Skip to main content

Abstract

The biodegradation of hydrocarbons under anaerobic conditions is a significant process that is now known to occur in diverse environments. Understanding this process has important implications for the bioremediation of hydrocarbon-contaminated terrestrial and marine environments, for enhanced energy recovery from deep subsurface fossil energy reservoirs, and for climate change effects related to the release of methane and other hydrocarbons from natural seeps and hydrothermal vents. While much understanding of anaerobic hydrocarbon metabolism has been gleaned from cultivation-based studies, cultivation-independent meta-omics approaches such as metagenomics can offer new insights into the process in more complex, natural hydrocarbon-containing environments. Further, a metabolomic approach that seeks specific metabolites diagnostic of anaerobic hydrocarbon biodegradation can provide the “ultimate proof” that this process is occurring in situ. This chapter highlights the key pathways of anaerobic hydrocarbon metabolism and summarizes metagenomic information garnered to date from sequencing hydrocarbon degraders, enrichment cultures, and diverse hydrocarbon-containing environmental samples. Further, a brief overview of hydrocarbon metabolomics is presented, along with research needs on this topic.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Abbai NS, Pillay B (2013) Analysis of hydrocarbon-contaminated groundwater metagenomes as revealed by high-throughput sequencing. Mol Biotechnol 54:900–912

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Abu Laban N, Dao A, Semple K, Foght J (2015) Biodegradation of C7 and C8 iso-alkanes under methanogenic conditions. Environ Microbiol 17:4898–4915

    Article  CAS  PubMed  Google Scholar 

  • Aeckersberg F, Rainey FA, Widdel F (1998) Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch Microbiol 170:361–369

    Article  CAS  PubMed  Google Scholar 

  • Agrawal A, Gieg LM (2013) In situ detection of anaerobic alkane metabolites in subsurface environments. Front Microbiol 4:140

    Article  PubMed  PubMed Central  Google Scholar 

  • Aklujkar M, Krushkal J, DiBartolo G, Lapidus A, Land ML, Lovley DR (2009) The genome sequence of Geobacter metallireducens: features of metabolism, physiology and regulation common and dissimilar to Geobacter sulfurreducens. BMC Microbiol 9:109. doi:10.1186/1471-2180-9-109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • An D, Brown D, Chatterjee I, Dong X, Ramos-Padron E, Wilson S, Bordenave S, Caffrey SM, Gieg LM, Sensen CW, Voordouw G (2013a) Microbial community and potential functional gene diversity involved in anaerobic hydrocarbon degradation and methanogenesis in an oil sands tailings pond. Genome 56:612–618

    Article  CAS  PubMed  Google Scholar 

  • An D, Caffrey SM, Soh J, Agrawal A, Brown D, Budwill K, Dong X, Dunfield PF, Foght J, Gieg LM, Hallam SJ, Hanson NW, He Z, Jack TR, Klassen J, Konwar KM, Kuatsjah E, Li C, Larter S, Leopatra V, Nesbø CL, Oldenburg T, Pagé AP, Ramos-Padron E, Rochman FF, Saidi-Mehrabad A, Sensen CW, Sipahimalani P, Song YC, Wilson S, Wolbring G, Wong ML, Voordouw G (2013b) Metagenomics of hydrocarbon resource environments indicates aerobic taxa and genes to be unexpectedly common. Environ Sci Technol 47:10708–10717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U, Brodie EL, Williams KH, Hubbard SS, Banfield JF (2016) Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun 7:13219. doi:10.1038/ncomms13219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson I, Risso C, Holmes D, Lucas S, Copeland A, Lapidus A, Cheng JF, Bruce D, Goodwin L, Pitluck S, Saunders E, Brettin T, Detter JC, Han C, Tapia R, Larimer F, Land M, Hauser L, Woyke T, Lovley D, Kyrpides N, Ivanova N (2011) Complete genome sequence of Ferroglobus placidus AEDII12DO. Stand Genomic Sci 5:50–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Assinder SJ, Williams PA (1990) The TOL plasmids: determinants of the catabolism of toluene and the xylenes. Adv Microb Physiol 31:1–69

    Article  CAS  PubMed  Google Scholar 

  • Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351

    Article  PubMed  CAS  Google Scholar 

  • Beller HR (2000) Metabolic indicators for detecting in situ anaerobic alkylbenzene degradation. Biodegradation 11:125–139

    Article  CAS  PubMed  Google Scholar 

  • Beller HR, Ding WH, Reinhard M (1995) Byproducts of anaerobic alkylbenzene metabolism useful as indicators of in situ bioremediation. Environ Sci Technol 29:2864–2870

    Article  CAS  PubMed  Google Scholar 

  • Beller HR, Kane SR, Legler TC, Alvarez PJ (2002) A real-time polymerase chain reaction method for monitoring anaerobic, hydrocarbon-degrading bacteria based on a catabolic gene. Environ Sci Technol 36:3977–3984

    Article  CAS  PubMed  Google Scholar 

  • Beller HR, Kane SR, Legler TC, McKelvie JR, Lollar BS, Pearson F, Balser L, Mackay DM (2008) Comparative assessments of benzene, toluene, and xylene natural attenuation by quantitative polymerase chain reaction analysis of a catabolic gene, signature metabolites, and compound-specific isotope analysis. Environ Sci Technol 42:6065–6072

    Article  CAS  PubMed  Google Scholar 

  • Bergmann F, Selesi D, Weinmaier T, Tischler P, Rattei T, Meckenstock RU (2011) Genomic insights into the metabolic potential of the polycyclic aromatic hydrocarbon degrading sulfate-reducing Deltaproteobacterium N47. Environ Microbiol 13:1125–1137

