Phylogenetic and Functional Diversity Within Toluene-Degrading, Sulphate-Reducing Consortia Enriched from a Contaminated Aquifer

Microbial Ecology

Volumn 68, Issue 2, 2014, Pages 222-234

  Kuppardt, Anke ^a   Kleinsteuber, Sabine ^a   Vogt, Carsten ^a   Lüders, Tillmann ^b   Harms, Hauke ^a,c   Chatzinotas, Antonis ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIA; DELTAPROTEOBACTERIA; DESULFOBULBACEAE; DESULFOSPOROSINUS;

BACTERIAL DNA; GROUND WATER; RNA 16S; TOLUENE; WATER POLLUTANT;

BACTERIAL GENE; BIOREMEDIATION; CLASSIFICATION; DELTAPROTEOBACTERIA; DNA SEQUENCE; ECOSYSTEM; GENETICS; GERMANY; GRAM NEGATIVE ANAEROBIC BACTERIA; METABOLISM; MICROBIAL CONSORTIUM; MICROBIOLOGY; PHYLOGENY; WATER POLLUTANT;

BIODEGRADATION, ENVIRONMENTAL; DELTAPROTEOBACTERIA; DNA, BACTERIAL; ECOSYSTEM; GENES, BACTERIAL; GERMANY; GROUNDWATER; MICROBIAL CONSORTIA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SULFUR-REDUCING BACTERIA; TOLUENE; WATER MICROBIOLOGY; WATER POLLUTANTS, CHEMICAL;

EID: 84904556171     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-014-0403-8     Document Type: Article

References (72)

