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

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Anaerobic Utilization of Hydrocarbons, Oils, and Lipids

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.

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References

  • 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 12:2783–2796

    PubMed  CAS  Google Scholar 

  • 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 34:892–896

    Article  CAS  Google Scholar 

  • 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 75:4248–4253

    Article  CAS  Google Scholar 

  • 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 Syracuse

    Google Scholar 

  • Atlas RM (1981) Microbial degradation of petroleum hydrocarbons – an environmental perspective. Microbiol Rev 45:180–209

    PubMed  PubMed Central  CAS  Google Scholar 

  • Audi G, Bersillon O, Blachot J, Wapstra AH (2003) The NUBASE evaluation of nuclear and decay properties. Nucl Phys A 729:3–128

    Article  CAS  Google Scholar 

  • Axcell BC, Geary PJ (1975) Purification and some properties of a soluble benzene-oxidizing system from a strain of pseudomonas. Biochem J 146:173–183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biot 74:13–21

    Article  CAS  Google Scholar 

  • Beller HR, Edwards EA (2000) Anaerobic toluene activation by benzylsuccinate synthase in a highly enriched methanogenic culture. Appl Environ Microbiol 66:5503–5505

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beller HR, Spormann AM (1997) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179:670–676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 45:6947–6953

    Article  PubMed  CAS  Google Scholar 

  • 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 238:661–668

    Article  PubMed  CAS  Google Scholar 

  • Bigeleisen J, Wolfsberg M (1958) Theoretical and experimental aspects of isotope effects in chemical kinetics. Adv Chem Phys 1:15–76

    CAS  Google Scholar 

  • Blanksby SJ, Ellison GB (2003) Bond dissociation energies of organic molecules. Acc Chem Res 36:255–263

    Article  PubMed  CAS  Google Scholar 

  • 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 168:493–503

    Article  PubMed  CAS  Google Scholar 

  • 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 16:612–627

    Article  PubMed  CAS  Google Scholar 

  • Bouchard D, Hunkeler D, Hohener P (2008) Carbon isotope fractionation during aerobic biodegradation of n-alkanes and aromatic compounds in unsaturated sand. Org Geochem 39:23–33

    Article  CAS  Google Scholar 

  • Brenna JT, Corso TN, Tobias HJ, Caimi RJ (1997) High-precision continuous-flow isotope ratio mass spectrometry. Mass Spectrom Rev 16:227–258

    Article  PubMed  CAS  Google Scholar 

  • 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.2013.00089

    Article  Google Scholar 

  • 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 171:461–468

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 151:459–462

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Davidova IA, Gieg LM, Duncan KE, Suflita JM (2007) Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME:436–442

    Google Scholar 

  • 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 287:36905–36916

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 48:5788–5797

    Article  PubMed  CAS  Google Scholar 

  • 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 48:9122–9132

    Article  PubMed  CAS  Google Scholar 

  • 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 211:271–281

    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 

  • 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 39:6896–6916

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 464:543–548

    Article  PubMed  CAS  Google Scholar 

  • 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 113:12792–12796

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 75:1173–1184

    Article  CAS  Google Scholar 

  • 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 41:3689–3696

    Article  PubMed  CAS  Google Scholar 

  • 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 42:4356–4363

    Article  PubMed  CAS  Google Scholar 

  • 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 23:2439–2447

    Article  CAS  Google Scholar 

  • 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 41:99–107

    Article  PubMed  CAS  Google Scholar 

  • 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 87:5198–5205

    Article  PubMed  CAS  Google Scholar 

  • Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243

    Article  PubMed  CAS  Google Scholar 

  • Gibson DT, Gschwendt B, Yeh WK, Kobal VM (1973) Initial reactions in the oxidation of ethylbenzene by Pseudomonas putida. Biochemistry 12:1520–1528

    Article  PubMed  CAS  Google Scholar 

  • 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 38:617–631

    Article  PubMed  CAS  Google Scholar 

  • Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241

    Article  PubMed  CAS  Google Scholar 

  • 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 171:5048–5055

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 26:29–44

    Article  PubMed  CAS  Google Scholar 

  • 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 26:45–62

    Article  PubMed  CAS  Google Scholar 

  • 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 1:535–544

    Article  PubMed  CAS  Google Scholar 

  • 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 1:370–376

    Article  PubMed  CAS  Google Scholar 

  • Hopper DJ, Taylor DG (1975) Pathways for the degradation of m-cresol and p-cresol by Pseudomonas putida. J Bacteriol 122:1–6

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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 43–78

    Google Scholar 

  • 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 16:130–140

    Article  PubMed  CAS  Google Scholar 

  • Jeffrey AM, Yeh HJC, Jerina DM, Patel DR, Davey JF, Gibson DT (1973) Initial reactions in the oxidation of naphthalene by Pseudomonas putida. Biochemistry 14:575–584