    Article  CAS  PubMed  Google Scholar 

  • Bian XY, Mbadinga SM, Liu YF, Yang SZ, Liu JF, Ye RQ, Gu JD, Mu BZ (2015) Insights into the anaerobic biodegradation pathway of n-alkanes in oil reservoirs by detection of signature metabolites. Sci Rep 5:9801. doi:10.1038/srep09801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boetius A, Wenzhöfer F (2013) Seafloor oxygen consumption fuelled by methane from cold seeps. Nat Geosci 6:725–734

    Article  CAS  Google Scholar 

  • Bombach P, Richnow HH, Kästner M, Fischer A (2010) Current approaches for the assessment of in situ biodegradation. Appl Microbiol Biotechnol 86:839–852

    Article  CAS  PubMed  Google Scholar 

  • Bozinovski D, Herrmann S, Richnow H-H, von Bergen M, Seifert J, Vogt C (2012) Functional analysis of an anaerobic m-xylene-degrading enrichment culture using protein-based stable isotope probing. FEMS Microbiol Ecol 81:134–144

    Article  CAS  PubMed  Google Scholar 

  • Bozinovski D, Taubert M, Kleinsteuber S, Richnow H-H, von Bergen M, Vogt C, Seifert J (2014) Metaproteogenomic analysis of a sulfate-reducing enrichment culture reveals genomic organization of key enzymes in the m-xylene degradation pathway and metabolic activity of proteobacteria. Syst Appl Microbiol 37:488–501

    Article  CAS  PubMed  Google Scholar 

  • Callaghan AV (2013a) Metabolomic investigations of anaerobic hydrocarbon-impacted environments. Curr Opin Biotechnol 24:506–515

    Article  CAS  PubMed  Google Scholar 

  • Callaghan AV (2013b) Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front Microbiol 4:89. doi:10.3389/fmicb.2013.00089

    Article  PubMed  PubMed Central  Google Scholar 

  • Callaghan AV, Wawrik B, Ní Chadhain SM, Young LY, Zylstra GJ (2008) Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes. Biochem Biophys Res Commun 366:142–148

    Article  CAS  PubMed  Google Scholar 

  • Callaghan AV, Tierney M, Phelps CD, Young LY (2009) Anaerobic biodegradation of n-hexadecane by a nitrate-reducing consortium. Appl Environ Microbiol 75:1339–1344

    Article  CAS  PubMed  Google Scholar 

  • Callaghan AV, Davidova IA, Savage-Ashlock K, Parisi VA, Gieg LM, Suflita JM, Kukor JJ, Wawrik B (2010) Diversity of benzyl- and alkylsuccinate synthase genes in hydrocarbon-impacted environments and enrichment cultures. Environ Sci Technol 44:7287–7294

    Article  CAS  PubMed  Google Scholar 

  • Callaghan A, Morris BE, Pereira IA, McInerney MJ, Austin RN, Groves JT, Kukor JJ, Suflita JM, Young LY, Zylstra GJ, Wawrik B (2012) The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation. Environ Microbiol 14:101–113

    Article  CAS  PubMed  Google Scholar 

  • Chanton J, Zhao T, Rosenheim BE, Joye S, Bosman S, Brunner C, Yeager KM, Diercks AR, Hollander D (2015) Using natural abundance radiocarbon to trace the flux of petrocarbon to the seafloor following the Deepwater Horizon oil spill. Environ Sci Technol 49:847–854

    Article  CAS  PubMed  Google Scholar 

  • Coates JD, Chakraborty R, Lack JG, O'Connor SM, Cole KA, Bender KS, Achenbach LA (2001) Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411:1039–1043

    Article  CAS  PubMed  Google Scholar 

  • Daly RA, Borton MA, Wilkins MJ, Hoyt DW, Kountz DJ, Wolfe RA, Welch SA, Marcus DN, Trexler RV, MacRae JD, Krzycki JA, Cole DR, Mouser PJ, Wrighton KC (2016) Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales. Nat Microbiol 5:16146. doi:10.1038/nmicrobiol.2016.146. [Epub ahead of print]

    Article  CAS  Google Scholar 

  • DiDonato RJ Jr, Young ND, Butler JE, Chin KJ, Hixson KK, Mouser P, Lipton MS, DeBoy R, Methé BA (2010) Genome sequence of the deltaproteobacterial strain NaphS2 and analysis of differential gene expression during anaerobic growth on naphthalene. PLoS One 5:e14072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duncan KE, Gieg LM, Parisi VA, Tanner RS, Tringe SG, Bristow J, Suflita JM (2009) Biocorrosive thermophilic microbial communities in Alaskan North Slope oil facilities. Environ Sci Technol 43:7977–7984

    Article  CAS  PubMed  Google Scholar 

  • Ehrenreich P, Behrends A, Harder J, Widdel F (2000) Anaerobic oxidation of alkanes by newly isolated denitrifying bacteria. Arch Microbiol 173:58–64

    Article  CAS  PubMed  Google Scholar 

  • Elshahed MA, Gieg LM, McInerney MJ, Suflita JM (2001) Signature metabolites attesting to the insitu attenuation of alkylbenzenes in anaerobic environments. Environ Sci Technol 35:682–689

    Article  CAS  PubMed  Google Scholar 

  • Embree M, Nagarajan H, Movahedi N, Chitsaz H, Zengler K (2014) Single-cell genome and metatranscriptome sequencing reveal metabolic interactions of an alkane-degrading methanogenic community. ISME J 8:757–767

    Article  CAS  PubMed  Google Scholar 

  • Embree M, Liu JK, Al-Bassam MM, Zengler K (2015) Networks of energetic and metabolic interactions define dynamics in microbial communities. Proc Natl Acad Sci U S A 112:15450–15455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Essaid HI, Bekins BA, Herkelrath WN, Delin GN (2011) Crude oil at the Bemidji site: 25 years of monitoring, modeling, and understanding. Ground Water 49:706–726

