Abstract
Biodegradation of anthropogenic pollutants in shallow aquifers is an important microbial ecosystem service which is mainly brought about by indigenous anaerobic microorganisms. For the management of contaminated sites, risk assessment and control of natural attenuation, the assessment of in situ biodegradation and the underlying microbial processes is essential. The development of novel molecular methods, “omics” approaches, and high-throughput techniques has revealed new insight into complex microbial communities and their functions in anoxic environmental systems. This review summarizes recent advances in the application of molecular methods to study anaerobic microbial communities in contaminated terrestrial subsurface ecosystems. We focus on current approaches to analyze composition, dynamics, and functional diversity of subsurface communities, to link identity to activity and metabolic function, and to identify the ecophysiological role of not yet cultured microbes and syntrophic consortia. We discuss recent molecular surveys of contaminated sites from an ecological viewpoint regarding degrader ecotypes, abiotic factors shaping anaerobic communities, and biotic interactions underpinning the importance of microbial cooperation for microbial ecosystem services such as contaminant degradation.
Similar content being viewed by others
References
Abbai NS, Govender A, Shaik R, Pillay B (2011) Pyrosequence analysis of unamplified and whole genome amplified DNA from hydrocarbon-contaminated groundwater. Mol Biotechnol 50:39–48
Abu Laban N, Selesi D, Jobelius C, Meckenstock RU (2009) Anaerobic benzene degradation by Gram-positive sulfate-reducing bacteria. FEMS Microbiol Ecol 68:300–311
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
Abulencia CB, Wyborski DL, Garcia JA, Podar M, Chen W, Chang SH, Chang HW, Watson D, Brodie EL, Hazen TC, Keller M (2006) Environmental whole-genome amplification to access microbial populations in contaminated sediments. Appl Environ Microbiol 72:3291–3301
Ahn YB, Chae JC, Zylstra GJ, Häggblom 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 Microbiol 75:4248–4253
Andreoni V, Gianfreda L (2007) Bioremediation and monitoring of aromatic-polluted habitats. Appl Microbiol Biotechnol 76:287–308
Anneser B, Pilloni G, Bayer A, Lueders T, Griebler C, Einsiedl F, Richters L (2010) High resolution analysis of contaminated aquifer sediments and groundwater—what can be learned in terms of natural attenuation? Geomicrobiol J 27:130–142
Armengaud J (2009) A perfect genome annotation is within reach with the proteomics and genomics alliance. Curr Opin Microbiol 12:292–300
Beckmann S, Lueders T, Krüger M, von Netzer F, Engelen B, Cypionka H (2011) Acetogens and acetoclastic methanosarcinales govern methane formation in abandoned coal mines. Appl Environ Microbiol 77:3749–3756
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
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
Benndorf D, Vogt C, Jehmlich N, Schmidt Y, Thomas H, Woffendin G, Shevchenko A, Richnow HH, von Bergen M (2009) Improving protein extraction and separation methods for investigating the metaproteome of anaerobic benzene communities within sediments. Biodegradation 20:737–750
Berdugo-Clavijo C, Dong X, Soh J, Sensen CW, Gieg LM (2012) Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol. doi:10.1111/j.1574-6941.2012.01328.x
Berg IA (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microbiol 77:1925–1936
Berlendis S, Lascourreges JF, Schraauwers B, Sivadon P, Magot M (2010) Anaerobic biodegradation of BTEX by original bacterial communities from an underground gas storage aquifer. Environ Sci Technol 44:3621–3628
Binga EK, Lasken RS, Neufeld JD (2008) Something from (almost) nothing: the impact of multiple displacement amplification on microbial ecology. ISME J 2:233–241
Bjerg PL, Rugge K, Cortsen J, Nielsen PH, Christensen TH (1999) Degradation of aromatic and chlorinated aliphatic hydrocarbons in the anaerobic part of the Grindsted landfill leachate plume: in situ microcosm and laboratory batch experiments. Ground Water 37:113–121
Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR (2011) Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6:e16626
Bombach P, Chatzinotas A, Neu TR, Kästner M, Lueders T, Vogt C (2010a) Enrichment and characterization of a sulfate-reducing toluene-degrading microbial consortium by combining in situ microcosms and stable isotope probing techniques. FEMS Microbiol Ecol 71:237–246
