3696PubMedCrossRefPubMedCentralGoogle Scholar
  35. Fischer A, Herklotz I, Herrmann S, Thullner M, Weelink SAB, Stams AJM, Schlomann M, Richnow HH, Vogt C (2008) Combined carbon and hydrogen isotope fractionation investigations for elucidating benzene biodegradation pathways. Environ Sci Technol 42:4356–4363PubMedCrossRefPubMedCentralGoogle Scholar
  36. Fischer A, Gehre M, Breitfeld J, Richnow HH, Vogt C (2009) Carbon and hydrogen isotope fractionation of benzene during biodegradation under sulfate-reducing conditions: a laboratory to field site approach. Rapid Comm Mass Spec 23:2439–2447CrossRefGoogle Scholar
  37. Fischer A, Manefield M, Bombach P (2016) Application of stable isotope tools for evaluating natural and stimulated biodegradation of organic pollutants in field studies. Curr Opin Biotechnol 41:99–107PubMedCrossRefPubMedCentralGoogle Scholar
  38. Gehre M, Renpenning J, Gilevska T, Qi HP, 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 87:5198–5205PubMedCrossRefPubMedCentralGoogle Scholar
  39. Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243PubMedCrossRefPubMedCentralGoogle Scholar
  40. Gibson DT, Gschwendt B, Yeh WK, Kobal VM (1973) Initial reactions in the oxidation of ethylbenzene by Pseudomonas putida. Biochemistry 12:1520–1528PubMedCrossRefPubMedCentralGoogle Scholar
  41. Griebler C, Safinowski M, Vieth A, Richnow HH, Meckenstock RU (2004) Combined application of stable carbon isotope analysis and specific metabolites determination for assessing in situ degradation of aromatic hydrocarbons in a tar oil-contaminated aquifer. Environ Sci Technol 38:617–631PubMedCrossRefPubMedCentralGoogle Scholar
  42. Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241PubMedCrossRefPubMedCentralGoogle Scholar
  43. Harayama S, Rekik M, Wubbolts M, Rose K, Leppik RA, Timmis KN (1989) Characterization of 5 genes in the upper pathway operon of Tol plasmid PWWO from Pseudomonas putida and identification of the gene products. J Bacteriol 171:5048–5055PubMedPubMedCentralCrossRefGoogle Scholar
  44. Heider J, Szaleniec M, Martins BM, Seyhan D, Buckel W, Golding BT (2016a) Structure and function of benzylsuccinate synthase and related fumarate-adding glycyl radical enzymes. J Mol Microbiol Biotechnol 26:29–44PubMedCrossRefPubMedCentralGoogle Scholar
  45. Heider J, Szaleniec M, Sunwoldt K, Boll M (2016b) Ethylbenzene dehydrogenase and related molybdenum enzymes involved in oxygen-independent alkyl chain hydroxylation. J Mol Microbiol Biotechnol 26:45–62PubMedCrossRefPubMedCentralGoogle Scholar
  46. Herrmann S, Vogt C, Fischer A, Kuppardt A, Richnow HH (2009) Characterization of anaerobic xylene biodegradation by two-dimensional isotope fractionation analysis. Environ Microbiol Rep 1:535–544PubMedCrossRefPubMedCentralGoogle Scholar
  47. Holler T, Wegener G, Knittel K, Boetius A, Brunner B, Kuypers MMM, Widdel F (2009) Substantial 13C/12C and D/H fractionation during anaerobic oxidation of methane by marine consortia enriched in vitro. Environ Microbiol Rep 1:370–376PubMedCrossRefPubMedCentralGoogle Scholar
  48. Hopper DJ, Taylor DG (1975) Pathways for the degradation of m-cresol and p-cresol by Pseudomonas putida. J Bacteriol 122:1–6PubMedPubMedCentralGoogle Scholar
  49. Hunkeler D, Elsner M (2010) Principles and Mechanisms of Isotope Fractionation. In: Aelion CM, Höhener P, Hunkeler D, Aravena R (eds) Environmental isotopes in biodegradation and bioremediation. CRC Press, Taylor & Francis Group, Boca Raton, pp 43–78Google Scholar
