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Next-Generation Sequencing of Functional Marker Genes for Anaerobic Degraders of Petroleum Hydrocarbons in Contaminated Environments

  • Frederick von Netzer
  • Michael S. Granitsiotis
  • Anna R. Szalay
  • Tillmann Lueders
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

The anaerobic degradation of petroleum hydrocarbons is an important ecosystem service provided by microbes in systems impacted by pollution. Research in recent years has resulted in substantial advances in our understanding of the diversity and ecology of natural populations of anaerobic hydrocarbon degraders, both in marine and terrestrial sedimentary and subsurface habitats. Part of this research has been fueled by the development and optimization of specific functional marker genes for anaerobic hydrocarbon degraders, i.e., qualitative and quantitative molecular assays, allowing for the detection of key catabolic genes or transcripts involved in degradation. These include the so-called “fumarate-adding enzymes” benzylsuccinate synthase (bssA) and alkylsuccinate synthase (assA/masD) involved in the primary activation of alkanes and alkylated aromatic hydrocarbons under anaerobic conditions. Here, we summarize the most important advances in the field and highlight the appeal of recent next-generation sequencing-based approaches toward catabolic marker genes for in-depth degrader community dissection. This contributes to a more routine and thorough inspection of intrinsic degrader populations responsible for key catabolic services in systems contaminated with petroleum hydrocarbons.

Keywords

Fumarate-adding enzymes Benzylsuccinate synthase FLX+ pyrosequencing Degrader communities Functional marker genes 

Notes

Acknowledgments

The authors wish to thank the Deutsche Forschungsgemeinschaft (DFG) for the support of parts of the research summarized and presented here within the Priority Programme “Biological transformation of hydrocarbons in the absence of oxygen” (SPP 1319, grants LU 118/4-1 and 4-2). We also acknowledge support of the Helmholtz Society within the ‘Helmholtz Wasserzentrum München.’