Bombach P, Richnow HH, Kästner M, Fischer A (2010b) Current approaches for the assessment of in situ biodegradation. Appl Microbiol Biotechnol 86:839–852
Bombach P, Hübschmann T, Fetzer I, Kleinsteuber S, Geyer R, Harms H, Müller S (2011) Resolution of natural microbial community dynamics by community fingerprinting, flow cytometry, and trend interpretation analysis. Adv Biochem Eng/Biotechnol 124:151–181
Botton S, van Harmelen M, Braster M, Parsons JR, Röling WF (2007) Dominance of Geobacteraceae in BTX-degrading enrichments from an iron-reducing aquifer. FEMS Microbiol Ecol 62:118–130
Bozinovski D, Herrmann S, Richnow H-H, van 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. doi:10.1111/j.1574- 6941.2012.01334.x
Callaghan AV, Wawrik B, Ni 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
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
Callister SJ, Wilkins MJ, Nicora CD, Williams KH, Banfield JF, VerBerkmoes NC, Hettich RL, N'Guessan L, Mouser PJ, Elifantz H, Smith RD, Lovley DR, Lipton MS, Long PE (2010) Analysis of biostimulated microbial communities from two field experiments reveals temporal and spatial differences in proteome profiles. Environ Sci Technol 44:8897–8903
Canfield DE, Rosing MT, Bjerrum C (2006) Early anaerobic metabolisms. Philos Trans R Soc Lond B Biol Sci 361:1819–1834
Cantarel BL, Erickson AR, Verberkmoes NC, Erickson BK, Carey PA, Pan C, Shah M, Mongodin EF, Jansson JK, Fraser-Liggett CM, Hettich RL (2011) Strategies for metagenomic-guided whole-community proteomics of complex microbial environments. PLoS One 6:e27173
Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85:207–228
Carmona M, Zamarro MT, Blazquez B, Durante-Rodriguez G, Juarez JF, Valderrama JA, Barragan MJ, Garcia JL, Diaz E (2009) Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev 73:71–133
Chang Y-J, Long PE, Geyer R, Peacock AD, Resch CT, Sublette K, Pfiffner S, Smithgall A, Anderson RT, Vrionis HA, Stephen JR, Dayvoult R, Ortiz-Bernad I, Lovley DR, White DC (2005) Microbial incorporation of 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U(VI). Environ Sci Technol 39:9039–9048
Chauhan A, Ogram A (2006) Phylogeny of acetate-utilizing microorganisms in soils along a nutrient gradient in the Florida Everglades. Appl Environ Microbiol 72:6837–6840
Chen Y, Murrell JC (2010) When metagenomics meets stable-isotope probing: progress and perspectives. Trends Microbiol 18:157–163
Chivian D, Brodie EL, Alm EJ, Culley DE, Dehal PS, DeSantis TZ, Gihring TM, Lapidus A, Lin LH, Lowry SR, Moser DP, Richardson PM, Southam G, Wanger G, Pratt LM, Andersen GL, Hazen TC, Brockman FJ, Arkin AP, Onstott TC (2008) Environmental genomics reveals a single-species ecosystem deep within Earth. Science 322:275–278
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
Cupples AM (2011) The use of nucleic acid based stable isotope probing to identify the microorganisms responsible for anaerobic benzene and toluene biodegradation. J Microbiol Methods 85:83–91
Da Silva ML, Alvarez PJ (2004) Enhanced anaerobic biodegradation of benzene–toluene–ethylbenzene–xylene–ethanol mixtures in bioaugmented aquifer columns. Appl Environ Microbiol 70:4720–4726
Davidova IA, Gieg LM, Duncan KE, Suflita JM (2007) Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME J 1:436–442
Dean FB, Nelson JR, Giesler TL, Lasken RS (2001) Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 11:1095–1099
Del Casale A, Flanagan PV, Larkin MJ, Allen CC, Kulakov LA (2011a) Analysis of transduction in wastewater bacterial populations by targeting the phage-derived 16S rRNA gene sequences. FEMS Microbiol Ecol 76:100–108
Del Casale A, Flanagan PV, Larkin MJ, Allen CC, Kulakov LA (2011b) Extent and variation of phage-borne bacterial 16S rRNA gene sequences in wastewater environments. Appl Environ Microbiol 77:5529–5532
Drake HL, Horn MA, Wüst PK (2009) Intermediary ecosystem metabolism as a main driver of methanogenesis in acidic wetland soil. Environ Microbiol Reports 1:307–318
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
Foght J (2008) Anaerobic biodegradation of aromatic hydrocarbons: pathways and prospects. J Mol Microbiol Biotechnol 15:93–120
Forbes CM, O'Leary ND, Dobson AD, Marchesi JR (2009) The contribution of ‘omic’-based approaches to the study of enhanced biological phosphorus removal microbiology. FEMS Microbiol Ecol 69:1–15
Fowler SJ, Dong X, Sensen CW, Suflita JM, Gieg LM (2012) Methanogenic toluene metabolism: community structures and intermediates. Environ Microbiol 14:754–764