  50. Jaekel U, Vogt C, Fischer A, Richnow HH, Musat F (2014) Carbon and hydrogen stable isotope fractionation associated with the anaerobic degradation of propane and butane by marine sulfate-reducing bacteria. Environ Microbiol 16:130–140PubMedCrossRefGoogle Scholar
  51. Jeffrey AM, Yeh HJC, Jerina DM, Patel DR, Davey JF, Gibson DT (1973) Initial reactions in the oxidation of naphthalene by Pseudomonas putida. Biochemistry 14:575–584CrossRefGoogle Scholar
  52. Ji YR, Mao GN, Wang YY, Bartlam M (2013) Structural insights into diversity and n-alkane biodegradation mechanisms of alkane hydroxylases. Front Microbiol 4:13.  https://doi.org/10.3389/fmicb.2013.00058CrossRefGoogle Scholar
  53. Johnson HA, Pelletier DA, Spormann AM (2001) Isolation and characterization of anaerobic ethylbenzene dehydrogenase, a novel Mo-Fe-S enzyme. J Bacteriol 183:4536–4542PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kane SR, Beller HR, Legler TC, Anderson RT (2002) Biochemical and genetic evidence of benzylsuccinate synthase in toluene-degrading, ferric iron-reducing Geobacter metallireducens. Biodegradation 13:149–154PubMedCrossRefPubMedCentralGoogle Scholar
  55. Kaschl A, Vogt C, Uhlig S, Nijenhuis I, Weiss H, Kastner M, Richnow HH (2005) Isotopic fractionation indicates anaerobic monochlorobenzene biodegradation. Environ Toxicol Chem 24:1315–1324PubMedCrossRefPubMedCentralGoogle Scholar
  56. Kniemeyer O, Heider J (2001) Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276:21381–21386PubMedCrossRefPubMedCentralGoogle Scholar
  57. Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye SB, Widdel F (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449:898–901PubMedCrossRefPubMedCentralGoogle Scholar
  58. Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process annual review of microbiology. Annu Rev Microbiol 63:311–334PubMedCrossRefPubMedCentralGoogle Scholar
  59. Kopinke FD, Georgi A, Voskamp M, Richnow HH (2005) Carbon isotope fractionation of organic contaminants due to retardation on humic substances: Implications for natural attenuation studies in aquifers. Environ Sci Technol 39:6052–6062PubMedCrossRefPubMedCentralGoogle Scholar
  60. Kopinke FD, Georgi A, Imfeld G, Richnow HH (2017) Isotope fractionation of benzene during partitioning – revisited. Chemosphere 168:508–513PubMedCrossRefPubMedCentralGoogle Scholar
  61. Krüger M, Meyerdierks A, Glöckner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt J, Böcher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426:878–881PubMedCrossRefPubMedCentralGoogle Scholar
  62. Kümmel S, Kuntze K, Vogt C, Boll M, Heider J, Richnow HH (2013) Evidence for benzylsuccinate synthase subtypes obtained by using stable isotope tools. J Bacteriol 195:4660–4667PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kümmel S, Starke R, Chen G, Musat F, Richnow HH, Vogt C (2016) Hydrogen isotope fractionation as a tool to identify aerobic and anaerobic PAH biodegradation. Environ Sci Technol 50:3091–3100PubMedCrossRefPubMedCentralGoogle Scholar
  64. Laso-Perez R, Wegener G, Knittel K, Widdel F, Harding KJ, Krukenberg V, Meier DV, Richter M, Tegetmeyer HE, Riedel D, Richnow HH, Adrian L, Reemtsma T, Lechtenfeld OJ, Musat F (2016) Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature 539:396–401PubMedCrossRefPubMedCentralGoogle Scholar