    Article  Google Scholar 

  • 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.2013.00058

    Article  Google Scholar 

  • Johnson HA, Pelletier DA, Spormann AM (2001) Isolation and characterization of anaerobic ethylbenzene dehydrogenase, a novel Mo-Fe-S enzyme. J Bacteriol 183:4536–4542

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 13:149–154

    Article  PubMed  CAS  Google Scholar 

  • Kaschl A, Vogt C, Uhlig S, Nijenhuis I, Weiss H, Kastner M, Richnow HH (2005) Isotopic fractionation indicates anaerobic monochlorobenzene biodegradation. Environ Toxicol Chem 24:1315–1324

    Article  PubMed  CAS  Google Scholar 

  • Kniemeyer O, Heider J (2001) Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276:21381–21386

    Article  PubMed  CAS  Google Scholar 

  • 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 449:898–901

    Article  PubMed  CAS  Google Scholar 

  • Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process annual review of microbiology. Annu Rev Microbiol 63:311–334

    Article  PubMed  CAS  Google Scholar 

  • 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 39:6052–6062

    Article  PubMed  CAS  Google Scholar 

  • Kopinke FD, Georgi A, Imfeld G, Richnow HH (2017) Isotope fractionation of benzene during partitioning – revisited. Chemosphere 168:508–513

    Article  PubMed  CAS  Google Scholar 

  • 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 426:878–881

    Article  PubMed  CAS  Google Scholar 

  • 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 195:4660–4667

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 50:3091–3100

    Article  PubMed  CAS  Google Scholar 

  • 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 539:396–401

    Article  PubMed  CAS  Google Scholar 

  • 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 68:634–641

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 28:615–628

    Article  PubMed  CAS  Google Scholar 

  • Lewis JC, Coelho PS, Arnold FH (2011) Enzymatic functionalization of carbon-hydrogen bonds. Chem Soc Rev 40:2003–2021

    Article  PubMed  CAS  Google Scholar 

  • Li P, Wang L, Feng L (2013) Characterization of a novel Rieske-type alkane monooxygenase system in Pusillimonas sp. strain T7-7. J Bacteriol 195:1892–1901

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 80:4095–4107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luykx D, Prenafeta-Boldu FX, de Bont JAM (2003) Toluene monooxygenase from the fungus Cladosporium sphaerospermum. Biochem Biophys Res Commun 312(2):373–379

    Article  PubMed  CAS  Google Scholar 

  • 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 178:3695–3700

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 69:191–198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 40:7675–7681

    Article  PubMed  CAS  Google Scholar 

  • 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 42:8290–8296

    Article  PubMed  CAS  Google Scholar 

  • 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 1:409–414

    Article  PubMed  CAS  Google Scholar 

  • 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 26:92–118

    Article  PubMed  CAS  Google Scholar 

  • Melander L, Saunders WH (1980) Reaction rates of isotopic molecules. Wiley, New York

    Google Scholar 

  • 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 67:4842–4849

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 68:5191–5194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 70:2935–2940

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 14:2770–2774

    Article  PubMed  CAS  Google Scholar 

  • 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 172:287–294

    Article  PubMed  Google Scholar 

  • 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 183:752–757

    Article  PubMed  PubMed Central  Google Scholar 

  • Murrell JC, McDonald IR, Gilbert B (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8:221–225

    Article  PubMed  CAS  Google Scholar 

  • 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 11:209–219

    Article  PubMed  CAS  Google Scholar 

  • 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 99:378–382

    Article  PubMed  CAS  Google Scholar 

  • 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 4:296–305

    Article  PubMed  CAS  Google Scholar 

  • 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 26:180–194

    Article  CAS  Google Scholar 

  • Nijenhuis I, Richnow HH (2016) Stable isotope fractionation concepts for characterizing biotransformation of organohalides. Curr Opin Biotechnol 41:108–113

    Article  PubMed  CAS  Google Scholar 

  • Northrop DB (1981) The expression of isotope effects on enzyme-catalyzed reactions. Annu Rev Biochem 50:103–131

    Article  PubMed  CAS  Google Scholar 

  • 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 50:6708–6716

    Article  PubMed  CAS  Google Scholar 

  • 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 189:4729–4738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peters KE, Walters CC, Moldowan JM (2007b) The biomarker guide, vol 2, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 78:103–108

    Article  CAS  Google Scholar 

  • Rabus R, Heider J (1998) Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulfate reducing bacteria. Arch Microbiol 170:377–384

