Molecular analysis of the metabolic rates of discrete subsurface populations of sulfate reducers

Applied and Environmental Microbiology

Volumn 77, Issue 18, 2011, Pages 6502-6509

  Miletto, M ^a   Williams, K H ^b   N'Guessan, A L ^c   Lovley, D R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVIRONMENTAL PERTURBATIONS; FIELD EXPERIMENT; IN-SITU; INDIVIDUAL CELLS; METABOLIC ACTIVITY; METABOLIC RATES; MOLECULAR ANALYSIS; PURE CULTURE; RELATIVE RATES; SEDIMENTARY ENVIRONMENT; SULFATE REDUCING; SULFATE-REDUCER; SULFITE REDUCTASE;

ANOXIC SEDIMENTS; CELL CULTURE; GROUNDWATER; GROUNDWATER POLLUTION; METABOLISM; PHYSIOLOGY; URANIUM; VOLATILE FATTY ACIDS;

GENE EXPRESSION;

BACTERIAL DNA; HYDROGEN SULFITE REDUCTASE; SULFATE;

ABUNDANCE; ACETATE; ANOXIC CONDITIONS; BACTERIUM; CELL ORGANELLE; CORRELATION; DISCRETE CHOICE ANALYSIS; EXPERIMENTAL STUDY; FIELD METHOD; GENE EXPRESSION; GROUNDWATER POLLUTION; METABOLISM; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; PERTURBATION; PHYLOGENETICS; POPULATION STRUCTURE; SPECIES DIVERSITY; SULFATE; URANIUM;

ARTICLE; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DELTAPROTEOBACTERIA; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION;

BIODIVERSITY; DELTAPROTEOBACTERIA; DNA, BACTERIAL; GENE EXPRESSION PROFILING; HYDROGENSULFITE REDUCTASE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SULFATES; WATER MICROBIOLOGY;

DESULFOBACTERACEAE; DESULFOBULBACEAE; SYNTROPHACEAE;

EID: 80052856931     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00576-11     Document Type: Article

References (64)