  65. Lessner DJ, Johnson GR, Parales RE, Spain JC, Gibson DT (2002) Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765. Appl Environ Microbiol 68:634–641PubMedPubMedCentralCrossRefGoogle Scholar
  66. Leuthner B, Leutwein C, Schulz H, Horth P, Haehnel W, Schiltz E, Schagger H, Heider J (1998) Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol Microbiol 28:615–628PubMedCrossRefGoogle Scholar
  67. Lewis JC, Coelho PS, Arnold FH (2011) Enzymatic functionalization of carbon-hydrogen bonds. Chem Soc Rev 40:2003–2021PubMedCrossRefGoogle Scholar
  68. Li P, Wang L, Feng L (2013) Characterization of a novel Rieske-type alkane monooxygenase system in Pusillimonas sp. strain T7-7. J Bacteriol 195:1892–1901PubMedPubMedCentralCrossRefGoogle Scholar
  69. Luo F, Gitiafroz R, Devine CE, Gong YC, Hug LA, Raskin L, Edwards EA (2014) Metatranscriptome of an anaerobic benzene-degrading, nitrate-reducing enrichment culture reveals involvement of carboxylation in benzene ring activation. Appl Environ Microbiol 80:4095–4107PubMedPubMedCentralCrossRefGoogle Scholar
  70. Luykx D, Prenafeta-Boldu FX, de Bont JAM (2003) Toluene monooxygenase from the fungus Cladosporium sphaerospermum. Biochem Biophys Res Commun 312(2):373–379PubMedCrossRefPubMedCentralGoogle Scholar
  71. Maeng JH, Sakai Y, Tani Y, Kato N (1996) Isolation and characterization of a novel oxygenase that catalyzes the first step of n-alkane oxidation in Acinetobacter sp. strain M-1. J Bacteriol 178:3695–3700PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mancini SA, Ulrich AC, Lacrampe-Couloume G, Sleep B, Edwards EA, Lollar BS (2003) Carbon and hydrogen isotopic fractionation during anaerobic biodegradation of benzene. Appl Environ Microbiol 69:191–198PubMedPubMedCentralCrossRefGoogle Scholar
  73. Mancini SA, Hirschorn SK, Elsner M, Lacrampe-Couloume G, Sleep BE, Edwards EA, Lollar BS (2006) Effects of trace element concentration on enzyme controlled stable isotope fractionation during aerobic biodegradation of toluene. Environ Sci Technol 40:7675–7681PubMedCrossRefPubMedCentralGoogle Scholar
  74. Mancini SA, Devine CE, Elsner M, Nandi ME, Ulrich AC, Edwards EA, Lollar BS (2008) Isotopic evidence suggests different initial reaction mechanisms for anaerobic benzene biodegradation. Environ Sci Technol 42:8290–8296PubMedCrossRefGoogle Scholar
  75. Meckenstock RU, Morasch B, Warthmann R, Schink B, Annweiler E, Michaelis W, Richnow HH (1999) C-13/C-12 isotope fractionation of aromatic hydrocarbons during microbial degradation. Environ Microbiol 1:409–414PubMedCrossRefGoogle Scholar
  76. Meckenstock RU, Boll M, Mouttaki H, Koelschbach JS, Tarouco PC, Weyrauch P, Dong XY, Himmelberg AM (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microbiol Biotechnol 26:92–118PubMedCrossRefGoogle Scholar
  77. Melander L, Saunders WH (1980) Reaction rates of isotopic molecules. Wiley, New YorkGoogle Scholar
  78. Morasch B, Richnow HH, Schink B, Meckenstock RU (2001) Stable hydrogen and carbon isotope fractionation during microbial toluene degradation: Mechanistic and environmental aspects. Appl Environ Microbiol 67:4842–4849PubMedPubMedCentralCrossRefGoogle Scholar
  79. Morasch B, Richnow HH, Schink B, Vieth A, Meckenstock RU (2002) Carbon and hydrogen stable isotope fractionation during aerobic bacterial degradation of aromatic hydrocarbons. Appl Environ Microbiol 68:5191–5194PubMedPubMedCentralCrossRefGoogle Scholar