    Article  CAS  Google Scholar 

  • 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 183:1707–1715

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 89:256–264

    Article  CAS  Google Scholar 

  • Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513

    Article  PubMed  CAS  Google Scholar 

  • 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 87:9443–9450

    Article  PubMed  CAS  Google Scholar 

  • Resnick SM, Lee K, Gibson DT (1996) Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Ind Microbiol Biotechnol 17:438–457

    Article  CAS  Google Scholar 

  • 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 65:101–120

    Article  PubMed  CAS  Google Scholar 

  • Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11:2477–2490

    Article  PubMed  CAS  Google Scholar 

  • 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 75:3912–3919

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 186:8044–8057

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schuhle K, Fuchs G (2004) Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic in phenol metabolism in Thauera aromatica. J Bacteriol 186:4556–4567

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 481:98–101

    Article  CAS  Google Scholar 

  • Simon H, Palm D (1966) Isotope effects in organic chemistry and biochemistry. Angew Chem-Int Edit 5:920–933

    Article  CAS  Google Scholar 

  • Söhngen NL (1913) Benzin, Petroleum, Paraffinol und Paraffin als Kohlenstoff- und Energiequellen für Mikroben. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten, Abteilung II 37:595–609

    Google Scholar 

  • 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 80:7592–7603

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swiderek K, Paneth P (2013) Binding isotope effects. Chem Rev 113:7851–7879

    Article  PubMed  CAS  Google Scholar 

  • 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 70:3814–3820

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 158–170

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Thullner M, Fischer A, Richnow HH, Wick LY (2013) Influence of mass transfer on stable isotope fractionation. Appl Microbiol Biotechnol 97:441–452

    Article  PubMed  CAS  Google Scholar 

  • Tissot BP, Welte DH (1984) Petroleum formation and occurrence, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • 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 41:7773–7780

    Article  PubMed  CAS  Google Scholar 

  • 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 42:7786–7792

    Article  PubMed  CAS  Google Scholar 

  • Ullrich R, Hofrichter M (2007) Enzymatic hydroxylation of aromatic compounds. Cell Mol Life Sci 64:271–293

    Article  PubMed  CAS  Google Scholar 

  • 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, Oklahoma

    Google Scholar 

  • Van Hook WA (2011) Isotope effects in chemistry. Nukleonika 56:217–240

    Google Scholar 

  • 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 70:651–665

    Article  CAS  Google Scholar 

  • 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 123–146

    Google Scholar 

  • 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 42:7793–7800

    Article  PubMed  CAS  Google Scholar 

  • Vogt C, Kleinsteuber S, Richnow HH (2011) Anaerobic benzene degradation by bacteria. Microb Biotechnol 4:710–724

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wang WP, Shao ZZ (2013) Enzymes and genes involved in aerobic alkane degradation. Front Microbiol 4:7. https://doi.org/10.3389/fmicb.2013.00116

    Article  Google Scholar 

  • 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 74:6672–6681

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 210:166–173

    Article  PubMed  CAS  Google Scholar 

  • 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 8:941–955

    Article  CAS  Google Scholar 

  • 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 217–273

    Google Scholar 

  • Wiedemeier TH, Rifai HS, Newell CJ, Wilson JT (1999) Natural attenuation of fuels and chlorinated solvents in the subsurface, 1st edn. Wiley, New York

    Book  Google Scholar 

  • Wilkes H, Buckel W, Golding BT, Rabus R (2016) Metabolism of hydrocarbons in n-alkane-utilizing anaerobic bacteria. J Mol Microbiol Biotechnol 26:138–151

    Article  PubMed  CAS  Google Scholar 

  • Wolfsberg M, Van Hook WA, Paneth P, Rebelo LPN (2009) Isotope effects in the chemical, geological, and bio sciences. Springer, Dordrecht

    Google Scholar 

  • Yeh WK, Gibson DT, Liu TN (1977) Toluene dioxygenase – multicomponent enzyme-system. Biochem Biophys Res Commun 78:401–410

    Article  PubMed  CAS  Google Scholar 

  • Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178:1018–1029

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 3:125–135

    Article  CAS  Google Scholar 

  • 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 172:204–212

    Article  PubMed  CAS  Google Scholar 

  • Zhang XM, Young LY (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63:4759–4764

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang T, Tremblay PL, Chaurasia AK, Smith JA, Bain TS, Lovley DR (2013) Anaerobic benzene oxidation via phenol in Geobacter metallireducens. Appl Environ Microbiol 79:7800–7806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 542:484–494

    Article  PubMed  CAS  Google Scholar 

  • 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:e02750-16

    Google Scholar 

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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.

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Vogt, C., Musat, F., Richnow, HH. (2018). Compound-Specific Isotope Analysis for Studying the Biological Degradation of Hydrocarbons. In: Boll, M. (eds) Anaerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-33598-8_18-1

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