    Article  CAS  PubMed  Google Scholar 

  • Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MS, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548

    Article  CAS  PubMed  Google Scholar 

  • Farwell C, Reddy CM, Peacock E, Nelson RK, Washburn L, Valentine DL (2009) Weathering and the fallout plume of heavy oil from strong petroleum seeps near Coal Oil Point, CA. Environ Sci Technol 43:3542–3548

    Article  CAS  PubMed  Google Scholar 

  • Foght J (2008) Anaerobic biodegradation of aromatic hydrocarbons: pathways and prospects. J Mol Microbiol Biotechnol 15:93–120

    Article  CAS  PubMed  Google Scholar 

  • Fowler SJ, Dong X, Sensen CW, Suflita JM, Gieg LM (2012) Methanogenic toluene metabolism: community structure and intermediates. Environ Microbiol 14:754–764

    Article  CAS  PubMed  Google Scholar 

  • Fowler SJ, Toth CR, Gieg LM (2016) Community structure in methanogenic enrichments provides insight into syntrophic interactions in hydrocarbon-impacted environments. Front Microbiol 7:562. doi:10.3389/fmicb.2016.00562

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9:803–816

    Article  CAS  PubMed  Google Scholar 

  • Galushko A, Minz D, Schink B, Widdel F (1999) Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environ Microbiol 1:415–420

    Article  CAS  PubMed  Google Scholar 

  • Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369. doi:10.3389/fmicb.2016.01369

    PubMed  PubMed Central  Google Scholar 

  • Gieg LM, Suflita JM (2002) Detection of anaerobic metabolites of saturated and aromatic hydrocarbons in petroleum-contaminated aquifers. Environ Sci Technol 36:3755–3762

    Article  CAS  PubMed  Google Scholar 

  • Gieg LM, Toth CRA (2016) Signature metabolite analysis to determine in situ anaerobic hydrocarbon biodegradation. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Submitted 19 Oct 2016

    Google Scholar 

  • Gieg LM, Kolhatkar RV, McInerney MJ, Tanner RS, Harris SH, Sublette KL, Suflita JM (1999) Evidence for intrinsic bioremediation in a gas condensate-contaminated aquifer. Environ Sci Technol 33:2550–2560

    Article  CAS  Google Scholar 

  • Gieg LM, Alumbaugh RE, Field J, Jones J, Istok JD, Suflita JM (2009) Assessing in situ rates of anaerobic hydrocarbon bioremediation. Microb Biotechnol 2:222–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gieg LM, Davidova IA, Duncan KE, Suflita JM (2010) Methanogenesis, sulfate reduction and crude oil biodegradation in hot Alaskan oilfields. Environ Microbiol 12:3074–3086

    Article  CAS  PubMed  Google Scholar 

  • Gieg LM, Fowler SJ, Berdugo-Clavijo C (2014) Syntrophic biodegradation of hydrocarbon contaminants. Curr Opin Biotechnol 27:21–19

    Article  CAS  PubMed  Google Scholar 

  • Gittel A, Donhauser J, Røy H, Girguis PR, Jørgensen BB, Kjeldsen KU (2015) Ubiquitous presence and novel diversity of anaerobic alkane degraders in cold marine sediments. Front Microbiol 6:1414

    Article  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Gründger F, Jiménez N, Thielemann T, Straaten N, Lüders T, Richnow HH, Krüger M (2015) Microbial methane formation in deep aquifers of a coal-bearing sedimentary basin, Germany. Front Microbiol 6:200. doi:10.3389/fmicb.2015.00200

    PubMed  PubMed Central  Google Scholar 

  • Grundmann O, Behrends A, Rabus R, Amann J, Halder T, Heider J, Widdel F (2008) Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium, strain HxN. Environ Microbiol 10:376–385

    Article  CAS  PubMed  Google Scholar 

  • Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, DeLong EF (2004) Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305:1457–1462 

    Google Scholar 

  • Harms G, Rabus R, Widdel F (1999) Anaerobic oxidation of the aromatic plant hydrocarbon p-cymene by newly isolated denitrifying bacteria. Arch Microbiol 172:303–312

    Article  CAS  PubMed  Google Scholar 

  • Håvelsrud OE, Haverkamp TH, Kristensen T, Jakobsen KS, Rike AG (2011) A metagenomic study of methanotrophic microorganisms in Coal Oil Point seep sediments. BMC Microbiol 11:221. doi:10.1186/1471-2180-11-221

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Håvelsrud OE, Haverkamp TH, Kristensen T, Jakobsen KS, Rike AG (2012) Metagenomic and geochemical characterization of pockmarked sediments overlaying the Troll petroleum reservoir in the North Sea. BMC Microbiol 12:203. doi:10.1186/1471-2180-12-203

    Article  PubMed  PubMed Central  Google Scholar 

  • Hawley ER, Malfatti SA, Pagani I, Huntemann M, Chen A, Foster B, Copeland A, del Rio TG, Pati A, Jansson JR, Gilbert JA, Tringe SG, Lorenson TD, Hess M (2014a) Metagenomes from two microbial consortia associated with Santa Barbara seep oil. Mar Genomics 18(Pt B):97–109