  80. Morasch B, Richnow HH, Vieth A, Schink B, Meckenstock RU (2004) Stable isotope fractionation caused by glycyl radical enzymes during bacterial degradation of aromatic compounds. Appl Environ Microbiol 70:2935–2940PubMedPubMedCentralCrossRefGoogle Scholar
  81. Mouttaki H, Johannes J, Meckenstock RU (2012) Identification of naphthalene carboxylase as a prototype for the anaerobic activation of non-substituted aromatic hydrocarbons. Environ Microbiol 14:2770–2774PubMedCrossRefPubMedCentralGoogle Scholar
  82. Müller JA, Galushko AS, Kappler A, Schink B (1999) Anaerobic degradation of m-cresol by Desulfobacterium cetonicum is initiated by formation of 3-hydroxybenzylsuccinate. Arch Microbiol 172:287–294PubMedCrossRefPubMedCentralGoogle Scholar
  83. Müller JA, Galushko AS, Kappler A, Schink B (2001) Initiation of anaerobic degradation of p-cresol by formation of 4-hydroxybenzylsuccinate in Desulfobacterium cetonicum. J Bacteriol 183:752–757PubMedPubMedCentralCrossRefGoogle Scholar
  84. Murrell JC, McDonald IR, Gilbert B (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8:221–225PubMedCrossRefPubMedCentralGoogle Scholar
  85. Musat F, Galushko A, Jacob J, Widdel F, Kube M, Reinhardt R, Wilkes H, Schink B, Rabus R (2009) Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environ Microbiol 11:209–219PubMedCrossRefPubMedCentralGoogle Scholar
  86. Na KS, Kuroda A, Takiguchi N, Ikeda T, Ohtake H, Kato J (2005) Isolation and characterization of benzene-tolerant Rhodococcus opacus strains. J Biosci Bioeng 99:378–382PubMedCrossRefPubMedCentralGoogle Scholar
  87. Nauhaus K, Boetius A, Krüger M, Widdel F (2002) In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol 4:296–305PubMedCrossRefPubMedCentralGoogle Scholar
  88. von Netzer F, Kuntze K, Vogt C, Richnow HH, Boll M, Lueders T (2016) Functional gene markers for fumarate-adding and dearomatizing key enzymes in anaerobic aromatic hydrocarbon degradation in terrestrial environments. J Mol Microbiol Biotechnol 26:180–194CrossRefGoogle Scholar
  89. Nijenhuis I, Richnow HH (2016) Stable isotope fractionation concepts for characterizing biotransformation of organohalides. Curr Opin Biotechnol 41:108–113PubMedCrossRefPubMedCentralGoogle Scholar
  90. Northrop DB (1981) The expression of isotope effects on enzyme-catalyzed reactions. Annu Rev Biochem 50:103–131PubMedCrossRefPubMedCentralGoogle Scholar
  91. Pati SG, Kohler HPE, Pabis A, Paneth P, Parales RE, Hofstetter TB (2016) Substrate and enzyme specificity of the kinetic isotope effects associated with the dioxygenation of nitroaromatic contaminants. Environ Sci Technol 50:6708–6716PubMedCrossRefPubMedCentralGoogle Scholar
  92. Peters F, Heintz D, Johannes J, van Dorsselaer A, Boll M (2007a) Genes, enzymes, and regulation of para-cresol metabolism in Geobacter metallireducens. J Bacteriol 189:4729–4738PubMedPubMedCentralCrossRefGoogle Scholar
  93. Peters KE, Walters CC, Moldowan JM (2007b) The biomarker guide, vol 2, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  94. Pilkington SJ, Dalton H (1991) Purification and characterization of the soluble methane monooxygenase from Methylosinus sporium-5 demonstrates the highly conserved nature of this enzyme in methanotrophs. FEMS Microbiol Lett 78:103–108CrossRefGoogle Scholar
  95. Rabus R, Heider J (1998) Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulfate reducing bacteria. Arch Microbiol 170:377–384CrossRefGoogle Scholar