Friedrich MW (2006) Stable-isotope probing of DNA: insights into the function of uncultivated microorganisms from isotopically labeled metagenomes. Curr Opin Biotechnol 17:59–66
Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol 9:803–816
Gallagher EM, Young LY, McGuinness LM, Kerkhof LJ (2010) Detection of 2,4,6-trinitrotoluene-utilizing anaerobic bacteria by 15N and 13C incorporation. Appl Environ Microbiol 76:1695–1698
Garcia Martin H, Ivanova N, Kunin V, Warnecke F, Barry KW, McHardy AC, Yeates C, He S, Salamov AA, Szeto E, Dalin E, Putnam NH, Shapiro HJ, Pangilinan JL, Rigoutsos I, Kyrpides NC, Blackall LL, McMahon KD, Hugenholtz P (2006) Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities. Nat Biotechnol 24:1263–1269
Gilbert JA, Dupont CL (2011) Microbial metagenomics: beyond the genome. Ann Rev Marine Sci 3:347–371
Gillham RW, Starr RC, Miller DJ (1990) A device for insitu determination of geochemical transport parameters. 2. Biochemical reactions. Ground Water 28:858–862
Glöckner J, Kube M, Shrestha PM, Weber M, Glöckner FO, Reinhardt R, Liesack W (2010) Phylogenetic diversity and metagenomics of candidate division OP3. Environ Microbiol 12:1218–1229
Griebler C, Lueders T (2009) Microbial biodiversity in groundwater ecosystems. Freshwat Biol 54:649–677
Griebler C, Mindl B, Slezak D, Geiger-Kaiser M (2002) Distribution patterns of attached and suspended bacteria in pristine and contaminated shallow aquifers studied with an in situ sediment exposure microcosm. Aquat Microb Ecol 28:117–129
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 10:376–385
Guermazi S, Daegelen P, Dauga C, Riviere D, Bouchez T, Godon JJ, Gyapay G, Sghir A, Pelletier E, Weissenbach J, Le Paslier D (2008) Discovery and characterization of a new bacterial candidate division by an anaerobic sludge digester metagenomic approach. Environ Microbiol 10:2111–2123
Günther S, Trutnau M, Kleinsteuber S, Hause G, Bley T, Röske I, Harms H, Müller S (2009) Dynamics of polyphosphate-accumulating bacteria in wastewater treatment plant microbial communities detected via DAPI (4′,6′-diamidino-2-phenylindole) and tetracycline labeling. Appl Environ Microbiol 75:2111–2121
Günther S, Koch C, Hübschmann T, Röske I, Müller RA, Bley T, Harms H, Müller S (2011) Correlation of community dynamics and process parameters as a tool for the prediction of the stability of wastewater treatment. Environ Sci Technol 46:84–92
Harwood CS, Burchhardt G, Herrmann H, Fuchs G (1998) Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol Rev 22:439–458
Hatamoto M, Imachi H, Yashiro Y, Ohashi A, Harada H (2007) Diversity of anaerobic microorganisms involved in long-chain fatty acid degradation in methanogenic sludges as revealed by RNA-based stable isotope probing. Appl Environ Microbiol 73:4119–4127
Heider J (2007) Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr Opin Chem Biol 11:188–194
Hemme CL, Deng Y, Gentry TJ, Fields MW, Wu L, Barua S, Barry K, Tringe SG, Watson DB, He Z, Hazen TC, Tiedje JM, Rubin EM, Zhou J (2010) Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J 4:660–672
Hendrickx B, Dejonghe W, Boenne W, Brennerova M, Cernik M, Lederer T, Bucheli-Witschel M, Bastiaens L, Verstraete W, Top EM, Diels L, Springael D (2005) Dynamics of an oligotrophic bacterial aquifer community during contact with a groundwater plume contaminated with benzene toluene, ethylbenzene, and xylenes: an in situ mesocosm study. Appl Environ Microbiol 71:3815–3825
Herrmann S, Kleinsteuber S, Neu TR, Richnow HH, Vogt C (2008) Enrichment of anaerobic benzene-degrading microorganisms by in situ microcosms. FEMS Microbiol Ecol 63:94–106
Herrmann S, Vogt C, Fischer A, Kuppardt A, Richnow H-H (2009) Characterization of anaerobic xylene biodegradation by two-dimensional isotope fractionation analysis. Environ Microbiol Reports 1:535–544
Herrmann S, Kleinsteuber S, Chatzinotas A, Kuppardt S, Lueders T, Richnow HH, Vogt C (2010) Functional characterization of an anaerobic benzene-degrading enrichment culture by DNA stable isotope probing. Environ Microbiol 12:401–411
Holmes DE, O'Neil RA, Vrionis HA, N'Guessan LA, Ortiz-Bernad I, Larrahondo MJ, Adams LA, Ward JA, Nicoll JS, Nevin KP, Chavan MA, Johnson JP, Long PE, Lovley DR (2007) Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J 1:663–677
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
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 16:591–601
