Depth-resolved quantification of anaerobic toluene degraders and aquifer microbial community patterns in distinct redox zones of a tar oil contaminant plume

Applied and Environmental Microbiology

Volumn 74, Issue 3, 2008, Pages 792-801

  Winded, Christian ^a   Anneser, Bettina ^a   Griebler, Christian ^a   Meckenstock, Rainer U ^a   Lueders, Tillmann ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AQUIFERS; BIODEGRADATION; GENES; MICROBIOLOGY;

BIOGEOCHEMICAL GRADIENT ZONE; MICROBIAL DEGRADATION; SULFATE REDUCTION; TAR OIL CONTAMINANT PLUME;

TOLUENE;

BENZENE; ETHYLBENZENE; GROUND WATER; RNA 16S; TAR; TOLUENE; XYLENE;

AQUIFER CHARACTERIZATION; BIODEGRADATION; BTEX; MICROBIAL COMMUNITY; NATURAL ATTENUATION; PLUME; POLYMERASE CHAIN REACTION; REDOX CONDITIONS;

ANAEROBIC METABOLISM; AQUIFER; ARTICLE; CLOSTRIDIA; DESULFOCAPSA; GEOBACTER; MICROBIAL ATTENUATION; MICROBIAL DEGRADATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLUME; PROTEOBACTERIA; QUANTITATIVE ANALYSIS; SEDIMENTIBACTER; WATER CONTAMINATION;

BACTERIA, ANAEROBIC; BENZENE DERIVATIVES; BIODEGRADATION, ENVIRONMENTAL; CARBON-CARBON LYASES; DELTAPROTEOBACTERIA; ECOSYSTEM; FRESH WATER; IRON; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SULFATES; TOLUENE; WATER POLLUTANTS, CHEMICAL; WATER SUPPLY;

BACTERIA (MICROORGANISMS); DESULFOCAPSA; GEOBACTER; SEDIMENTIBACTER;

EID: 38949131277     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01951-07     Document Type: Article

References (60)