1. Heider J, Spormann AM, Beller HR, Widdel F (1998) Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol Rev 22: 459-473. doi: 10. 1111/j. 1574-6976. 1998. tb00381. x.
2. 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. doi: 10. 1007/s00253-012-4025-0.
3. Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12: 259-276.
4. Morasch B, Schink B, Tebbe CC, Meckenstock RU (2004) Degradation of o-xylene and m-xylene by a novel sulfate-reducer belonging to the genus Desulfotomaculum. Arch Microbiol 181: 407-417.
5. 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: 1314-1325. doi: 10. 1038/ismej. 2010. 54.
6. 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. doi: 10. 1111/j. 1574-6941. 2011. 01083. x.
7. Boll M, Fuchs G, Heider J (2002) Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr Opin Chem Biol 6: 604-611.
8. 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.
9. 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.
10. Vieth A, Kästner M, Schirmer M, Weiß H, Gödeke S, Meckenstock RU, Richnow HH (2005) Monitoring in situ biodegradation of benzene and toluene by stable carbon isotope fractionation. Environ Toxicol Chem 24: 51-60. doi: 10. 1002/etc. 5620240108.
11. Fischer A, Bauer J, Meckenstock RU, Stichler W, Griebler C, Maloszewski P, Kästner M, Richnow HH (2006) A multitracer test proving the reliability of Rayleigh equation-based approach for assessing biodegradation in a BTEX contaminated aquifer. Environ Sci Technol 40: 4245-4252.
12. Fischer A, Theuerkorn K, Stelzer N, Gehre M, Thullner M, Richnow HH (2007) Applicability of stable isotope fractionation analysis for the characterization of benzene biodegradation in a BTEX-contaminated aquifer. Environ Sci Technol 41: 3689-3696. doi: 10. 1021/es061514m.
13. Schirmer M, Dahmke A, Dietrich P, Dietze M, Gödeke S, Richnow HH, Schirmer K, Weiß H, Teutsch G (2006) Natural attenuation research at the contaminated megasite Zeitz. J Hydrol 328: 393-407.
14. Alfreider A, Vogt C (2007) Bacterial diversity and aerobic biodegradation potential in a BTEX-contaminated aquifer. Water Air Soil Pollut 183: 415-426.
15. Gödeke S, Richnow HH, Weiß H, Fischer A, Vogt C, Borsdorf H, Schirmer M (2006) Multi tracer test for the implementation of enhanced in-situ bioremediation at a BTEX-contaminated megasite. J Contam Hydrol 87: 211-236. doi: 10. 1016/j. jconhyd. 2006. 05. 008.
16. 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.
17. Fischer A, Gehre M, Breitfeld J, Richnow HH, Vogt C (2009) Carbon and hydrogen isotope fractionation of benzene during biodegradation under sulfate-reducing conditions: a laboratory to field site approach. Rapid Commun Mass Spectrom 23: 2439-2447. doi: 10. 1002/rcm. 4049.
18. 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.
19. 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.
20. Taubert M, Vogt C, Wubet T, Kleinsteuber S, Tarkka MT, Harms H, Buscot F, Richnow HH, von Bergen M, Seifert J (2012) Protein-SIP enables time-resolved analysis of the carbon flux in a sulfate-reducing, benzene-degrading microbial consortium. ISME J 6: 2291-2301. doi: 10. 1038/ismej. 2012. 68.
21. Cline J (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454-458.
22. Kleinsteuber S, Riis V, Fetzer I, Harms H, Müller S (2006) Population dynamics within a microbial consortium during growth on diesel fuel in saline environments. Appl Environ Microbiol 72: 3531-3542.
23. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic Acid Tech. Bact. Syst. John Wiley & Sons, Chichester, pp 115-175.
24. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
25. 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. doi: 10. 1128/AEM. 00062-07.
26. Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319. doi: 10. 1093/bioinformatics/bth226.
27. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
28. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
29. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739. doi: 10. 1093/molbev/msr121.
30. 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.
31. Meckenstock RU (1999) Fermentative toluene degradation in anaerobic defined syntrophic cocultures. FEMS Microbiol Lett 177: 67-73. doi: 10. 1111/j. 1574-6968. 1999. tb13715. x.
32. Jehmlich N, Kleinsteuber S, Vogt C, Benndorf D, Harms H, Schmidt F, Von Bergen M, Seifert J (2010) Phylogenetic and proteomic analysis of an anaerobic toluene-degrading community. J Appl Microbiol 109: 1937-1945. doi: 10. 1111/j. 1365-2672. 2010. 04823. x.
33. Herrmann S, Vogt C, Fischer A, Kuppardt A, Richnow HH (2009) Characterization of anaerobic xylene biodegradation by two-dimensional isotope fractionation analysis. Environ Microbiol Rep 1: 535-544.
34. Callaghan AV, Davidova IA, Savage-Ashlock K, Grieg 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.
35. Yagi JM, Suflita JM, Gieg LM et al (2010) Subsurface cycling of nitrogen and anaerobic aromatic hydrocarbon biodegradation revealed by nucleic acid and metabolic biomarkers. Appl Environ Microbiol 76: 3124-3134. doi: 10. 1128/AEM. 00172-10.
36. 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. doi: 10. 1128/AEM. 02362-12.
37. Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64: 3869-3877.
38. Bombach P, Chatzinotas A, Neu TR, Kästner M, Lueders T, Vogt C (2010) 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. doi: 10. 1111/j. 1574-6941. 2009. 00809. x.
39. Müller S, Hübschmann T, Kleinsteuber S, Vogt C (2012) High resolution single cell analytics to follow microbial community dynamics in anaerobic ecosystems. Methods 57: 338-349. doi: 10. 1016/j. ymeth. 2012. 04. 001.
40. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile ε-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468. doi: 10. 1038/nrmicro1414.