Huang WE, Stoecker K, Griffiths R, Newbold L, Daims H, Whiteley AS, Wagner M (2007) Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ Microbiol 9:1878–1889
Hubert CR, Oldenburg TB, Fustic M, Gray ND, Larter SR, Penn K, Rowan AK, Seshadri R, Sherry A, Swainsbury R, Voordouw G, Voordouw JK, Head IM (2011) Massive dominance of Epsilonproteobacteria in formation waters from a Canadian oil sands reservoir containing severely biodegraded oil. Environ Microbiol 14:387–404
Hugenholtz P, Tyson GW (2008) Microbiology: metagenomics. Nature 455:481–483
Hunkeler D, Jorger D, Haberli K, Hohener P, Zeyer J (1998) Petroleum hydrocarbon mineralization in anaerobic laboratory aquifer columns. J Contam Hydrol 32:41–61
Imachi H, Sekiguchi Y, Kamagata Y, Loy A, Qiu YL, Hugenholtz P, Kimura N, Wagner M, Ohashi A, Harada H (2006) Non-sulfate-reducing, syntrophic bacteria affiliated with Desulfotomaculum cluster I are widely distributed in methanogenic environments. Appl Environ Microbiol 72:2080–2091
Ishii S, Tago K, Senoo K (2010) Single-cell analysis and isolation for microbiology and biotechnology: methods and applications. Appl Microbiol Biotechnol 86:1281–1292
Ishoey T, Woyke T, Stepanauskas R, Novotny M, Lasken RS (2008) Genomic sequencing of single microbial cells from environmental samples. Curr Opin Microbiol 11:198–204
Iwai S, Johnson TA, Chai B, Hashsham SA, Tiedje JM (2011) Comparison of the specificities and efficacies of primers for aromatic dioxygenase gene analysis of environmental samples. Appl Environ Microbiol 77:3551–3557
Jackson BE, Bhupathiraju VK, Tanner RS, Woese CR, McInerney MJ (1999) Syntrophus aciditrophicus sp. nov., a new anaerobic bacterium that degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms. Arch Microbiol 171:107–114
Jehmlich N, Schmidt F, Hartwich M, von Bergen M, Richnow HH, Vogt C (2008a) Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein-SIP). Rapid Commun Mass Spectrom 22:2889–2897
Jehmlich N, Schmidt F, von Bergen M, Richnow HH, Vogt C (2008b) Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. ISME J 2:1122–1133
Jehmlich N, Hübschmann T, Gesell Salazar M, Volker U, Benndorf D, Müller S, von Bergen M, Schmidt F (2010a) Advanced tool for characterization of microbial cultures by combining cytomics and proteomics. Appl Microbiol Biotechnol 88:575–584
Jehmlich N, Kleinsteuber S, Vogt C, Benndorf D, Harms H, Schmidt F, von Bergen M, Seifert J (2010b) Phylogenetic and proteomic analysis of an anaerobic toluene-degrading community. J Appl Microbiol 109:1937–1945
Jehmlich N, Schmidt F, Taubert M, Seifert J, Bastida F, von Bergen M, Richnow HH, Vogt C (2010c) Protein-based stable isotope probing. Nature Protoc 5:1957–1966
Jones DS, Tobler DJ, Schaperdoth I, Mainiero M, Macalady JL (2010) Community structure of subsurface biofilms in the thermal sulfidic caves of Acquasanta Terme, Italy. Appl Environ Microbiol 76:5902–5910
Kasai Y, Takahata Y, Manefield M, Watanabe K (2006) RNA-based stable isotope probing and isolation of anaerobic benzene-degrading bacteria from gasoline-contaminated groundwater. Appl Environ Microbiol 72:3586–3592
Kato S, Hashimoto K, Watanabe K (2011) Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ Microbiol. doi:10.1111/j.1462-2920.2011.02611.x
Keller M, Hettich R (2009) Environmental proteomics: a paradigm shift in characterizing microbial activities at the molecular level. Microbiol Mol Biol Rev 73:62–70
Kerkhof LJ, Williams KH, Long PE, McGuinness LR (2011) Phase preference by active, acetate-utilizing bacteria at the Rifle, CO integrated field research challenge site. Environ Sci Technol 45:1250–1256
Kiely PD, Regan JM, Logan BE (2011) The electric picnic: synergistic requirements for exoelectrogenic microbial communities. Curr Opin Biotechnol 22:378–385
Kleemann R, Meckenstock RU (2011) Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiol Ecol 78:488–496
Kleinsteuber S, Schleinitz KM, Breitfeld J, Harms H, Richnow HH, Vogt C (2008) Molecular characterization of bacterial communities mineralizing benzene under sulfate-reducing conditions. FEMS Microbiol Ecol 66:143–157
Kosaka T, Kato S, Shimoyama T, Ishii S, Abe T, Watanabe K (2008) The genome of Pelotomaculum thermopropionicum reveals niche-associated evolution in anaerobic microbiota. Genome Res 18:442–448
Kuhn EP, Colberg PJ, Schnoor JL, Wanner O, Zehnder AJB, Schwarzenbach RP (1985) Microbial transformations of substituted benzenes during infiltration of river water to groundwater—laboratory column studies. Environ Sci Technol 19:961–968