    Article  PubMed  Google Scholar 

  • Hawley ER, Piao H, Scott NM, Malfatti S, Pagani I, Huntemann M, Chen A, Glavina Del Rio T, Foster B, Copeland A, Jansson J, Pati A, Tringe S, Gilbert JA, Lorenson TD, Hess M (2014b) Metagenomic analysis of microbial consortium from natural crude oil that seeps into the marine ecosystem offshore Southern California. Stand Genomic Sci 9:1259–1274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N, Jansson JK, Probst A, Borglin SE, Fortney JL, Stringfellow WT, Bill M, Conrad ME, Tom LM, Chavarria KL, Alusi TR, Lamendella R, Joyner DC, Spier C, Baelum J, Auer M, Zemla ML, Chakraborty R, Sonnenthal EL, D'haeseleer P, Holman HY, Osman S, Lu Z, Van Nostrand JD, Deng Y, Zhou J, Mason OU (2010) Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204–208

    Article  CAS  PubMed  Google Scholar 

  • Hazen TC, Prince RC, Mahmoudi N (2016) Marine oil biodegradation. Environ Sci Technol 50:2121–2129

    Article  CAS  PubMed  Google Scholar 

  • He Y, Xiao X, Wang F (2013) Metagenome reveals potential microbial degradation of hydrocarbon coupled with sulfate reduction in an oil-immersed chimney from Guaymas Basin. Front Microbiol 4:148. doi:10.3389/fmicb.2013.00148

    Article  PubMed  PubMed Central  Google Scholar 

  • He Y, Feng X, Fang J, Zhang Y, Xiao X (2015) Metagenome and metatranscriptome revealed a highly active and intensive sulfur cycle in an oil-immersed hydrothermal chimney in Guaymas Basin. Front Microbiol 6:1236. doi:10.3389/fmicb.2015.01236

    PubMed  PubMed Central  Google Scholar 

  • Head IM, Gray ND, Larter SR (2014) Life in the slow lane; biogeochemistry of biodegraded petroleum containing reservoirs and implications for energy recovery and carbon management. Front Microbiol 5:566. doi:10.3389/fmicb.2014.00566

    Article  PubMed  PubMed Central  Google Scholar 

  • Heider J, Schühle K (2013) Anaerobic biodegradation of hydrocarbons including methane. In: Rosenburg E (ed) The prokaryotes – prokaryotic physiology and biochemistry. Springer, Berlin, pp 605–634

    Google Scholar 

  • Holmes DE, Risso C, Smith JA, Lovley DR (2011) Anaerobic oxidation of benzene by the hyperthermophilic archaeon Ferroglobus placidus. Appl Environ Microbiol 77:5926–5933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornafius JS, Quigley D, Luyendk BP (1999) The world’s most spectacular marine hydrocarbon seeps (coal oil point, Santa Barbara Channel, California): quantification of emissions. J Geophys Res 104:703–720

    Article  Google Scholar 

  • Hu P, Tom L, Singh A, Thomas BC, Baker BJ, Piceno YM, Andersen GL, Banfield JF (2016) Genome-resolved metagenomic analysis reveals roles for candidate phyla and other microbial community members in biogeochemical transformations in oil reservoirs. MBio 7:e01669–e01615. doi:10.1128/mBio.01669-15

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiménez N, Richnow HH, Vogt C, Treude T, Krüger M (2016) Methanogenic hydrocarbon degradation: evidence from field and laboratory studies. J Mol Microbiol Biotechnol 26:227–242

    Article  PubMed  CAS  Google Scholar 

  • Jobelius C, Ruth B, Griebler C, Meckenstock RU, Hollender J, Reineke A, Frimmel FH, Zwiener C (2011) Metabolites indicate hot spots of biodegradation and biogeochemical gradients in a high resolution monitoring well. Environ Sci Technol 45:474–481

    Article  CAS  PubMed  Google Scholar 

  • Johnson JM, Wawrik B, Isom C, Boling WB, Callaghan AV (2015) Interrogation of Chesapeake Bay sediment microbial communities for intrinsic alkane-utilizing potential under anaerobic conditions. FEMS Microbiol Ecol 91:114

    Article  CAS  Google Scholar 

  • Joye SB, Teske AP, Kostka JE (2014) Microbial dynamics following the Macondo oil well blowout across Gulf of Mexico environments. Bioscience 64:766–777

    Article  Google Scholar 

  • Keller AH, Schleinitz KM, Starke R, Bertilsson S, Vogt C, Kleinsteuber S (2015) Metagenome-based metabolic reconstruction reveals the ecophysiological function of Epsilonproteobacteria in a hydrocarbon-contaminated sulfidic aquifer. Front Microbiol 6:1396. doi:10.3389/fmicb.2015.01396

    Article  PubMed  PubMed Central  Google Scholar 

  • Khelifi N, Grossi V, Hamdi M, Dolla A, Tholozan JL, Ollivier B, Hirschler-Réa A (2010) Anaerobic oxidation of fatty acids and alkenes by the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus. Appl Environ Microbiol 76:3057–3060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khelifi N, Amin Ali O, Roche P, Grossi V, Brochier-Armanet C, Valette O, Ollivier B, Dolla A, Hirschler-Réa A (2014) Anaerobic oxidation of long-chain n-alkanes by the hyperthermophilic sulfate-reducing archaeon, Archaeoglobus fulgidus. ISME J 8:2153–2166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimes NE, Callaghan AV, Aktas DF, Smith WL, Sunner J, Golding B, Drozdowska M, Hazen TC, Suflita JM, Morris PJ (2013) Metagenomic analysis and metabolite profiling of deep-sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill. Front Microbiol 4:50. doi:10.3389/fmicb.2013.00050

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimes NE, Callaghan AV, Suflita JM, Morris PJ (2014) Microbial transformation of the Deepwater Horizon oil spill – past, present, and future perspectives. Front Microbiol 5:603. doi:10.3389/fmicb.2014.00603