41. 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. doi: 10. 1111/j. 1574-6941. 2012. 01334. x.
42. Zhang T, Ke SZ, Liu Y, Fang HP (2005) Microbial characteristics of a methanogenic phenol-degrading sludge. Water Sci Technol J Int Assoc Water Pollut Res 52: 73-78.
43. Phelps CD, Kerkhof LJ, Young LY (1998) Molecular characterization of a sulfate-reducing consortium which mineralizes benzene. FEMS Microbiol Ecol 27: 269-279.
44. Hubert CRJ, Oldenburg TBP, Fustic M, Gray ND, Larter SR, Penn K, Rowan AK, Seshadri R, Sherry A, Swainsbury R, Voordouw G, Voordouw JK, Head IM (2012) Massive dominance of Epsilonproteobacteria in formation waters from a Canadian oil sands reservoir containing severely biodegraded oil. Environ Microbiol 14: 387-404. doi: 10. 1111/j. 1462-2920. 2011. 02521. x.
45. Porter ML, Engel AS (2008) Diversity of uncultured Epsilonproteobacteria from terrestrial sulfidic caves and springs. Appl Environ Microbiol 74: 4973-4977. doi: 10. 1128/AEM. 02915-07.
46. 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. doi: 10. 1128/AEM. 00647-10.
47. Engel AS, Meisinger DB, Porter ML, Payn RA, Schmid M, Stern LA, Schleifer KH, Lee NM (2009) Linking phylogenetic and functional diversity to nutrient spiraling in microbial mats from Lower Kane Cave (USA). ISME J 4: 98-110.
48. Liang JB, Chen YQ, Lan CY, Tam NFY, Zan QJ, Huang LN (2007) Recovery of novel bacterial diversity from mangrove sediment. Mar Biol 150: 739-747.
49. Oude Elferink SJWH, Maas RN, Harmsen HJM, Stams AJM (1995) Desulforhabdus amnigenus gen. nov. sp. nov., a sulfate reducer isolated from anaerobic granular sludge. Arch Microbiol 164: 119-124.
50. Harmsen HJM, van Kuijk BLM, Plugge CM, Akkermans ADL, De Vos WM, Stams AJM (1998) Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48: 1383-1387.
51. Chen S, Liu X, Dong X (2005) Syntrophobacter sulfatireducens sp. nov., a novel syntrophic, propionate-oxidizing bacterium isolated from UASB reactors. Int J Syst Evol Microbiol 55: 1319-1324.
52. Plugge CM, Zhang W, Scholten JCM, Stams AJM (2011) Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2: 81. doi: 10. 3389/fmicb. 2011. 00081.
53. Widdel F, Hansen TA (1992) The dissimilatory sulfate- and sulfur-reducing bacteria, 2nd edn. The prokaryotes, Springer, New York, pp 583-624.
54. Diekert G, Wohlfarth G (1994) Metabolism of homoacetogens. Antonie van Leeuwenhoek 66: 209-221.
55. Grabowski A, Nercessian O, Fayolle F, Blanchet D, Jeanthon C (2005) Microbial diversity in production waters of a low-temperature biodegraded oil reservoir. FEMS Microbiol Ecol 54: 427-443. doi: 10. 1016/j. resmic. 2005. 03. 009.
56. Behrens S, Azizian MF, McMurdie PJ, Sabalowsky A, Dolan ME, Semprini L, Spormann AM (2008) Monitoring abundance and expression of "Dehalococcoides" species chloroethene-reductive dehalogenases in a tetrachloroethene-dechlorinating flow column. Appl Environ Microbiol 74: 5695-5703.
57. Macbeth TW, Cummings DE, Spring S, Petzke LM, Sorenson KS (2004) Molecular characterization of a dechlorinating community resulting from in situ biostimulation in a trichloroethene-contaminated deep, fractured basalt aquifer and comparison to a derivative laboratory culture. Appl Environ Microbiol 70: 7329-7341.
58. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJP, Gorby YA, Goodwin S (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159: 336-344.
59. Coates JD, Bhupathiraju VK, Achenbach LA, Mclnerney MJ, Lovely DR (2001) Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe (III)-reducers. Int J Syst Evol Microbiol 51: 581-588.
60. 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.
61. 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. doi: 10. 1111/j. 1574-6941. 2007. 00371. x.
62. 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, Lovely DR (2007) Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J 1: 663-677. doi: 10. 1038/ismej. 2007. 85.
63. Staats M, Braster M, Röling WFM (2011) Molecular diversity and distribution of aromatic hydrocarbon-degrading anaerobes across a landfill leachate plume. Environ Microbiol 13: 1216-1227. doi: 10. 1111/j. 1462-2920. 2010. 02421. x.
64. Ishii S, Yamamoto M, Kikuchi M, Oshima K, Hattori M, Otsuka S, Senoo K (2009) Microbial populations responsive to denitrification-inducing conditions in rice paddy soil, as revealed by comparative 16S rRNA gene analysis. Appl Environ Microbiol 75: 7070-7078.
65. 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. doi: 10. 1016/j. jbiosc. 2009. 06. 005.
66. Ramamoorthy S, Sass H, Langner H, Schumann P, Kroppenstedt RM, Spring S, Overmann J, Rosenzweig RF (2006) Desulfosporosinus lacus sp. nov., a sulfate-reducing bacterium isolated from pristine freshwater lake sediments. Int J Syst Evol Microbiol 56: 2729-2736.
67. Liu A, Garcia-Dominguez E, Rhine E, Young L (2004) A novel arsenate respiring isolate that can utilize aromatic substrates. FEMS Microbiol Ecol 48: 323-332. doi: 10. 1016/j. femsec. 2004. 02. 008.
68. Spring S, Rosenzweig F (2006) The genera Desulfitobacterium and Desulfosporosinus: taxonomy. The prokaryotes. Springer, Berlin, pp 771-786.
69. 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. doi: 10. 1111/j. 1462-2920. 2008. 01756. x.
70. Grundmann O, Behrends A, Rabus R, Amann J, Halder T, Heider J, Widdel F (2007) Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium, strain HxN1. Environ Microbiol 10: 376-385.
71. 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. doi: 10. 1111/j. 1758-2229. 2010. 00198. x.
72. 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. doi: 10. 1016/j. bbrc. 2007. 11. 094.