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 12:2783–2796PubMedGoogle Scholar
  2. Abu Laban N, Dao A, Foght J (2015) DNA stable-isotope probing of oil sands tailings pond enrichment cultures reveals different key players for toluene degradation under methanogenic and sulfidogenic conditions. FEMS Microbiol Ecol 91:fiv039Google Scholar
  3. Acosta-González A, Rosselló-Móra R, Marqués S (2013) Diversity of benzylsuccinate synthase-like (bssA) genes in hydrocarbon-polluted marine sediments suggests substrate-dependent clustering. Appl Environ Microbiol 79:3667–3676CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aitken CM, Jones DM, Maguire MJ, Gray ND, Sherry A, Bowler BFJ, Ditchfield AK, Larter SR, Head IM (2013) Evidence that crude oil alkane activation proceeds by different mechanisms under sulfate-reducing and methanogenic conditions. Geochim Cosmochim Acta 109:162–174CrossRefGoogle Scholar
  5. Annweiler E, Materna A, Safinowski M, Kappler A, Richnow HH, Michaelis W, Meckenstock RU (2000) Anaerobic degradation of 2-methylnaphthalene by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:5329–5333CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 36:3977–3984CrossRefPubMedGoogle Scholar
  7. Beller HR, Kane SR, Legler TC, McKelvie JR, Sherwood Lollar B, 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 42:6065–6072CrossRefPubMedGoogle Scholar
  8. Benedek T, Táncsics A, Szabó I, Farkas M, Szoboszlay S, Fábián K, Maróti G, Kriszt B (2016) Polyphasic analysis of an Azoarcus-Leptothrix-dominated bacterial biofilm developed on stainless steel surface in a gasoline-contaminated hypoxic groundwater. Environ Sci Pollut Res 23:9019–9035CrossRefGoogle Scholar
  9. Benítez-Páez A, Portune KJ, Sanz Y (2016) Species-level resolution of 16S rRNA gene amplicons sequenced through the MinION™ portable nanopore sequencer. GigaScience 5:4CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bergmann F, Selesi D, Meckenstock R (2011) Identification of new enzymes potentially involved in anaerobic naphthalene degradation by the sulfate-reducing enrichment culture N47. Arch Microbiol 193:241–250CrossRefPubMedGoogle Scholar
  11. Biegert T, Fuchs G, Heider J (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 238:661–668CrossRefPubMedGoogle Scholar
  12. Boll M, Löffler C, Morris BEL, Kung JW (2014) Anaerobic degradation of homocyclic aromatic compounds via arylcarboxyl-coenzyme A esters: organisms, strategies and key enzymes. Environ Microbiol 16:612–627CrossRefPubMedGoogle Scholar
  13. Brow CN, O’Brien Johnson R, Johnson RL, Simon HM (2013) Assessment of anaerobic toluene biodegradation activity by bssA transcript/gene ratios. Appl Environ Microbiol 79:5338–5344CrossRefPubMedPubMedCentralGoogle Scholar
  14. Callaghan AV (2013a) Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front Microbiol 4(89)Google Scholar
  15. Callaghan AV (2013b) Metabolomic investigations of anaerobic hydrocarbon-impacted environments. Curr Opin Biotechnol 24:506–515CrossRefPubMedGoogle Scholar
  16. Callaghan AV, Wawrik B (2016) AnHyDeg: a curated database of anaerobic hydrocarbon degradation genes.  https://doi.org/10.5281/zenodo.61278. https://github.com/AnaerobesRock/AnHyDeg/tree/v1.0
  17. 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 366:142–148CrossRefPubMedGoogle Scholar
  18. 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 44:7287–7294CrossRefPubMedGoogle Scholar
  19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  20. D’Amore R, Ijaz UZ, Schirmer M, Kenny JG, Gregory R, Darby AC, Shakya M, Podar M, Quince C, Hall N (2016) A comprehensive benchmarking study of protocols and sequencing platforms for 16S rRNA community profiling. BMC Genomics 17(55)Google Scholar
  21. Daghio M, Vaiopoulou E, Patil SA, Suárez-Suárez A, Head IM, Franzetti A, Rabaey K (2016) Anodes stimulate anaerobic toluene degradation via sulfur cycling in marine sediments. Appl Environ Microbiol 82:297–307CrossRefPubMedGoogle Scholar
  22. Dorer C, Vogt C, Neu TR, Stryhanyuk H, Richnow H-H (2016) Characterization of toluene and ethylbenzene biodegradation under nitrate-, iron(III)- and manganese(IV)-reducing conditions by compound-specific isotope analysis. Environ Pollut 211:271–281CrossRefPubMedGoogle Scholar