    Article  PubMed  PubMed Central  Google Scholar 

  • King GM, Kostka JE, Hazen TC, Sobecky PA (2015) Microbial responses to the Deepwater Horizon oil spill: from coastal wetlands to the deep sea. Annu Rev Mar Sci 7:377–401

    Article  CAS  Google Scholar 

  • Kleindienst S, Herbst FA, Stagars M, von Netzer F, von Bergen M, Seifert J, Peplies J, Amann R, Musat F, Lueders T, Knittel K (2014) Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J 8:2029–2044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleinsteuber S, Schleinitz KM, Vogt C (2012) Key players and team play: anaerobic microbial communities in hydrocarbon-contaminated aquifers. Appl Microbiol Biotechnol 94:851–873

    Article  CAS  PubMed  Google Scholar 

  • Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, Richardson DL, Kerlavage AR, Graham DE, Kyrpides NC, Fleischmann RD, Quackenbush J, Lee NH, Sutton GG, Gill S, Kirkness EF, Dougherty BA, McKenney K, Adams MD, Loftus B, Peterson S, Reich CI, McNeil LK, Badger JH, Glodek A, Zhou L, Overbeek R, Gocayne JD, Weidman JF, McDonald L, Utterback T, Cotton MD, Spriggs T, Artiach P, Kaine BP, Sykes SM, Sadow PW, D'Andrea KP, Bowman C, Fujii C, Garland SA, Mason TM, Olsen GJ, Fraser CM, Smith HO, Woese CR, Venter JC (1997) The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390:364–370

    Article  CAS  PubMed  Google Scholar 

  • Kniemeyer O, Fischer T, Wilkes H, Glöckner FO, Widdel F (2003) Anaerobic degradation of ethylbenzene by a new type of marine sulfate-reducing bacterium. Appl Environ Microbiol 69:760–768

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Konopka A, Wilkins MJ (2012) Application of meta-transcriptomics and -proteomics to analysis of in situ physiological state. Front Microbiol 3:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Kotlar HK, Lewin A, Johansen J, Throne-Holst M, Haverkamp T, Markussen S, Winnberg A, Ringrose P, Aakvik T, Ryeng E, Jakobsen K, Drabløs F, Valla S (2011) High coverage sequencing of DNA from microorganisms living in an oil reservoir 2.5 kilometres subsurface. Environ Microbiol Rep 3:674–681

    Article  PubMed  Google Scholar 

  • Laso-Pérez 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 O, Musat F (2016) Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature Oct 17. doi: 10.1038/nature20152. [Epub ahead of print]

    Google Scholar 

  • Lawson CE, Strachan CR, Williams DD, Koziel S, Hallam SJ, Budwill K (2015) Patterns of endemism and habitat selection in coalbed microbial communities. Appl Environ Microbiol 81:7924–7937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewin A, Johansen J, Wentzel A, Kotlar HK, Drabløs F, Valla S (2014) The microbial communities in two apparently physically separated deep subsurface oil reservoirs show extensive DNA sequence similarities. Environ Microbiol 16:545–558

    Article  CAS  PubMed  Google Scholar 

  • Li W, Wang L-Y, Duan R-Y, Liu JF, Gu J-D, Mu B-Z (2012) Microbial community characteristics of petroleum reservoir production water amended with n-alkanes and incubated under nitrate-, sulfate-reducing and methanogenic conditions. Int Biodeterior Biodegrad 69:87–96

    Article  CAS  Google Scholar 

  • Li C, Lim KM, Chng KR, Nagarajan N (2016) Predicting microbial interactions through computational approaches. Methods 102:12–19

    Article  CAS  PubMed  Google Scholar 

  • Luo F, Gitiafroz R, Devine CE, Gong Y, 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 

  • Luo F, Devine CE, Edwards EA (2016) Cultivating microbial dark matter in benzene-degrading methanogenic consortia. Environ Microbiol 18:2923–2936

    Article  CAS  PubMed  Google Scholar 

  • Mahajan MC, Phale PS, Vaidyanathan CS (1994) Evidence for the involvement of multiple pathways in the biodegradation of 1- and 2-methylnaphthalene by Pseudomonas putida CSV86. Arch Microbiol 161:425–433

    Article  CAS  PubMed  Google Scholar 

  • Martín-Moldes Z, Zamarro MT, Del Cerro C, Valencia A, Gómez MJ, Arcas A, Udaondo Z, García JL, Nogales J, Carmona M, Díaz E (2015) Whole-genome analysis of Azoarcus sp. strain CIB provides genetic insights to its different lifestyles and predicts novel metabolic features. Syst Appl Microbiol 38:462–471

    Article  PubMed  CAS  Google Scholar 

  • Martus P, Püttman W (2003) Formation of alkylated aromatic acids in groundwater by anaerobic degradation of alkylbenzenes. Sci Total Environ 307:19–33

    Article  CAS  PubMed  Google Scholar 

  • Mason OU, Hazen TC, Borglin S, Chain PS, Dubinsky EA, Fortney JL, Han J, Holman HY, Hultman J, Lamendella R, Mackelprang R, Malfatti S, Tom LM, Tringe SG, Woyke T, Zhou J, Rubin EM, Jansson JK (2012) Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6:1715–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mason OU, Scott NM, Gonzalez A, Robbins-Pianka A, Bælum J, Kimbrel J, Bouskill NJ, Prestat E, Borglin S, Joyner DC, Fortney JL, Jurelevicius D, Stringfellow WT, Alvarez-Cohen L, Hazen TC, Knight R, Gilbert JA, Jansson JK (2014) Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill. ISME J 8:1464–1475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayumi D, Mochimaru H, Tamaki H, Yamamoto K, Yoshioka H, Suzuki Y, Kamagata Y, Sakata S (2016) Methane production for coal by a single methanogen. Science 354:222–225