  96. Rabus R, Wilkes H, Behrends A, Armstroff A, Fischer T, Pierik AJ, Widdel F (2001) Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol 183:1707–1715PubMedPubMedCentralCrossRefGoogle Scholar
  97. Rasigraf O, Vogt C, Richnow HH, Jetten MSM, Ettwig KF (2012) Carbon and hydrogen isotope fractionation during nitrite-dependent anaerobic methane oxidation by Methylomirabilis oxyfera. Geochim Cosmochim Acta 89:256–264CrossRefGoogle Scholar
  98. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513PubMedCrossRefPubMedCentralGoogle Scholar
  99. Renpenning J, Kummel S, Hitzfeld KL, Schimmelmann A, Gehre M (2015) Compound-specific hydrogen isotope analysis of heteroatom-bearing compounds via gas chromatography-chromium-based high-temperature conversion (Cr/HTC)-isotope ratio mass spectrometry. Anal Chem 87:9443–9450PubMedCrossRefPubMedCentralGoogle Scholar
  100. Resnick SM, Lee K, Gibson DT (1996) Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Ind Microbiol Biotechnol 17:438–457CrossRefGoogle Scholar
  101. Richnow HH, Annweiler E, Michaelis W, Meckenstock RU (2003) Microbial in situ degradation of aromatic hydrocarbons in a contaminated aquifer monitored by carbon isotope fractionation. J Contam Hydrol 65:101–120PubMedCrossRefPubMedCentralGoogle Scholar
  102. Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11:2477–2490PubMedCrossRefPubMedCentralGoogle Scholar
  103. Schleinitz KM, Schmeling S, Jehmlich N, von Bergen M, Harms H, Kleinsteuber S, Vogt C, Fuchs G (2009) Phenol degradation in the strictly anaerobic iron-reducing bacterium Geobacter metallireducens GS-15. Appl Environ Microbiol 75:3912–3919PubMedPubMedCentralCrossRefGoogle Scholar
  104. Schmeling S, Narmandakh A, Schmitt O, Gad'on N, Schuhle K, Fuchs G (2004) Phenylphosphate synthase: a new phosphotransferase catalyzing the first step in anaerobic phenol metabolism in Thauera aromatica. J Bacteriol 186:8044–8057PubMedPubMedCentralCrossRefGoogle Scholar
  105. Schuhle K, Fuchs G (2004) Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic in phenol metabolism in Thauera aromatica. J Bacteriol 186:4556–4567PubMedPubMedCentralCrossRefGoogle Scholar
  106. Shima S, Krueger M, Weinert T, Demmer U, Kahnt J, Thauer RK, Ermler U (2012) Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically. Nature 481:98–101CrossRefGoogle Scholar
  107. Simon H, Palm D (1966) Isotope effects in organic chemistry and biochemistry. Angew Chem-Int Edit 5:920–933CrossRefGoogle Scholar
  108. Söhngen NL (1913) Benzin, Petroleum, Paraffinol und Paraffin als Kohlenstoff- und Energiequellen für Mikroben. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten, Abteilung II 37:595–609Google Scholar
  109. Strijkstra A, Trautwein K, Jarling R, Wohlbrand L, Dorries M, Reinhardt R, Drozdowska M, Golding BT, Wilkes H, Rabus R (2014) Anaerobic activation of p-cymene in denitrifying betaproteobacteria: methyl group hydroxylation versus addition to fumarate. Appl Environ Microbiol 80:7592–7603PubMedPubMedCentralCrossRefGoogle Scholar
  110. Swiderek K, Paneth P (2013) Binding isotope effects. Chem Rev 113:7851–7879PubMedCrossRefPubMedCentralGoogle Scholar
  111. Tao Y, Fishman A, Bentley WE, Wood TK (2004) Oxidation of benzene to phenol, catechol, and 1,2,3-trihydroxybenzene by toluene 4-monooxygenase of Pseudomonas mendocina KR1 and toluene 3-monooxygenase of Ralstonia pickettii PKO1. Appl Environ Microbiol 70:3814–3820PubMedPubMedCentralCrossRefGoogle Scholar