  23. Fahrenfeld N, Cozzarelli I, Bailey Z, Pruden A (2014) Insights into biodegradation through depth-resolved microbial community functional and structural profiling of a crude-oil contaminant plume. Microbial Ecol 68:453–462CrossRefGoogle Scholar
  24. Fish J, Chai B, Wang Q, Sun Y, Brown CT, Tiedje J, Cole J (2013) FunGene: the functional gene pipeline and repository. Front Microbiol 4:291CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fowler SJ, Dong X, Sensen CW, Suflita JM, Gieg LM (2012) Methanogenic toluene metabolism: community structure and intermediates. Environ Microbiol 14:754–764CrossRefPubMedGoogle Scholar
  26. Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9:803–816CrossRefPubMedGoogle Scholar
  27. 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 6:1414CrossRefPubMedPubMedCentralGoogle Scholar
  28. Grbić-Galić D, Vogel TM (1987) Transformation of toluene and benzene by mixed methanogenic cultures. Appl Environ Microbiol 53:254–260PubMedPubMedCentralGoogle Scholar
  29. 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 HxN1. Environ Microbiol 10:376–385CrossRefPubMedGoogle Scholar
  30. Heider J, Schühle K (2013) Anaerobic biodegradation of hydrocarbons including methane. In: Rosenberg E, DeLong E, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin/Heidelberg, pp 605–634CrossRefGoogle Scholar
  31. 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 26:29–44CrossRefPubMedGoogle Scholar
  32. Heider J, Szaleniec M, Sünwoldt K, Boll M (2016b) Ethylbenzene dehydrogenase and related molybdenum enzymes involved in oxygen-independent alkyl chain hydroxylation. J Mol Microbiol Biotechnol 26:45–62CrossRefPubMedGoogle Scholar
  33. Higashioka Y, Kojima H, Sato S, Fukui M (2009) Microbial community analysis at crude oil-contaminated soils targeting the 16S ribosomal RNA, xylM, C23O, and bcr genes. J Appl Microbiol 107:126–135CrossRefPubMedGoogle Scholar
  34. Higashioka Y, Kojima H, Fukui M (2011) Temperature-dependent differences in community structure of bacteria involved in degradation of petroleum hydrocarbons under sulfate-reducing conditions. J Appl Microbiol 110:314–322CrossRefPubMedGoogle Scholar
  35. Hosoda A, Kasai Y, Hamamura N, Takahata Y, Watanabe K (2005) Development of a PCR method for the detection and quantification of benzoyl-CoA reductase genes and its application to monitored natural attenuation. Biodegradation 16:591–601CrossRefPubMedGoogle Scholar
  36. 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 91:1–14CrossRefPubMedGoogle Scholar
  37. Karst SM, Dueholm MS, McIlroy SJ, Kirkegaard RH, Nielsen PH, Albertsen M (2016) Thousands of primer-free, high-quality, full-length SSU rRNA sequences from all domains of life. bioRxiv.  https://doi.org/10.1101/070771
  38. Kimes NE, Callaghan AV, Aktas DF, Smith WL, Sunner J, Golding BT, 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 4:50CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kuntze K, Shinoda Y, Moutakki H, McInerney MJ, Vogt C, Richnow H-H, Boll M (2008) 6-Oxocyclohex-1-ene-1-carbonyl-coenzyme A hydrolases from obligately anaerobic bacteria: characterization and identification of its gene as a functional marker for aromatic compounds degrading anaerobes. Environ Microbiol 10:1547–1556CrossRefPubMedGoogle Scholar
  40. Kuntze K, Vogt C, Richnow H-H, Boll M (2011) Combined application of PCR-based functional assays for the detection of aromatic-compound-degrading anaerobes. Appl Environ Microbiol 77:5056–5061CrossRefPubMedPubMedCentralGoogle Scholar
  41. Li C, Ren H, Yin E, Tang S, Li Y, Cao J (2015) Pilot-scale study on nitrogen and aromatic compounds removal in printing and dyeing wastewater by reinforced hydrolysis-denitrification coupling process and its microbial community analysis. Environ Sci Pollut Res 22:9483–9493CrossRefGoogle Scholar
  42. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lueders T (2017) The ecology of anaerobic degraders of BTEX hydrocarbons in aquifers. FEMS Microbiol Ecol 93:fiw220CrossRefPubMedGoogle Scholar
  44. Lueders T, von Netzer F (2014) Primers: functional genes for anaerobic hydrocarbon degrading microbes. In: TJ MG et al (eds) Hydrocarbon and lipid microbiology protocols, Springer Protocols Handbooks. Springer, Berlin/Heidelberg.  https://doi.org/10.1007/8623_2014_1044CrossRefGoogle Scholar