Kuhn EP, Zeyer J, Eicher P, Schwarzenbach RP (1988) Anaerobic degradation of alkylated benzenes in denitrifying laboratory aquifer columns. Appl Environ Microbiol 54:490–496
Kunapuli U, Lueders T, Meckenstock RU (2007) The use of stable isotope probing to identify key iron-reducing microorganisms involved in anaerobic benzene degradation. ISME J 1:643–653
Kunapuli U, Jahn MK, Lueders T, Geyer R, Heipieper HJ, Meckenstock RU (2010) Desulfitobacterium aromaticivorans sp. nov. and Geobacter toluenoxydans sp. nov., iron-reducing bacteria capable of anaerobic degradation of monoaromatic hydrocarbons. Int J Syst Evol Microbiol 60:686–695
Kung JW, Löffler C, Dorner K, Heintz D, Gallien S, Van Dorsselaer A, Friedrich T, Boll M (2009) Identification and characterization of the tungsten-containing class of benzoyl-coenzyme A reductases. Proc Nat Acad Sci USA 106:17687–17692
Kuntze K, Shinoda Y, Moutakki H, McInerney MJ, Vogt C, Richnow HH, 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 10:1547–1556
Kuntze K, Vogt C, Richnow HH, Boll M (2011) Combined application of PCR-based functional assays for the detection of aromatic-compound-degrading anaerobes. Appl Environ Microbiol 77:5056–5061
Lasken RS (2007) Single-cell genomic sequencing using multiple displacement amplification. Curr Opin Microbiol 10:510–516
Li T, Mazéas L, Sghir A, Leblon G, Bouchez T (2009) Insights into networks of functional microbes catalysing methanization of cellulose under mesophilic conditions. Environ Microbiol 11:889–904
Liou JS, Derito CM, Madsen EL (2008) Field-based and laboratory stable isotope probing surveys of the identities of both aerobic and anaerobic benzene-metabolizing microorganisms in freshwater sediment. Environ Microbiol 10:1964–1977
Löffler C, Kuntze K, Vazquez JR, Rugor A, Kung JW, Böttcher A, Boll M (2011) Occurrence, genes and expression of the W/Se-containing class II benzoyl-coenzyme A reductases in anaerobic bacteria. Environ Microbiol 13:696–709
Lombard N, Prestat E, van Elsas JD, Simonet P (2011) Soil-specific limitations for access and analysis of soil microbial communities by metagenomics. FEMS Microbiol Ecol 78:31–49
Lopez Barragan MJ, Carmona M, Zamarro MT, Thiele B, Boll M, Fuchs G, Garcia JL, Diaz E (2004) The bzd gene cluster, coding for anaerobic benzoate catabolism, in Azoarcus sp. strain CIB. J Bacteriol 186:5762–5774
Lykidis A, Chen CL, Tringe SG, McHardy AC, Copeland A, Kyrpides NC, Hugenholtz P, Macarie H, Olmos A, Monroy O, Liu WT (2011) Multiple syntrophic interactions in a terephthalate-degrading methanogenic consortium. ISME J 5:122–130
MacGregor BJ, Boschker HT, Amann R (2006) Comparison of rRNA and polar-lipid-derived fatty acid biomarkers for assessment of 13C-substrate incorporation by microorganisms in marine sediments. Appl Environ Microbiol 72:5246–5253
Madsen EL (2006) The use of stable isotope probing techniques in bioreactor and field studies on bioremediation. Curr Opin Biotechnol 17:92–97
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
Manefield M, Whiteley AS, Bailey MJ (2004) What can stable isotope probing do for bioremediation? Int Biodeterior Biodegrad 54:163–166
Mbadinga SM, Wang L-Y, Zhou L, Liu J-F, Gu J-D, Mu B-Z (2011) Microbial communities involved in anaerobic degradation of alkanes. Int Biodeterior Biodegrad 65:1–13
McInerney MJ, Sieber JR, Gunsalus RP (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20:623–632
Meckenstock RU (1999) Fermentative toluene degradation in anaerobic defined syntrophic cocultures. FEMS Microbiol Lett 177:67–73
Meckenstock RU, Mouttaki H (2011) Anaerobic degradation of non-substituted aromatic hydrocarbons. Curr Opin Biotechnol 22:406–414
Melnyk RA, Engelbrektson A, Clark IC, Carlson HK, Byrne-Bailey K, Coates JD (2011) Identification of a perchlorate reduction genomic island with novel regulatory and metabolic genes. Appl Environ Microbiol 77:7401–7404
Miyatake T, MacGregor BJ, Boschker HT (2009) Linking microbial community function to phylogeny of sulfate-reducing Deltaproteobacteria in marine sediments by combining stable isotope probing with magnetic-bead capture hybridization of 16S rRNA. Appl Environ Microbiol 75:4927–4935
Morales SE, Holben WE (2011) Linking bacterial identities and ecosystem processes: can ‘omic’ analyses be more than the sum of their parts? FEMS Microbiol Ecol 75:2–16
Mountfort DO, Brulla WJ, Krumholz MR, Bryant MP (1984) Syntrophus buswellii gen. nov., sp. nov.—a benzoate catabolizer from methanogenic ecosystems. Int J Syst Bacteriol 34:216–217