  112. Thauer RK, Shima S (2008) Methane as fuel for anaerobic microorganisms. In: Wiegel J, Maier RJ, Adams MWW (eds) Incredible anaerobes: from physiology to genomics to fuels. Annals of the New York Academy of Sciences, vol 1125. Blackwell Publishing, Oxford, pp 158–170Google Scholar
  113. 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 42:1440–1460CrossRefGoogle Scholar
  114. Thullner M, Fischer A, Richnow HH, Wick LY (2013) Influence of mass transfer on stable isotope fractionation. Appl Microbiol Biotechnol 97:441–452PubMedCrossRefPubMedCentralGoogle Scholar
  115. Tissot BP, Welte DH (1984) Petroleum formation and occurrence, 2nd edn. Springer, BerlinCrossRefGoogle Scholar
  116. Tobler NB, Hofstetter TB, Schwarzenbach RP (2007) Assessing iron-mediated oxidation of toluene and reduction of nitroaromatic contaminants in anoxic environments using compound-specific isotope analysis. Environ Sci Technol 41:7773–7780PubMedCrossRefGoogle Scholar
  117. Tobler NB, Hofstetter TB, Schwarzenbach RP (2008) Carbon and hydrogen isotope fractionation during anaerobic toluene oxidation by Geobacter metallireducens with different Fe(III) phases as terminal electron acceptors. Environ Sci Technol 42:7786–7792PubMedCrossRefPubMedCentralGoogle Scholar
  118. Ullrich R, Hofrichter M (2007) Enzymatic hydroxylation of aromatic compounds. Cell Mol Life Sci 64:271–293PubMedCrossRefPubMedCentralGoogle Scholar
  119. US-EPA (2008) A guide for assessing biodegradation and source identification of organic ground water contaminants using compound specific isotope analysis (CSIA). Office of Research and Development, OklahomaGoogle Scholar
  120. Van Hook WA (2011) Isotope effects in chemistry. Nukleonika 56:217–240Google Scholar
  121. Vieth A, Wilkes H (2006) Deciphering biodegradation effects on light hydrocarbons in crude oils using their stable carbon isotopic composition: a case study from the Gullfaks oil field, offshore Norway. Geochim Cosmochim Acta 70:651–665CrossRefGoogle Scholar
  122. Vogt C, Richnow HH (2014) Bioremediation via in situ microbial degradation of organic pollutants. In: Schippers A, Glombitza F, Sand W (eds) Geobiotechnology II: energy resources, subsurface technologies, organic pollutants and mining legal principles. Advances in biochemical engineering-biotechnology, vol 142. Springer-Verlag Berlin, Berlin, pp 123–146Google Scholar
  123. Vogt C, Cyrus E, Herklotz I, Schlosser D, Bahr A, Herrmann S, Richnow HH, Fischer A (2008) Evaluation of toluene degradation pathways by two-dimensional stable isotope fractionation. Environ Sci Technol 42:7793–7800PubMedCrossRefPubMedCentralGoogle Scholar
  124. Vogt C, Kleinsteuber S, Richnow HH (2011) Anaerobic benzene degradation by bacteria. Microb Biotechnol 4:710–724PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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 41:90–98PubMedCrossRefPubMedCentralGoogle Scholar
  126. Wang WP, Shao ZZ (2013) Enzymes and genes involved in aerobic alkane degradation. Front Microbiol 4:7.  https://doi.org/10.3389/fmicb.2013.00116CrossRefGoogle Scholar
  127. Weelink SAB, Tan NCG, ten Broeke H, van den Kieboom C, van Doesburg W, Langenhoff AAM, Gerritse J, Junca H, Stams AJM (2008) Isolation and characterization of Alicycliphilus denitrificans strain BC, which grows on benzene with chlorate as the electron acceptor. Appl Environ Microbiol 74:6672–6681PubMedPubMedCentralCrossRefGoogle Scholar