  45. Lüke C, Frenzel P (2011) Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77:6305–6309CrossRefPubMedPubMedCentralGoogle Scholar
  46. Luo C, Tsementzi D, Kyrpides N, Read T, Konstantinidis KT (2012) Direct comparisons of Illumina vs. Roche 454 sequencing technologies on the same microbial community DNA sample. PLoS One 7:e30087CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 80:4095–4107CrossRefPubMedPubMedCentralGoogle Scholar
  48. Martirani-Von Abercron S-M, Pacheco D, Benito-Santano P, Marín P, Marqués S (2016) Polycyclic aromatic hydrocarbon-induced changes in bacterial community structure under anoxic nitrate reducing conditions. Front Microbiol 7:1775CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 26:92–118CrossRefPubMedGoogle Scholar
  50. Morris BEL, Gissibl A, Kümmel S, Richnow H-H, Boll M (2014) A PCR-based assay for the detection of anaerobic naphthalene degradation. FEMS Microbiol Lett 354:55–59CrossRefPubMedGoogle Scholar
  51. 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 14:2770–2774CrossRefPubMedGoogle Scholar
  52. 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 11:209–219CrossRefPubMedGoogle Scholar
  53. Oka AR, Phelps CD, Zhu X, Saber DL, Young LY (2011) Dual biomarkers of anaerobic hydrocarbon degradation in historically contaminated groundwater. Environ Sci Technol 45:3407–3414CrossRefPubMedGoogle Scholar
  54. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists., R package version: 2.4–2 edn. https://cran.r-project.org/web/packages/vegan/
  55. Osman OA, Gudasz C, Bertilsson S (2014) Diversity and abundance of aromatic catabolic genes in lake sediments in response to temperature change. FEMS Microbiol Ecol 88:468–481CrossRefPubMedGoogle Scholar
  56. Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539CrossRefPubMedPubMedCentralGoogle Scholar
  57. Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron P-A (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619CrossRefPubMedPubMedCentralGoogle Scholar
  58. Pilloni G, von Netzer F, Engel M, Lueders T (2011) Electron acceptor-dependent identification of key anaerobic toluene degraders at a tar-oil-contaminated aquifer by Pyro-SIP. FEMS Microbiol Ecol 78:165–175CrossRefPubMedGoogle Scholar
  59. Pilloni G, Granitsiotis MS, Engel M, Lueders T (2012) Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to T-RFLP fingerprinting of aquifer microbes. PLoS One 7:e40467CrossRefPubMedPubMedCentralGoogle Scholar
  60. Porter AW, Young LY (2013) The bamA gene for anaerobic ring fission is widely distributed in the environment. Front Microbiol 4:302CrossRefPubMedPubMedCentralGoogle Scholar
  61. Porter AW, Young LY (2014) Benzoyl-CoA, a universal biomarker for anaerobic degradation of aromatic compounds. In: Sariaslani S, Gadd GM (eds) Adv Appl Microbiol, vol 88. Academic Press, London, UK, pp 167–203Google Scholar
  62. Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, Ermler U, Golding BT, Gunsalus RP, Kroneck PMH, 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 26:5–28CrossRefPubMedGoogle Scholar
  63. Ranchou-Peyruse M, Gasc C, Guignard M, Aüllo T, Dequidt D, Peyret P, Ranchou-Peyruse A (2016) The sequence capture by hybridization: a new approach for revealing the potential of mono-aromatic hydrocarbons bioattenuation in a deep oligotrophic aquifer. Microb Biotechnol 10:469–479CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sampaio DS, Almeida JRB, de Jesus HE, Rosado AS, Seldin L, Jurelevicius D (2017) Distribution of anaerobic hydrocarbon-degrading bacteria in soils from King George Island, Maritime Antarctica. Microbial Ecol 74:810–820CrossRefGoogle Scholar
  65. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  66. Schloss PD, Jenior ML, Koumpouras CC, Westcott SL, Highlander SK (2016) Sequencing 16S rRNA gene fragments using the PacBio SMRT DNA sequencing system. Peer J 4:e1869CrossRefPubMedGoogle Scholar
  67. Scoma A, Yakimov MM, Daffonchio D, Boon N (2017) Self-healing capacity of deep-sea ecosystems affected by petroleum hydrocarbons: understanding microbial oil degradation at hydrocarbon seeps is key to sustainable bioremediation protocols. EMBO Rep 18:868–872CrossRefPubMedPubMedCentralGoogle Scholar