1. Allen, J. P., E. A. Atekwana, E. A. Atekwana, J. W. Duris, D. D. Werkema, and S. Rossbach. 2007. The microbial community structure in petroleum-contaminated sediments corresponds to geophysical signatures. Appl. Environ. Microbiol. 73:2860-2870.
2. Anderson, R. T., and D. R. Lovley. 1997. Ecology and biogeochemistry of in situ groundwater bioremediation. Adv. Microb. Ecol. 15:289-350.
3. Anneser, B., F. Einsiedl, R. U. Meckenstock, L. Richters, F. Wisotzky, and C. Griebler. High-resolution monitoring of biogeochemical gradients in a taroil contaminated aquifer. Appl. Geochem., in press.
4. Bauer, R. D., Y. Zhang, P. Maloszewski, R. U. Meckenstock, and C. Griebler. Aerobic and anaerobic degradation in anoxic toluene plumes - 2D microcosm studies. J. Contam. Hydrol., in press.
5. Bekins, B. A., I. M. Cozzarelli, E. M. Godsy, E. Warren, H. I. Essaid, and M. E. Tuccillo. 2001. Progression of natural attenuation processes at a crude oil spill site. II. Controls on spatial distribution of microbial populations. J. Contam. Hydrol. 53:387-406.
6. Beller, H. R., S. R. Kane, T. C. Legler, and P. J. Alvarez. 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.
7. Breitenstein, A., J. Wiegel, C. Haertig, N. Weiss, J. R. Andreesen, and U. Lechner. 2002. Reclassification of Clostridium hydroxybenzoicum as Sedimentibacter hydroxybenzoicus gen. nov., comb, nov., and description of Sedimentibacter saalensis sp. nov. Int. J. Syst. Evol. Microbiol. 52:801-807.
8. Caccavo, F., Jr., D. J. Lonergan, D. R. Lovley, M. Davis, J. F. Stolz, and M. J. McInerney. 1994. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 60:3752-3759.
9. Christensen, T. H., P. L. Bjerg, S. A. Banwart, R. Jakobsen, G. Heron, and H. J. Albrechtsen. 2000. Characterization of redox conditions in groundwater contaminant plumes. J. Contam. Hydrol. 45:165-241.
10. Coates, J. D., V. K. Bhupathiraju, L. A. Achenbach, M. J. McInerney, and D. R. Lovley. 2001. Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int. J. Syst. Evol. Microbiol. 51:581-588.
11. Coates, J. D., E. J. P. Phillips, D. J. Lonergan, H. Jenter, and D. R. Lovley. 1996. Isolation of Geobacter species from diverse sedimentary environments. Appl. Environ. Microbiol. 62:1531-1536.
12. Cozzarelli, I. M., B. A. Bekins, M. J. Baedecker, G. R. Aiken, R. P. Eganhouse, and M. E. Tuccillo. 2001. Progression of natural attenuation processes at a crude-oil spill site. I. Geochemical evolution of the plume. J. Contam. Hydrol. 53:369-385.
13. Dojka, M. A., P. Hugenholtz, S. K. Haack, and N. R. Pace. 1998. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64:3869-3877.
14. Eckert, P., F. Wisotzky, P. Obermann, O. Kracht, and H. Strauss. 2000. Natural bioattenuation and active remediation in a BTEX contaminated aquifer in Duesseldorf (Germany), p. 389-399. In P. L. Bjerg, P. Engesgaard, and T. D. Krom (ed.), Groundwater 2000. Balkema, Rotterdam, The Netherlands.
15. Egert, M., and M. W. Friedrich. 2003. Formation of pseudo-terminal restriction fragments, a PCR-related bias affecting terminal restriction fragment length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol. 69:2555-2562.
16. Franzmann, P. D., W. J. Robertson, L. R. Zappia, and G. B. Davis. 2002. The role of microbial populations in the containment of aromatic hydrocarbons in the subsurface. Biodegradation 13:65-78.
17. Griffiths, R. I., A. S. Whiteley, A. G. O'Donnell, and M. J. Bailey. 2000. Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl. Environ. Microbiol. 66:5488-5491.
18. Haack, S. K., L. R. Fogarty, T. G. West, E. W. Alm, J. T. McGuire, D. T. Long, D. W. Hyndman, and L. J. Forney. 2004. Spatial and temporal changes in microbial community structure associated with recharge-influenced chemical gradients in a contaminated aquifer. Environ. Microbiol. 6:438-448.
19. Hill, T. C. J., K. A. Walsh, J. A. Harris, and B. F. Moffett. 2003. Using ecological diversity measures with bacterial communities. FEMS Microbiol. Ecol. 43:1-11.
20. Kane, S. R., H. R. Beller, T. C. Legler, and R. T. Anderson. 2002. Biochemical and genetic evidence of benzylsuccinate synthase in toluene-degrading, ferric iron-reducing Geobacter metallireducens. Biodegradation 13:149-154.
21. Kitts, C. L. 2001. Terminal restriction fragment patterns: a tool for comparing microbial communities and assessing community dynamics. Curr. Issues Intest. Microbiol. 2:17-25.
22. Krieger, C. J., H. R. Beller, M. Reinhard, and A. M. Spormann. 1999. Initial reactions in anaerobic oxidation of m-xylene by the denitrifying bacterium Azoarcus sp. strain T. J. Bacteriol. 181:6403-6410.
23. Kube, M., J. Heider, J. Amann, P. Hufnagel, S. Kuhner, A. Beck, R. Reinhardt, and R. Rabus. 2004. Genes involved in the anaerobic degradation of toluene in a denitrifying bacterium, strain EbN1. Arch. Microbiol. 181:182-194.
24. Lerner, D. N., S. F. Thornton, M. J. Spence, S. A. Banwart, S. H. Bottrell, J. J. Higgo, H. E. H. Mallinson, R. W. Pickup, and G. M. Williams. 2000. Ineffective natural attenuation of degradable organic compounds in a phenol-contaminated aquifer. Ground Water 38:922-928.
25. Leuthner, B., C. Leutwein, H. Schulz, P. Horth, W. Haehnel, E. Schiltz, H. Schagger, and J. Heider. 1998. Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol. Microbiol. 28:615-628.
26. Liebich, D., M. Rosenberg, J. Schaefer, and H. Juette. 2000. Sanierung einer ehemaligen Gaskokerei in Düsseldorf. TerraTech 2:21-25.
27. Lin, B., M. Braster, B. M. van Breukelen, H. W. van Verseveld, H. V. Westerhoff, and W. F. M. Röling. 2005. Geobacteraceae community composition is related to hydrochemistry and biodegradation in an iron-reducing aquifer polluted by a neighboring landfill. Appl. Environ. Microbiol. 71:5983-5991.