Müller S, Nebe-von-Caron G (2010) Functional single-cell analyses: flow cytometry and cell sorting of microbial populations and communities. FEMS Microbiol Rev 34:554–587
Müller S, Vogt C, Laube M, Harms H, Kleinsteuber S (2009) Community dynamics within a bacterial consortium during growth on toluene under sulfate-reducing conditions. FEMS Microbiol Ecol 70:586–596
Musat F, Widdel F (2008) Anaerobic degradation of benzene by a marine sulfate-reducing enrichment culture, and cell hybridization of the dominant phylotype. Environ Microbiol 10:10–19
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
Musat N, Foster R, Vagner T, Adam B, Kuypers MM (2011) Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol Rev 36:486–511
Neufeld JD, Dumont MG, Vohra J, Murrell JC (2007a) Methodological considerations for the use of stable isotope probing in microbial ecology. Microb Ecol 53:435–442
Neufeld JD, Wagner M, Murrell JC (2007b) Who eats what, where and when? Isotope-labelling experiments are coming of age. ISME J 1:103–110
Nielsen PH, Christensen TH, Albrechtsen HJ, Gillham RW (1996) Performance of the in situ microcosm technique for measuring the degradation of organic chemicals in aquifers. Ground Water Monit Remediat 16:130–140
Oka AR, Phelps CD, McGuinness LM, Mumford A, Young LY, Kerkhof LJ (2008) Identification of critical members in a sulfidogenic benzene-degrading consortium by DNA stable isotope probing. Appl Environ Microbiol 74:6476–6480
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
Omsland A, Cockrell DC, Howe D, Fischer ER, Virtaneva K, Sturdevant DE, Porcella SF, Heinzen RA (2009) Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc Nat Acad Sci USA 106:4430–4434
Orphan VJ (2009) Methods for unveiling cryptic microbial partnerships in nature. Curr Opin Microbiol 12:231–237
Parsley LC, Consuegra EJ, Thomas SJ, Bhavsar J, Land AM, Bhuiyan NN, Mazher MA, Waters RJ, Wommack KE, Harper WF Jr, Liles MR (2010) Census of the viral metagenome within an activated sludge microbial assemblage. Appl Environ Microbiol 76:2673–2677
Peacock AD, Chang YJ, Istok JD, Krumholz L, Geyer R, Kinsall B, Watson D, Sublette KL, White DC (2004) Utilization of microbial biofilms as monitors of bioremediation. Microb Ecol 47:284–292
Pelletier E, Kreimeyer A, Bocs S, Rouy Z, Gyapay G, Chouari R, Riviere D, Ganesan A, Daegelen P, Sghir A, Cohen GN, Medigue C, Weissenbach J, Le Paslier D (2008) “Candidatus Cloacamonas acidaminovorans”: genome sequence reconstruction provides a first glimpse of a new bacterial division. J Bacteriol 190:2572–2579
Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ (2008) Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Nat Acad Sci USA 105:7052–7057
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 78:165–175
Plugge CM, Zhang W, Scholten JCM, Stams AJM (2011) Metabolic flexibility of sulfate-reducing bacteria. Frontiers Microbiol 2:1–8
Pope PB, Smith W, Denman SE, Tringe SG, Barry K, Hugenholtz P, McSweeney CS, McHardy AC, Morrison M (2011) Isolation of Succinivibrionaceae implicated in low methane emissions from Tammar wallabies. Science 333:646–648
Porter ML, Engel AS (2008) Diversity of uncultured Epsilonproteobacteria from terrestrial sulfidic caves and springs. Appl Environ Microbiol 74:4973–4977
Qiu LY, Sekiguchi Y, Imachi H, Kamagata Y, Tseng IC, Cheng SS, Ohashi A, Harada H (2003) Sporotomaculum syntrophicum sp. nov., a novel anaerobic, syntrophic benzoate-degrading bacterium isolated from methanogenic sludge treating wastewater from terephthalate manufacturing. Arch Microbiol 179:242–249
Qiu LY, Sekiguchi Y, Hanada S, Imachi H, Tseng IC, Cheng SS, Ohashi A, Harada H, Kamagata Y (2006) Pelotomaculum terephthalicum sp. nov. and Pelotomaculum isophthalicum sp. nov.: two anaerobic bacteria that degrade phthalate isomers in syntrophic association with hydrogenotrophic methanogens. Arch Microbiol 185:172–182
Rabus R (2005) Functional genomics of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Appl Microbiol Biotechnol 68:580–587
Rakoczy J, Schleinitz KM, Müller N, Richnow HH, Vogt C (2011) Effects of hydrogen and acetate on benzene mineralisation under sulphate-reducing conditions. FEMS Microbiol Ecol 77:238–247
Rodrigue S, Malmstrom RR, Berlin AM, Birren BW, Henn MR, Chisholm SW (2009) Whole genome amplification and de novo assembly of single bacterial cells. PLoS One 4:e6864
Rui J, Qiu Q, Lu Y (2011) Syntrophic acetate oxidation under thermophilic methanogenic condition in Chinese paddy field soil. FEMS Microbiol Ecol 77:264–273