    Article  CAS  PubMed  Google Scholar 

  • Meckenstock RU, Elsner M, Griebler C, Lueders T, Stumpp C, Aamand J, Agathos SN, Albrechtsen HJ, Bastiaens L, Bjerg PL, Boon N, Dejonghe W, Huang WE, Schmidt SI, Smolders E, Sørensen SR, Springael D, van Breukelen BM (2015) Biodegradation: updating the concepts of control for microbial cleanup in contaminated aquifers. Environ Sci Technol 49:7073–7081

    Article  CAS  PubMed  Google Scholar 

  • Meckenstock RU, Boll M, Mouttaki H, Koelschbach JS, Cunha Tarouco P, Weyrauch P, Dong X, Himmelberg AM (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microbiol Biotechnol 26:92–118

    Article  CAS  PubMed  Google Scholar 

  • Mohan AM, Bibby KJ, Lipus D, Hammack RW, Gregory KB (2014) The functional potential of microbial communities in hydraulic fracturing source water and produced water from natural gas extraction characterized by metagenomic sequencing. PLoS One 9:e107682. doi:10.1371/journal.pone.0107682

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morasch B, Hunkeler D, Zopfi J, Temime B, Höhener P (2011) Intrinsic biodegradation potential of aromatic hydrocarbons in an alluvial aquifer – potentials and limits of signature metabolite analysis and two stable isotope-based techniques. Water Res 45:4459–4469

    Article  CAS  PubMed  Google Scholar 

  • Mouser PJ, Borton M, Darrah TH, Hartsock A, Wrighton KC (2016) Hydraulic fracturing offers view of microbial life in the deep terrestrial subsurface. FEMS Microbiol Ecol. Nov 92: fiw166. doi:10.1093/femsec/fiw166

    PubMed  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  CAS  PubMed  Google Scholar 

  • Musat F (2015) The anaerobic degradation of gaseous, nonmethane alkanes – from in situ processes to microorganisms. Comput Struct Biotechnol J 13:222–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • National Research Council (NRC) (1993) In situ bioremediation: when does it work? National Academy Press, Washington, DC

    Google Scholar 

  • Nie Y, Zhao JY, Tang YQ, Guo P, Yang Y, Wu XL, Zhao F (2016) Species divergence vs. functional convergence characterizes crude oil microbial community assembly. Front Microbiol 7:1254. doi:10.3389/fmicb.2016.01254

    Article  PubMed  PubMed Central  Google Scholar 

  • Oberding L, Gieg LM (2016) Metagenomic analyses reveal that energy transfer gene abundances can predict the syntrophic potential of environmental microbial communities. Microorganisms 4:E5. doi:10.3390/microorganisms4010005

    Article  PubMed  Google Scholar 

  • Oka AR, Phelps CD, Zhu X, Saber DL, Young LY (2011) Dual biomarkers of anaerobic hydrocarbon degradation in historically contaminated groundwater. Environ Sci Technol 45:3407–3414

    Article  CAS  PubMed  Google Scholar 

  • Orcutt B, Samarkin V, Boetius A, Joye S (2008) On the relationship between methane production and oxidation by anaerobic methanotrophic communities from cold seeps of the Gulf of Mexico. Environ Microbiol 10:1108–1117

    Article  CAS  PubMed  Google Scholar 

  • Orem WH, Voytek MA, Jones EJ, Lerch HE, Bates AL, Corum MD, Warwick PD, Clark AC (2010) Organic intermediates in the anaerobic biodegradation of coal to methane under laboratory conditions. Org Geochem 41:997–1000

    Article  CAS  Google Scholar 

  • Orphan VJ, Taylor LT, Hafenbradl D, Delong EF (2000) Culture-dependent and culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl Environ Microbiol 66:700–711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oulas A, Polymenakou PN, Seshadri R, Tripp HJ, Mandalakis M, Paez-Espino AD, Pati A, Chain P, Nomikou P, Carey S, Kilias S, Christakis C, Kotoulas G, Magoulas A, Ivanova NN, Kyrpides NC (2016) Metagenomic investigation of the geologically unique Hellenic Volcanic Arc reveals a distinctive ecosystem with unexpected physiology. Environ Microbiol 18:1122–11236

    Article  CAS  PubMed  Google Scholar 

  • Parisi VA, Brubaker GR, Zenker MJ, Prince RC, Gieg LM, Da Silva ML, Alvarez PJ, Suflita JM (2009) Field metabolomics and laboratory assessments of anaerobic intrinsic bioremediation of hydrocarbons at a petroleum-contaminated site. Microb Biotechnol 2:202–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penner TJ, Foght JM (2010) Mature fine tailings from oil sands processing harbour diverse methanogenic communities. Can J Microbiol 56:459–470

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Wohlfeil E, Arjona-Medina JA, Torreno O, Ulzurrun E, Trelles O (2016) Computational workflow for the fine-grained analysis of metagenomic samples. BMC Genomics 17(Suppl 8):802

    Article  PubMed  PubMed Central  Google Scholar 

  • Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163:96–103

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Nordhaus R, Ludwig W, Widdel F (1993) Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium. Appl Environ Microbiol 59:1444–1451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183:27–36

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, Ermler U, Golding BT, Gunsalus RP, Kroneck PM, Krüger M, Lueders T, Martins BM, Musat F, Richnow HH, Schink B, Seifert J, Szaleniec M, Treude T, Ullmann GM, Vogt C, von Bergen M, Wilkes H (2016) Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol 26:5–28