28. Liu, W. T., T. L. Marsh, H. Cheng, and L. J. Forney. 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63:4516-4522.
29. Lovley, D. R. 1997. Microbial Fe(III) reduction in subsurface environments. FEMS Microbiol. Rev. 20:305-313.
30. Lovley, D. R., S. J. Giovannoni, D. C. White, J. E. Champine, E. J. P. Phillips, Y. A. Gorby, and S. Goodwin. 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.
31. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
32. Lueders, T., and M. W. Friedrich. 2002. Effects of amendment with ferrihydrite and gypsum on the structure and activity of methanogenic populations in rice field soil. Appl. Environ. Microbiol. 68:2484-2494.
33. Lueders, T., and M. W. Friedrich. 2003. Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl. Environ. Microbiol. 69:320-326.
34. Lueders, T., R. Kindler, A. Miltner, M. W. Friedrich, and M. Kaestner. 2006. Identification of bacterial micropredators distinctively active in a soil microbial food web. Appl. Environ. Microbiol. 72:5342-5348.
35. Lueders, T., M. Manefield, and M. W. Friedrich. 2004. Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ. Microbiol. 6:73-78.
36. Lukow, T., P. F. Dunfield, and W. Liesack. 2000. Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and nontransgenic potato plants. FEMS Microbiol. Ecol. 32:241-247.
37. McGuire, J. T., D. T. Long, and D. W. Hyndman. 2005. Analysis of recharge-induced geochemical change in a contaminated aquifer. Ground Water 43: 518-530.
38. Meckenstock, R. U. 1999. Fermentative toluene degradation in anaerobic defined syntrophic cocultures. FEMS Microbiol. Lett. 177:67-73.
39. Mouser, P. J., D. M. Rizzo, W. F. M. Röling, and B. M. van Breukelen. 2005. A multivariate statistical approach to spatial representation of groundwater contamination using hydrochemistry and microbial community profiles. Environ. Sci. Technol. 39:7551-7559.
40. Muyzer, G., A. Teske, C. O. Wirsen, and H. W. Jannasch. 1995. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch. Microbiol. 164:165-172.
41. Osborn, A. M., E. R. B. Moore, and K. N. Timmis. 2000. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ. Microbiol. 2:39-50.
42. Rabus, R., M. Kube, J. Heider, A. Beck, K. Heitmann, F. Widdel, and R. Reinhardt. 2005. The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch. Microbiol. 183:27-36.
43. Ramakrishnan, B., T. Lueders, P. F. Dunfield, R. Conrad, and M. W. Friedrich. 2001. Archaeal community structures in rice soils from different geographical regions before and after initiation of methane production. FEMS Microbiol. Ecol. 37:175-186.
44. Rappé, M. S., and S. J. Giovannoni. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369-394.
45. Robertson, W. J., J. P. Bowman, P. D. Franzmann, and B. J. Mee. 2001. Desulfosporosinus meridiei sp. nov., a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwater. Int. J. Syst. Evol. Microbiol. 51:133-140.
46. Röling, W. F., and H. W. van Verseveld. 2002. Natural attenuation: what does the subsurface have in store? Biodegradation 13:53-64.
47. Schryver, J., C. Brandt, S. Pfiffner, A. Palumbo, A. Peacock, D. White, J. McKinley, and P. Long. 2006. Application of nonlinear analysis methods for identifying relationships between microbial community structure and groundwater geochemistry. Microb. Ecol. 51:177-188.
48. Shinoda, Y., J. Akagi, Y. Uchihashi, A. Hiraishi, H. Yukawa, H. Yurimoto, Y. Sakai, and N. Kato. 2005. Anaerobic degradation of aromatic compounds by Magnetospirillum strains: isolation and degradation genes. Biosci. Biotechnol. Biochem. 69:1483-1491.
49. Smith, R. L., R. W. Harvey, and D. R. LeBlanc. 1991. Importance of closely spaced vertical sampling in delineating chemical and microbiological gradients in groundwater studies. J. Contam. Hydrol. 7:285-300.
50. Spring, S., R. Ainann. W. Ludwig, K. H. Schleifer, H. van Gemerden, and N. Petersen. 1993. Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl. Environ. Microbiol. 59:2397-2403.
51. Stubner, S. 2002. Enumeration of 16S rDNA of Desulfotomaculum lineage 1 in rice field soil by real-time PCR with SybrGreen detection. J. Microbiol. Methods 50:155-164.
52. Thies, J. E. 2007. Soil microbial community analysis using terminal restriction fragment length polymorphisms. Soil Sci. Soc. Am. J. 71:579-591.
53. Tuxen, N., H.-J. Albrechtsen, and P. L. Bjerg. 2006. Identification of a reactive degradation zone at a landfill leachate plume fringe using high resolution sampling and incubation techniques. J. Contam. Hydrol. 85:179-194.
54. 4 oxidation. J. Contam. Hydrol. 73:181-205.
55. Washer, C. E., and E. A. Edwards. 2007. Identification and expression of benzylsuccinate synthase genes in a toluene-degrading methanogenic consortium. Appl. Environ. Microbiol. 73:1367-1369.
56. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703.
57. Wilson, R. D., S. F. Thornton, and D. M. Mackay. 2004. Challenges in monitoring the natural attenuation of spatially variable plumes. Biodegradation 15:359-369.
58. Winderl, C., S. Schaefer, and T. Lueders. 2007. Detection of anaerobic toluene and hydrocarbon degraders in contaminated aquifers using benzyl-succinate synthase (bssA) genes as a functional marker. Environ. Microbiol. 9:1035-1046.
59. Wisotzky, F., and P. Eckert. 1997. Sulfat-dominierter BTEX-Abbau im Grundwasser eines ehemaligen Gaswerksstandortes. Grundwasser 2:11-20.
60. Wöhlbrand, L., B. Kallerhoff, D. Lange, P. Hufnagel, J. Thiermann, R. Reinhardt, and R. Rabus. 2007. Functional proteomic view of metabolic regulation in "Aromatoleum aromaticum" strain EbN1. Proteomics 7:2222-2239.