Sakai N, Kurisu F, Yagi O, Nakajima F, Yamamoto K (2009) Identification of putative benzene-degrading bacteria in methanogenic enrichment cultures. J Biosci Bioeng 108:501–507
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
Schlüter A, Bekel T, Diaz NN, Dondrup M, Eichenlaub R, Gartemann KH, Krahn I, Krause L, Kromeke H, Kruse O, Mussgnug JH, Neuweger H, Niehaus K, Pühler A, Runte KJ, Szczepanowski R, Tauch A, Tilker A, Viehover P, Goesmann A (2008) The metagenome of a biogas-producing microbial community of a production-scale biogas plant fermenter analysed by the 454-pyrosequencing technology. J Biotechnol 136:77–90
Scholz MB, Lo C-C, Chain PSG (2012) Next generation sequencing and bioinformatic bottlenecks: the current state of metagenomic data analysis. Curr Opin Biotechnol 23:9–15
Schwarz JI, Lueders T, Eckert W, Conrad R (2007) Identification of acetate-utilizing Bacteria and Archaea in methanogenic profundal sediments of Lake Kinneret (Israel) by stable isotope probing of rRNA. Environ Microbiol 9:223–237
Selesi D, Meckenstock RU (2009) Anaerobic degradation of the aromatic hydrocarbon biphenyl by a sulfate-reducing enrichment culture. FEMS Microbiol Ecol 68:86–93
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
Simon C, Daniel R (2009) Achievements and new knowledge unraveled by metagenomic approaches. Appl Microbiol Biotechnol 85:265–276
Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77:1153–1161
Smith RJ, Jeffries TC, Roudnew B, Fitch AJ, Seymour JR, Delpin MW, Newton K, Brown MH, Mitchell JG (2011) Metagenomic comparison of microbial communities inhabiting confined and unconfined aquifer ecosystems. Environ Microbiol 14:240–253
Song B, Ward BB (2005) Genetic diversity of benzoyl coenzyme A reductase genes detected in denitrifying isolates and estuarine sediment communities. Appl Environ Microbiol 71:2036–2045
Staats M, Braster M, Röling WF (2011) Molecular diversity and distribution of aromatic hydrocarbon-degrading anaerobes across a landfill leachate plume. Environ Microbiol 13:1216–1227
Stelzer N, Buning C, Pfeifer F, Dohrmann AB, Tebbe CC, Nijenhuis I, Kästner M, Richnow HH (2006) In situ microcosms to evaluate natural attenuation potentials in contaminated aquifers. Org Geochem 37:1394–1410
Stepanauskas R, Sieracki ME (2007) Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc Nat Acad Sci USA 104:9052–9057
Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Medigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJ, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MS, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794
Sueoka K, Satoh H, Onuki M, Mino T (2009) Microorganisms involved in anaerobic phenol degradation in the treatment of synthetic coke-oven wastewater detected by RNA stable-isotope probing. FEMS Microbiol Lett 291:169–174
Sun W, Cupples AM (2011) Diversity of five anaerobic toluene degrading microbial communities investigated using stable isotope probing (SIP). Appl Environ Microbiol 78:972–980
Tamaki H, Zhang R, Angly FE, Nakamura S, Hong PY, Yasunaga T, Kamagata Y, Liu WT (2011) Metagenomic analysis of DNA viruses in a wastewater treatment plant in tropical climate. Environ Microbiol 14:441–452
Taubert M, Baumann S, von Bergen M, Seifert J (2011) Exploring the limits of robust detection of incorporation of 13C by mass spectrometry in protein-based stable isotope probing (protein-SIP). Anal Bioanal Chem 401:1975–1982
Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810
Tyson GW, Lo I, Baker BJ, Allen EE, Hugenholtz P, Banfield JF (2005) Genome-directed isolation of the key nitrogen fixer Leptospirillum ferrodiazotrophum sp. nov. from an acidophilic microbial community. Appl Environ Microbiol 71:6319–6324
Uhlik O, Jecna K, Leigh MB, Mackova M, Macek T (2009) DNA-based stable isotope probing: a link between community structure and function. Sci Total Environ 407:3611–3619
Ulrich AC, Edwards EA (2003) Physiological and molecular characterization of anaerobic benzene-degrading mixed cultures. Environ Microbiol 5:92–102
Van der Zaan BM, Saia FT, Stams AJM, Plugge CM, de Vos WM, Smidt H, Langenhoff AAM, Gerritse J (2012) Anaerobic benzene degradation under denitrifying conditions: Peptococcaceae as dominant benzene degraders and evidence for a syntrophic process. Environ Microbiol. doi:10.1111/j.1462-2920.2012.02697.x
VerBerkmoes NC, Denef VJ, Hettich RL, Banfield JF (2009) Systems biology: functional analysis of natural microbial consortia using community proteomics. Nat Rev Microbiol 7:196–205