1. Anderson, R. T., and D. R. Lovley. 2000. Anaerobic bioremediation of benzene under sulfate-reducing conditions in a petroleum-contaminated aquifer. Environ. Sci. Technol. 34:2261-2266.
2. Anderson, R. T., et al. 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl. Environ. Microbiol. 69:5884-5891.
3. Baker, B. J., et al. 2003. Related assemblages of sulphate-reducing bacteria associated with ultradeep gold mines of South Africa and deep basalt aquifers of Washington State. Environ. Microbiol. 5:267-277.
4. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and D. L. Wheeler. 2005. GenBank. Nucleic Acids Res. 33:D34-D38.
5. Callister, S. J., et al. 2010. Analysis of biostimulated microbial communities from two field experiments reveals temporal and spatial differences in proteome profiles. Environ. Sci. Technol. 44:8897-8903.
6. Castro, H., S. Newman, K. R. Reddy, and A. Ogram. 2005. Distribution and stability of sulfate-reducing prokaryotic and hydrogenotrophic methanogenic assemblages in nutrient-impacted regions of the Florida Everglades. Appl. Environ. Microbiol. 71:2695-2704.
7. Castro, H., K. R. Reddy, and A. Ogram. 2002. Composition and function of sulfate-reducing prokaryotes in eutrophic and pristine areas of the Florida Everglades. Appl. Environ. Microbiol. 68:6129-6137.
8. Chandler, D. P., et al. 2010. Monitoring microbial community structure and dynamics during in situ U(VI) bioremediation with a field-portable microarray analysis system. Environ. Sci. Technol. 44:5516-5522.
9. Chang, Y. J., et al. 2001. Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl. Environ. Microbiol. 67:3149-3160.
10. Chin, K. J., M. L. Sharma, L. A. Russell, K. R. O'Neill, and D. R. Lovley. 2008. Quantifying expression of a dissimilatory (bi)sulfite reductase gene in petroleum-contaminated marine harbor sediments. Microb. Ecol. 55:489-499.
11. Cottrell, M. T., and S. C. Cary. 1999. Diversity of dissimilatory bisulfite reductase genes of bacteria associated with the deep-sea hydrothermal vent polychaete annelid Alvinella pompejana. Appl. Environ. Microbiol. 65:1127-1132.
12. Crane, B. R., L. M. Siegel, and E. D. Getzoff. 1995. Sulfite reductase structure at 1.6 Å: evolution and catalysis for reduction of inorganic anions. Science 270:59-67.
13. Dubilier, N., et al. 2001. Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411:298-302.
14. Finneran, K. T., R. T. Anderson, K. P. Nevin, and D. R. Lovley. 2002. Potential for bioremediation of uranium-contaminated aquifers with microbial U(VI) reduction. Soil Sediment Contam. 11:339-357.
15. Friedrich, M. W. 2002. Phylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulfate reductase genes among sulfate-reducing microorganisms. J. Bacteriol. 184:278-289.
16. García, C., D. A. Moreno, A. Ballester, M. L. Blázquez, and F. González. 2001. Bioremediation of an industrial acid mine water by metal-tolerant sulphate-reducing bacteria. Miner. Eng. 14:997-1008.
17. Garrity, G. M., J. A. Bell, and T. G. Lilburn. 2004. Taxonomic outline of the prokaryotes. Bergey's manual of systematic bacteriology, 2nd ed. Springer, New York, NY.
18. Geets, J., et al. 2006. Column experiments to assess the effects of electron donors on the efficiency of in situ precipitation of Zn, Cd, Co and Ni in contaminated groundwater applying the biological sulfate removal technology. Environ. Sci. Pollut. Res. 13:362-378.
19. Holmes, D. E., et al. 2008. Genes for two multicopper proteins required for Fe(III) oxide reduction in Geobacter sulfurreducens have different expression patterns both in the subsurface and on energy-harvesting electrodes. Microbiology 154:1422-1435.
20. Holmes, D. E., K. P. Nevin, and D. R. Lovley. 2004. In situ expression of nifD in Geobacteraceae in subsurface sediments. Appl. Environ. Microbiol. 70:7251-7259.
21. Holmes, D. E., et al. 2005. Potential for quantifying expression of the Geobacteraceae citrate synthase gene to assess the activity of Geobacteraceae in the subsurface and on current-harvesting electrodes. Appl. Environ. Microbiol. 71:6870-6877.
22. Karr, E. A., et al. 2005. Diversity and distribution of sulfate-reducing bacteria in permanently frozen Lake Fryxell, McMurdo Dry Valleys, Antarctica. Appl. Environ. Microbiol. 71:6353-6359.
23. King, J. K., S. M. Harmon, T. T. Fu, and J. B. Gladden. 2002. Mercury removal, methylmercury formation, and sulfate-reducing bacteria profiles in wetland mesocosms. Chemosphere 46:859-870.
24. Kjeldsen, K. U., et al. 2007. Diversity of sulfate-reducing bacteria from an extreme hypersaline sediment, Great Salt Lake (Utah). FEMS Microbiol. Ecol. 60:287-298.
25. Kleikemper, J., et al. 2002. Activity and diversity of sulfate-reducing bacteria in a petroleum hydrocarbon-contaminated aquifer. Appl. Environ. Microbiol. 68:1516-1523.
26. Leloup, J., et al. 2007. Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea. Environ. Microbiol. 9:131-142.
27. Leloup, J., L. Quillet, T. Berthe, and F. Petit. 2006. Diversity of the dsrAB (dissimilatory sulfite reductase) gene sequences retrieved from two contrasting mudflats of the Seine estuary, France. FEMS Microbiol. Ecol. 55:230-238.
28. Lovley, D. R., E. J. P. Phillips, Y. A. Gorby, and E. R. Landa. 1991. Microbial reduction of uranium. Nature 350:413-416.
29. Lovley, D. R., E. E. Roden, E. J. P. Phillips, and J. C. Woodward. 1993. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar. Geol. 113:41-53.
30. Loy, A., K. Kusel, A. Lehner, H. L. Drake, and M. Wagner. 2004. Microarray and functional gene analyses of sulfate-reducing prokaryotes in low-sulfate, acidic fens reveal cooccurrence of recognized genera and novel lineages. Appl. Environ. Microbiol. 70:6998-7009.
31. Ludwig, W., et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
32. Miletto, M., R. Loeb, A. M. Antheunisse, P. L. E. Bodelier, and H. J. Laanbroek. 2010. Response of the sulfate-reducing community to the re- establishment of estuarine conditions in two contrasting soils: a mesocosm approach. Microb. Ecol. 59:109-120.