  128. Wei X, Gilevska T, Wetzig F, Dorer C, Richnow HH, Vogt C (2016) Characterization of phenol and cresol biodegradation by compound-specific stable isotope analysis. Environ Pollut 210:166–173PubMedCrossRefPubMedCentralGoogle Scholar
  129. Welte CU, Rasigraf O, Vaksmaa A, Versantvoort W, Arshad A, Op den Camp HJM, Jetten MSM, Luke C, Reimann J (2016) Nitrate- and nitrite-dependent anaerobic oxidation of methane. Env Microbiol Rep 8:941–955CrossRefGoogle Scholar
  130. Westaway KC (2006) Using kinetic isotope effects to determine the structure of the transition states of S(N)2 reactions. In: Advances in physical organic chemistry, vol 41. Academic Press Ltd-Elsevier Science Ltd, London, pp 217–273Google Scholar
  131. Wiedemeier TH, Rifai HS, Newell CJ, Wilson JT (1999) Natural attenuation of fuels and chlorinated solvents in the subsurface, 1st edn. Wiley, New YorkCrossRefGoogle Scholar
  132. Wilkes H, Buckel W, Golding BT, Rabus R (2016) Metabolism of hydrocarbons in n-alkane-utilizing anaerobic bacteria. J Mol Microbiol Biotechnol 26:138–151PubMedCrossRefPubMedCentralGoogle Scholar
  133. Wolfsberg M, Van Hook WA, Paneth P, Rebelo LPN (2009) Isotope effects in the chemical, geological, and bio sciences. Springer, DordrechtGoogle Scholar
  134. Yeh WK, Gibson DT, Liu TN (1977) Toluene dioxygenase – multicomponent enzyme-system. Biochem Biophys Res Commun 78:401–410PubMedCrossRefPubMedCentralGoogle Scholar
  135. Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178:1018–1029PubMedPubMedCentralCrossRefGoogle Scholar
  136. Zedelius J, Rabus R, Grundmann O, Werner I, Brodkorb D, Schreiber F, Ehrenreich P, Behrends A, Wilkes H, Kube M, Reinhardt R, Widdel F (2011) Alkane degradation under anoxic conditions by a nitrate-reducing bacterium with possible involvement of the electron acceptor in substrate activation. Env Microbiol Rep 3:125–135CrossRefGoogle Scholar
  137. Zengler K, Heider J, Rossello-Mora R, Widdel F (1999) Phototrophic utilization of toluene under anoxic conditions by a new strain of Blastochloris sulfoviridis. Arch Microbiol 172:204–212PubMedCrossRefPubMedCentralGoogle Scholar
  138. Zhang XM, Young LY (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63:4759–4764PubMedPubMedCentralGoogle Scholar
  139. Zhang T, Tremblay PL, Chaurasia AK, Smith JA, Bain TS, Lovley DR (2013) Anaerobic benzene oxidation via phenol in Geobacter metallireducens. Appl Environ Microbiol 79:7800–7806PubMedPubMedCentralCrossRefGoogle Scholar
  140. Zhang N, Geronimo I, Paneth P, Schindelka J, Schaefer T, Herrmann H, Vogt C, Richnow HH (2016) Analyzing sites of OH radical attack (ring vs. side chain) in oxidation of substituted benzenes via dual stable isotope analysis (delta(13)C and delta(2)H). Sci Total Environ 542:484–494PubMedCrossRefPubMedCentralGoogle Scholar
  141. Zhu B, Bradford L, Huang S, Szalay A, Leix C, Weissbach M, Tancsics A, Drewes JE, Lueders T (2017) Unexpected diversity and high abundance of putative nitric oxide dismutase (Nod) genes in contaminated aquifers and wastewater treatment systems. Appl Environ Microbiol 83:e02750-16Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Carsten Vogt
    • 1
  • Florin Musat
    • 1
  • Hans-Hermann Richnow
    • 1
  1. 1.Department of Isotope BiogeochemistryHelmholtz Centre for Environmental Research – UFZLeipzigGermany

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