Vogt C, Gödeke S, Treutler HC, Weiss H, Schirmer M, Richnow HH (2007) Benzene oxidation under sulfate-reducing conditions in columns simulating in situ conditions. Biodegradation 18:625–636
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
Vogt C, Kleinsteuber S, Richnow HH (2011) Anaerobic benzene degradation by bacteria. Microb Biotechnol 4:710–724
Wallrabenstein C, Gorny N, Springer N, Ludwig W, Schink B (1995) Pure culture of Syntrophus buswellii, definition of its phylogenetic status, and description of Syntropus gentianae sp. nov. Syst Appl Microbiol 18:62–66
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Wang Y, Hammes F, De Roy K, Verstraete W, Boon N (2010) Past, present and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol 28:416–424
Warnecke F, Hugenholtz P (2007) Building on basic metagenomics with complementary technologies. Genome Biol 8:231
Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565
Washer CE, Edwards EA (2007) Identification and expression of benzylsuccinate synthase genes in a toluene-degrading methanogenic consortium. Appl Environ Microbiol 73:1367–1369
Weelink SAB, van Doesburg W, Saia FT, Rijpstra WIC, Röling WFM, Smidt H, Stams AJM (2009) A strictly anaerobic betaproteobacterium Georgfuchsia toluolica gen. nov., sp. nov. degrades aromatic compounds with Fe(III), Mn(IV) or nitrate as an electron acceptor. FEMS Microbiol Ecol 70:575–585
Weelink SAB, Eekert MHA, Stams AJM (2010) Degradation of BTEX by anaerobic bacteria: physiology and application. Rev Environ Sci Bio/Technol 9:359–385
Weiss JV, Cozzarelli IM (2008) Biodegradation in contaminated aquifers: incorporating microbial/molecular methods. Ground Water 46:305–322
Whiteley AS, Manefield M, Lueders T (2006) Unlocking the ‘microbial black box’ using RNA-based stable isotope probing technologies. Curr Opin Biotechnol 17:67–71
Wilkins MJ, Verberkmoes NC, Williams KH, Callister SJ, Mouser PJ, Elifantz H, N'Guessan AL, Thomas BC, Nicora CD, Shah MB, Abraham P, Lipton MS, Lovley DR, Hettich RL, Long PE, Banfield JF (2009) Proteogenomic monitoring of Geobacter physiology during stimulated uranium bioremediation. Appl Environ Microbiol 75:6591–6599
Williams KH, Long PE, Davis JA, Wilkins MJ, N'Guessan AL, Steefel CI, Yang L, Newcomer D, Spane FA, Kerkhof LJ, McGuinness L, Dayvault R, Lovley DR (2011) Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater. Geomicrobiol J 28:519–539
Wilmes P, Bond PL (2009) Microbial community proteomics: elucidating the catalysts and metabolic mechanisms that drive the Earth's biogeochemical cycles. Curr Opin Microbiol 12:310–317
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
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
Winderl C, Penning H, 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 4:1314–1325
Wischgoll S, Heintz D, Peters F, Erxleben A, Sarnighausen E, Reski R, Van Dorsselaer A, Boll M (2005) Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens. Mol Microbiol 58:1238–1252
Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W, Lapidus A, Wu D, McCutcheon JP, McDonald BR, Moran NA, Bristow J, Cheng JF (2010) One bacterial cell, one complete genome. PLoS One 5:e10314
Yagi JM, Suflita JM, Gieg LM, DeRito CM, Jeon CO, Madsen EL (2010) Subsurface cycling of nitrogen and anaerobic aromatic hydrocarbon biodegradation revealed by nucleic acid and metabolic biomarkers. Appl Environ Microbiol 76:3124–3134
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 Reports 3:125–135
Zhang T, Ke SZ, Liu Y, Fang HP (2005) Microbial characteristics of a methanogenic phenol-degrading sludge. Water Sci Technol 52:73–78
Zhang S, Wang Q, Xie S (2011) Stable isotope probing identifies anthracene degraders under methanogenic conditions. Biodegradation. doi:10.1007/s10532-011-9501-1
Zwolinski MD, Harris RF, Hickey WJ (2000) Microbial consortia involved in the anaerobic degradation of hydrocarbons. Biodegradation 11:141–158
Acknowledgments
This work is integrated in the internal research and development program of the UFZ as well as the SAFIRA project (Remediation research in regionally contaminated aquifers) and the CITE program (Chemicals in the environment).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kleinsteuber, S., Schleinitz, K.M. & Vogt, C. Key players and team play: anaerobic microbial communities in hydrocarbon-contaminated aquifers. Appl Microbiol Biotechnol 94, 851–873 (2012). https://doi.org/10.1007/s00253-012-4025-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-012-4025-0