33. Miletto, M., et al. 2008. Biogeography of sulfate-reducing prokaryotes in river floodplains. FEMS Microbiol. Ecol. 64:395-406.
34. Mouser, P. J., et al. 2009. Quantifying expression of Geobacter spp. oxidative stress genes in pure culture and during in situ uranium bioremediation. ISME J. 3:454-465.
35. Mouser, P. J., et al. 2009. Influence of heterogeneous ammonium availability on bacterial community structure and the expression of nitrogen fixation and ammonium transporter genes during in situ bioremediation of uranium-contaminated groundwater. Environ. Sci. Technol. 43:4386-4392.
36. Nakagawa, T., and M. Fukui. 2003. Molecular characterization of community structures and sulfur metabolism within microbial streamers in Japanese hot springs. Appl. Environ. Microbiol. 69:7044-7057.
37. Neria-Gonzalez, I., E. T. Wang, F. Ramirez, J. M. Romero, and C. Hernan- dez-Rodriguez. 2006. Characterization of bacterial community associated to biofilms of corroded oil pipelines from the southeast of Mexico. Anaerobe 12:122-133.
38. Nevin, K. P., and D. R. Lovley. 2002. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19:141-159.
39. N'Guessan A. L., et al. 2010. Molecular analysis of phosphate limitation in Geobacteraceae during the bioremediation of a uranium-contaminated aquifer. ISME J. 4:253-266.
40. O'Neil, R. A., et al. 2008. Gene transcript analysis of assimilatory iron limitation in Geobacteraceae during groundwater bioremediation. Environ. Microbiol. 10:1218-1230.
41. Oude Elferink, S. J. W. H., W. M. Akkermans-van Vliet, J. J. Bogte, and A. J. M. Stams. 1999. Desulfobacca acetoxidans gen. nov., sp. nov., a novel acetate-degrading sulfate reducer isolated from sulfidogenic granular sludge. Int. J. Syst. Bacteriol. 49:345-350.
42. Oude Elferink, S. J. W. H., A. Visser, L. W. H. Pol, and A. J. M. Stams. 1994. Sulfate reduction in methanogenic bioreactors. FEMS Microbiol. Rev. 15: 119-136.
43. Peduzzi, S., M. Tonolla, and D. Hahn. 2003. Isolation and characterization of aggregate-forming sulfate-reducing and purple sulfur bacteria from the chemocline of meromictic Lake Cadagno, Switzerland. FEMS Microbiol. Ecol. 45:29-37.
44. Pérez-Jiménez, J. R., and L. J. Kerkhof. 2005. Phylogeography of sulfate-reducing bacteria among disturbed sediments, disclosed by analysis of the dissimilatory sulfite reductase genes (dsrAB). Appl. Environ. Microbiol. 71:1004-1011.
45. Pester, M., N. Bittner, P. Deevong, M. Wagner, and A. Loy. 2010. A "rare biosphere" microorganism contributes to sulfate reduction in a peatland. ISME J. 4:1591-1602.
46. Phillips, E. J. P., E. R. Landa, and D. R. Lovley. 1995. Remediation of uranium-contaminated soils with bicarbonate extraction and microbial U(VI) reduction. J. Ind. Microbiol. 14:203-207.
47. Rabus, R., T. Hansen, and F. Widdel. 2006. Dissimilatory sulfate- and sulfur-reducing prokaryotes, p. 659-768. In M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt (ed.), The prokaryotes, 3rd ed. Springer, New York, NY.
48. Rowan, A. K., et al. 2003. Composition and diversity of ammonia-oxidising bacterial communities in wastewater treatment reactors of different design treating identical wastewater. FEMS Microbiol. Ecol. 43:195-206.
49. Schmalenberger, A., H. L. Drake, and K. Kusel. 2007. High unique diversity of sulfate-reducing prokaryotes characterized in a depth gradient in an acidic fen. Environ. Microbiol. 9:1317-1328.
50. Seth, A. D., and R. G. J. Edyvean. 2006. The function of sulfate-reducing bacteria in corrosion of potable water mains. Int. Biodeterior. Biodegradation 58:108-111.
51. Smith, S. W., R. Overbeek, C. R. Woese, W. Gilbert, and P. M. Gillevet. 1994. The Genetic Data Environment (GDE): an expandable GUI for multiple sequence analysis. Comput. Appl. Biosci. 10:671-675.
52. Stubner, S. 2004. Quantification of Gram-negative sulphate-reducing bacte- ria in rice field soil by 16S rRNA gene-targeted real-time PCR. J. Microbiol. Methods 57:219-230.
53. Suzuki, Y., S. D. Kelly, K. M. Kemner, and J. F. Banfield. 2004. Enzymatic U(VI) reduction by Desulfosporosinus species. Radiochimica Acta 92:11-16.
54. Tebo, B. M., and A. Y. Obraztsova. 1998. Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol. Lett. 162:193-198.
55. Teske, A., C. Wawer, G. Muyzer, and N. B. Ramsing. 1996. Distribution of sulfate-reducing bacteria in a stratified fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl. Environ. Microbiol. 62:1405-1415.
56. Vile, M. A., S. D. Bridgham, R. K. Wieder, and M. Novák. 2003. Atmospheric sulfur deposition alters pathways of gaseous carbon production in peatlands. Global Biogeochem. Cycles 17:1058-1064.
57. Villanueva, L., S. A. Haveman, Z. M. Summers, and D. R. Lovley. 2008. Quantification of Desulfovibrio vulgaris dissimilatory sulfite reductase gene expression during electron donor- and electron acceptor-limited growth. Appl. Environ. Microbiol. 74:5850-5853.
58. Vrionis, H. A., et al. 2005. Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site. Appl. Environ. Microbiol. 71: 6308-6318.
59. Wagner, M., A. J. Roger, J. L. Flax, G. A. Brusseau, and D. A. Stahl. 1998. Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J. Bacteriol. 180:2975-2982.
60. Wendt-Potthoff, K., and M. Koschorreck. 2002. Functional groups and ac- tivities of bacteria in a highly acidic volcanic mountain stream and lake in Patagonia, Argentina. Microb. Ecol. 43:92-106.
61. Widdel, F. 1987. New types of acetate-oxidizing, sulfate-reducing Desulfo- bacter species, D. hydrogenophilus sp. nov., D. latus sp. nov., and D. curvatus sp. nov. Arch. Microbiol. 148:286-291.
62. Williams, K. H., et al. 2011. Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater. Geomicrobiol. J. 28:519-539.
63. Zhuang, K., et al. 2011. Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J. 5:305-316.
64. Zverlov, V., et al. 2005. Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. J. Bacteriol. 187:2203-2208.