    Article  CAS  PubMed  Google Scholar 

  • Ramos-Padrón E, Bordenave S, Lin S, Bhaskar IM, Dong X, Sensen CW, Fournier J, Voordouw G, Gieg LM (2011) Carbon and sulfur cycling by microbial communities in a gypsum-treated oil sands tailings pond. Environ Sci Technol 45:439–446

    Article  PubMed  CAS  Google Scholar 

  • Redmond MC, Valentine DL (2012) Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci U S A 109:20292–20297

    Article  CAS  PubMed  Google Scholar 

  • Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 10:2477–2490

    Article  CAS  Google Scholar 

  • Rueter P, Rabus R, Wilkes H, Aeckersberg F, Rainey FA, Jannasch HW, Widdel F (1994) Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 372:455–458

    Article  CAS  PubMed  Google Scholar 

  • Safinowski M, Meckenstock RU (2006) Methylation is the initial reaction in anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Environ Microbiol 8:347–352

    Article  CAS  PubMed  Google Scholar 

  • Salinero KK, Keller K, Feil WS, Feil H, Trong S, Di Bartolo G, Lapidus A (2009) Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genomics 10:351

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Segata N, Boernigen D, Tickle TL, Morgan XC, Garrett WS, Huttenhower C (2013) Computational meta’omics for microbial community studies. Mol Syst Biol 9:666

    Article  PubMed  PubMed Central  Google Scholar 

  • Selesi D, Jehmlich N, von Bergen M, Schmidt F, Rattei T, Tischler P, Lueders T, Meckenstock RU (2010) Combined genomic and proteomic approaches identify gene clusters involved in anaerobic 2-methylnaphthalene degradation in the sulfate-reducing enrichment culture N47. J Bacteriol 192:295–306

    Article  CAS  PubMed  Google Scholar 

  • Siddique T, Fedorak PM, Foght JM (2006) Biodegradation of short-chain n-alkanes in oil sands tailings under methanogenic conditions. Environ Sci Technol 40:5459–5464

    Article  CAS  PubMed  Google Scholar 

  • Siddique T, Fedorak PM, MacKinnon M, Foght JM (2007) Metabolism of BTEX and naphtha compounds to methane in oil sands tailings. Environ Sci Technol 41:2350–2356

    Article  CAS  PubMed  Google Scholar 

  • Sieber JR, McInerney MJ, Gunsalus RP (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429–452

    Article  CAS  PubMed  Google Scholar 

  • Singer E, Bushnell B, Coleman-Derr D, Bowman B, Bowers RM, Levy A, Gies EA, Cheng JF, Copeland A, Klenk HP, Hallam SJ, Hugenholtz P, Tringe SG, Woyke T (2016) High-resolution phylogenetic microbial community profiling. ISME J 10:2020–2032

    Article  PubMed  PubMed Central  Google Scholar 

  • So CM, Young LY (1999) Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl Environ Microbiol 65:2969–2976

    CAS  PubMed  PubMed Central  Google Scholar 

  • So CM, Phelps CD, Young LY (2003) Anaerobic transformation of alkanes to fatty acids by a sulfate-reducing bacterium, strain Hxd3. Appl Environ Microbiol 69:3892–3900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song B, Häggblom MM, Zhou J, Tiedje JM, Palleroni NJ (1999) Taxonomic characterization of denitrifying bacteria that degrade aromatic compounds and description of Azoarcus toluvorans sp. nov. and Azoarcus toluclasticus sp. nov. Int J Syst Bacteriol 49:1129–1140

    Article  CAS  PubMed  Google Scholar 

  • Stagars MH, Ruff SE, Amann R, Knittel K (2016) High diversity of anaerobic alkane-degrading microbial communities in marine seep sediments based on (1-methylalkyl)succinate synthase genes. Front Microbiol 6:1511. doi:10.3389/fmicb.2015.01511

    Article  PubMed  PubMed Central  Google Scholar 

  • Stasik S, Wick LY, Wendt-Potthoff K (2015) Anaerobic BTEX degradation in oil sands tailings ponds: impact of labile organic carbon and sulfate-reducing bacteria. Chemosphere 138:133–139

    Article  CAS  PubMed  Google Scholar 

  • Strąpoć D, Mastalerz M, Dawson K, Macaladay JL, Callaghan AV, Wawrik B et al (2011) Biogeochemistry of microbial coal-bed methane. Annu Rev Earth Planet Sci 39:617–656

    Article  CAS  Google Scholar 

  • Tan B, Dong X, Sensen CW, Foght J (2013) Metagenomic analysis of an anaerobic alkane-degrading microbial culture: potential hydrocarbon-activating pathways and inferred roles of community members. Genome 56:599–611

    Article  CAS  PubMed  Google Scholar 

  • Tan B, Nesbø C, Foght J (2014) Re-analysis of omics data indicates Smithella may degrade alkanes by addition to fumarate under methanogenic conditions. ISME J 8:2353–2356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan B, Fowler SJ, Abu Laban N, Dong X, Sensen CW, Foght J, Gieg LM (2015a) Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples. ISME J 9:2028–2045

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan BF, Semple K, Foght J (2015b) Anaerobic alkane biodegradation by cultures enriched from oil sands tailings ponds involves multiple species capable of fumarate addition. FEMS Microbiol Ecol 91:fiv042

    Article  PubMed  CAS  Google Scholar 

  • Techtmann SM, Hazen TC (2016) Metagenomic applications in environmental monitoring and bioremediation. J Ind Microbiol Biotechnol 43:1345–1354

    Article  CAS  PubMed  Google Scholar 

  • Teske A, Callaghan AV, LaRowe DE (2014) Biosphere frontiers of subsurface life in the sedimented hydrothermal system of Guaymas Basin. Front Microbiol 5:362. doi:10.3389/fmicb.2014.00362