  68. Song B, Ward BB (2005) Genetic diversity of benzoyl coenzyme-A reductase genes detected in denitrifying isolates and estuarine sediment communities. Appl Environ Microbiol 71:2036–2045CrossRefPubMedPubMedCentralGoogle Scholar
  69. Spencer SJ, Tamminen MV, Preheim SP, Guo MT, Briggs AW, Brito IL, Weitz DA, Pitkanen LK, Vigneault F, Virta MP, Alm EJ (2016) Massively parallel sequencing of single cells by epicPCR links functional genes with phylogenetic markers. ISME J 10:427–436CrossRefPubMedGoogle Scholar
  70. Staats M, Braster M, Röling WFM (2011) Molecular diversity and distribution of aromatic hydrocarbon-degrading anaerobes across a landfill leachate plume. Environ Microbiol 13:1216–1227CrossRefPubMedGoogle Scholar
  71. 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 6:1511CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sun W, Sun X, Cupples A (2014) Presence, diversity and enumeration of functional genes (bssA and bamA) relating to toluene degradation across a range of redox conditions and inoculum sources. Biodegradation 25:189–203CrossRefPubMedGoogle Scholar
  73. 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 anaerobic hydrocarbon degraders in terrestrial and marine systems. Appl Environ Microbiol 79:543–552CrossRefGoogle Scholar
  74. 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
  75. Wagner J, Coupland P, Browne HP, Lawley TD, Francis SC, Parkhill J (2016) Evaluation of PacBio sequencing for full-length bacterial 16S rRNA gene classification. BMC Microbiol 16:274CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wallisch S, Gril T, Dong X, Welzl G, Bruns C, Heath E, Engel M, Suhadolc M, Schloter M (2014) Influence of compost amendments on the diversity of alkane degrading bacteria in hydrocarbon contaminated soils. Front Microbiol 5(96)Google Scholar
  77. Weelink SAB, van Eekert MHA, Stams AJM (2010) Degradation of BTEX by anaerobic bacteria: physiology and application. Rev Environ Sci Biotechnol 9:359–385CrossRefGoogle Scholar
  78. Widdel F, Knittel K, Galushko A (2010) Anaerobic hydrocarbon-degrading microorganisms: an overview. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg, pp 1997–2021CrossRefGoogle Scholar
  79. Wilkes H, Buckel W, Golding BT, Rabus R (2016) Metabolism of hydrocarbons in n-alkane-utilizing anaerobic bacteria. J Mol Microbiol Biotechnol 26:138–151CrossRefPubMedGoogle Scholar
  80. 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 9:1035–1046CrossRefPubMedGoogle Scholar
  81. 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 74:792–801CrossRefPubMedGoogle Scholar
  82. Winderl C, Penning H, von Netzer F, Meckenstock RU, Lueders T (2010) DNA-SIP identifies sulfate-reducing Clostridia as important toluene degraders in tar-oil-contaminated aquifer sediment. ISME J 4:1314–1325CrossRefPubMedGoogle Scholar
  83. Yagi JM, Suflita JM, Gieg LM, DeRito CM, Jeon C-O, Madsen EL (2010) Subsurface cycling of nitrogen and anaerobic aromatic hydrocarbon biodegradation revealed by nucleic acid and metabolic biomarkers. Appl Environ Microbiol 76:3124–3134CrossRefPubMedPubMedCentralGoogle Scholar
  84. Zhang L, Lueders T (2017) Micropredator niche differentiation between bulk soil and rhizosphere of an agricultural soil depends on bacterial prey. FEMS Microbiol Ecol 93:fix103CrossRefGoogle Scholar
  85. Zhang B, Penton CR, Xue C, Wang Q, Zheng T, Tiedje JM (2015) Evaluation of the Ion Torrent Personal Genome Machine for gene-targeted studies using amplicons of the nitrogenase gene nifH. Appl Environ Microbiol 81:4536–4545CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Frederick von Netzer
    • 1
    • 2
  • Michael S. Granitsiotis
    • 3
    • 4
    • 5
  • Anna R. Szalay
    • 1
  • Tillmann Lueders
    • 1
  1. 1.Helmholtz Zentrum München – German Research Center for Environmental Health, Institute of Groundwater EcologyNeuherbergGermany
  2. 2.Department of Civil and Environmental EngineeringUniversity of WashingtonSeattleUSA
  3. 3.Research Unit Comparative Microbiome AnalysisHelmholtz Zentrum München – German Research Center for Environmental HealthNeuherbergGermany
  4. 4.Department of EnergyJoint Genome InstituteWalnut CreekUSA
  5. 5.Department of Environmental and Natural Resources ManagementUniversity of PatrasAgrinioGreece

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