    Article  PubMed  PubMed Central  Google Scholar 

  • Teske A, de Beer D, McKay LJ, Tivey MK, Biddle JF, Hoer D, Lloyd KG, Lever MA, Røy H, Albert DB, Mendlovitz HP, MacGregor BJ (2016) The Guaymas Basin hiking guide to hydrothermal mounds, chimneys, and microbial mats: complex seafloor expressions of subsurface hydrothermal circulation. Front Microbiol 7:75. doi:10.3389/fmicb.2016.00075

    Article  PubMed  PubMed Central  Google Scholar 

  • Ulrich AC, Beller HR, Edwards EA (2005) Metabolites detected during biodegradation of 13C6-benzene in nitrate-reducing and methanogenic enrichment cultures. Environ Sci Technol 39:6681–6691

    Article  CAS  PubMed  Google Scholar 

  • Vergnoux A, Malleret L, Asia L, Doumenq P, Theraulaz F (2011) Impact of forest fires on PAH level and distribution in soils. Environ Res 111:193–198

    Article  CAS  PubMed  Google Scholar 

  • von Netzer F, Pilloni G, Kleindienst S, Krüger M, Knittel K, Gründger F, Lueders T (2013) Enhanced gene detection assays for fumarate-adding enzymes allow uncovering of anaerobic hydrocarbon degraders in terrestrial and marine systems. Appl Environ Microbiol 79:543–552

    Article  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 

  • Wawrik B, Mendivelso M, Parisi VA, Suflita JM, Davidova IA, Marks CR, Van Nostrand JD, Liang Y, Zhou J, Huizinga BJ, Strąpoć D, Callaghan AV (2012) Field and laboratory studies on the bioconversion of coal to methane in the San Juan Basin. FEMS Microbiol Ecol 81:26–42

    Article  CAS  PubMed  Google Scholar 

  • Wawrik B, Marks CR, Davidova IA, McInerney MJ, Pruitt S, Duncan KE, Suflita JM, Callaghan AV (2016) Methanogenic paraffin degradation proceeds via alkane addition to fumarate by ‘Smithella’ spp. mediated by a syntrophic coupling with hydrogenotrophic methanogens. Environ Microbiol 18:2604–2619

    Article  CAS  PubMed  Google Scholar 

  • Weiss JV, Cozzarelli IM (2008) Biodegradation in contaminated aquifers: incorporating microbial/molecular methods. Ground Water 46:305–322

    Article  CAS  PubMed  Google Scholar 

  • Widdel F, Musat F (2010) Diversity and common principles in enzymatic activation of hydrocarbons. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 983–1009

    Google Scholar 

  • Widdel F, Knittel K, Galusko A (2010) Anaerobic hydrocarbon-degrading organisms: an overview. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1997–2021

    Chapter  Google Scholar 

  • Williams RJ, Howe A, Hofmockel KS (2014) Demonstrating microbial co-occurrence pattern analyses within and between ecosystems. Front Microbiol 5:358. doi:10.3389/fmicb.2014.00358

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson SL, Li C, Ramos-Padrón E, Nesbø C, Soh J, Sensen CW, Voordouw G, Foght J, Gieg LM (2016) Oil sands tailings ponds harbour a small core prokaryotic microbiome and diverse accessory communities. J Biotechnol 235:187–196

    Article  CAS  PubMed  Google Scholar 

  • Winderl C, Schaefer S, Lueders T (2007) Detection of anaerobic toluene and hydrocarbon degraders in contaminated aquifers using benzylsuccinate synthase (bssA) genes as a functional marker. Environ Microbiol 9:1035–1046

    Article  CAS  PubMed  Google Scholar 

  • Winderl C, Anneser B, Griebler C, Meckenstock RU, Lueders T (2008) Depth-resolved quantification of anaerobic toluene degraders and aquifer microbial community patterns in distinct redox zones of a tar oil contaminant plume. Appl Environ Microbiol 74:792–801

    Article  CAS  PubMed  Google Scholar 

  • Wöhlbrand L, Jacob JH, Kube M, Mussmann M, Jarling R, Beck A, Amann R, Wilkes H, Reinhardt R, Rabus R (2013) Complete genome, catabolic sub-proteomes and key metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium. Environ Microbiol 15:1334–1355

    Article  PubMed  CAS  Google Scholar 

  • Yang T, Speare K, McKay L, MacGregor BJ, Joye SB, Teske A (2016) Distinct bacterial communities in surficial seafloor sediments following the 2010 Deepwater Horizon blowout. Front Microbiol 7:1384. doi:10.3389/fmicb.2016.01384

    PubMed  PubMed Central  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. Environ Microbiol Rep 3:125–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zengler K, Richnow HH, Rosselló-Mora R, Michaelis W, Widdel F (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 6750:266–269

    Google Scholar 

  • Zhang X, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Bain TS, Nevin KP, Barlett MA, Lovley DR (2012) Anaerobic benzene oxidation by Geobacter species. Appl Environ Microbiol 78:8304–8310

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Li K-P, Mbadinga SM, Yang S-Z, Gu J-D, Mu B-Z (2012) Analyses of n-alkanes degrading community dynamics of a high-temperature methanogenic consortium enriched from production water of a petroleum reservoir by a combination of molecular techniques. Exotoxicology 21:1680–1691

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lisa M. Gieg .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing AG

About this entry

Cite this entry

Gieg, L.M., Toth, C.R.A. (2016). Anaerobic Biodegradation of Hydrocarbons: Metagenomics and Metabolomics. In: Steffan, R. (eds) Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids: Biodegradation and Bioremediation. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-44535-9_16-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-44535-9_16-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-44535-9

  • Online ISBN: 978-3-319-44535-9

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics