Microbial community changes in response to ethanol or methanol amendments for U(VI) reduction

Applied and Environmental Microbiology

Volumn 76, Issue 17, 2010, Pages 5728-5735

  Vishnivetskaya, Tatiana A ^a   Brandt, Craig C ^a   Madden, Andrew S ^b   Drake, Meghan M ^a   Kostka, Joel E ^c   Akob, Denise M ^c,d   Küsel, Kirsten ^d   Palumbo, Anthony V ^a  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; BACTERIAL COMMUNITY; BACTERIAL COMMUNITY STRUCTURE; BETAPROTEOBACTERIA; BIOREDUCTIONS; CARBON SOURCE; CONTAMINATED SITES; FIRMICUTES; LABORATORY MICROCOSM; MICROBIAL COMMUNITIES; PHYLOGENETIC DIVERSITY; SAMPLING SITE;

BACTERIOLOGY; CLONING; ETHANOL; GROUNDWATER; GROUNDWATER POLLUTION; RNA; URANIUM;

METHANOL;

ALCOHOL; BACTERIAL DNA; CARBON; METHANOL; RIBOSOME DNA; RNA 16S; URANIUM;

BACTERIUM; CARBON; CLONE; COMMUNITY STRUCTURE; ETHANOL; GENETIC ANALYSIS; METHANOL; MICROBIAL COMMUNITY; MICROCOSM; PHYLOGENETICS; URANIUM;

ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; GEOGRAPHY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY; POLLUTANT; TIME;

BACTERIA; BIODIVERSITY; CARBON; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; ENVIRONMENTAL POLLUTANTS; ETHANOL; GEOGRAPHY; METHANOL; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; TIME FACTORS; URANIUM; WATER MICROBIOLOGY;

OAK RIDGE RESERVATION; TENNESSEE; UNITED STATES;

BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; BURKHOLDERIACEAE; CLOSTRIDIUM; COMAMONADACEAE; DELTAPROTEOBACTERIA; DESULFOSPOROSINUS; FIRMICUTES; JANTHINOBACTERIUM; METHYLOPHILACEAE; METHYLOPHILALES; OXALOBACTERACEAE; POLAROMONAS; RHODOCYCLACEAE;

EID: 77956595989     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00308-10     Document Type: Article

References (72)

1. Akob, D. M., H. J. Mills, T. M. Gihring, L. Kerkhof, J. W. Stucki, A. S. Anastacio, K. J. Chin, K. Kusel, A. V. Palumbo, D. B. Watson, and J. E. Kostka. 2008. Functional diversity and electron donor dependence of microbial populations capable of U (VI) reduction in radionuclide-contaminated subsurface sediments. Appl. Environ. Microbiol. 74:3159-3170.
2. Amos, B. K., Y. Sung, K. E. Fletcher, T. J. Gentry, W. M. Wu, C. S. Criddle, J. Zhou, and F. E. Loffler. 2007. Detection and quantification of Geobacter lovleyi strain SZ: implications for bioremediation at tetrachloroethene-and uranium-impacted sites. Appl. Environ. Microbiol. 73:6898-6904.
3. Anderson, R. T., H. A. Vrionis, I. Ortiz-Bernad, C. T. Resch, P. E. Long, R. Dayvault, K. Karp, S. Marutzky, D. R. Metzler, A. Peacock, D. C. White, M. Lowe, and D. R. Lovley. 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.
4. Angly, F. E., D. Willner, A. Prieto-Davó, R. A. Edwards, R. Schmieder, R. Vega-Thurber, D. A. Antonopoulos, K. Barott, M. T. Cottrell, C. Desnues, E. A. Dinsdale, M. Furlan, M. Haynes, M. R. Henn, Y. Hu, D. L. Kirchman, T. McDole, J. D. McPherson, F. Meyer, R. M. Miller, E. Mundt, R. K. Naviaux, B. Rodriguez-Mueller, R. Stevens, L. Wegley, L. Zhang, B. Zhu, and F. Rohwer. 2009. The GAAS metagenomic tool and Its estimations of viral and microbial average genome size in four major biomes. PLoS Comput. Biol. 5: e1000593.
5. Barns, S. M., E. C. Cain, L. Sommerville, and C. R. Kuske. 2007. Acidobactetia phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl. Environ. Microbiol. 73:3113-3116.
6. Bellion, E., M. E. Kent, J. C. Aud, M. Y. Alikhan, and J. A. Bolbot. 1983. Uptake of methylamine and methanol by Pseudomonas sp. strain Am1. J. Bacteriol. 154:1168-1173.
7. Byrne-Bailey, K. G., K. A. Weber, A. H. Chair, S. Bose, T. Knox, T. L. Spanbauer, O. Chertkov, and J. D. Coates. 2010. Completed genome sequence of the anaerobic iron-oxidizing bacterium Acidovorax ebreus strain TPSY. J. Bacteriol. 192:1475-1476.
8. Cardenas, E., W. M. Wu, M. B. Leigh, J. Carley, S. Carroll, T. Gentry, J. Luo, D. Watson, B. Gu, M. Ginder-Vogel, P. K. Kitanidis, P. M. Jardine, J. Zhou, C. S. Criddle, T. L. Marsh, and J. A. Tiedje. 2008. Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl. Environ. Microbiol. 74:3718-3729.
9. Chang, Y. J., P. E. Long, R. Geyer, A. D. Peacock, C. T. Resch, K. Sublette, S. Pfiffner, A. Smithgall, R. T. Anderson, H. A. Vrionis, J. R. Stephen, R. Dayvault, I. Ortiz-Bernad, D. R. Lovley, and D. C. White. 2005. Microbial incorporation of C-13-labeled acetate at the field scale: Detection of microbes responsible for reduction of U (VI). Environ. Sci. Technol. 39:9039-9048.
10. Coates, J. D., K. A. Cole, R. Chakraborty, S. M. O'Connor, and L. A. Achenbach. 2002. Diversity and ubiquity of bacteria capable of utilizing humic substances as electron donors for anaerobic respiration. Appl. Environ. Microbiol. 68:2445-2452.
11. Coates, J. D., D. J. Ellis, C. V. Gaw, and D. R. Lovley. 1999. Geothrix fermentans gen. nov., sp nov., a novel Fe (III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int. J. Syst. Bacteriol. 49:1615-1622.
12. 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.
13. De Wever, H., J. R. Cole, M. R. Fettig, D. A. Hogan, and J. M. Tiedje. 2000. Reductive dehalogenation of trichloroacetic acid by Trichlorobacter thiogenes gen. nov., sp. nov. Appl. Environ. Microbiol. 66:2297-2301.
14. Dilling, S., F. Imkamp, S. Schmidt, and V. Muller. 2007. Regulation of caffeate respiration in the acetogenic bacterium Acetobacterium woodii. Appl. Environ. Microbiol. 73:3630-3636.
15. Drake, H. L., K. Küsel, and C. Matthies. 2006. Acetogenic prokaryotes, p. 354-420. In M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt (ed.), The prokaryotes, vol. 2. Springer-Verlag, New York, NY.
16. Ellenbroek, F. M., and T. E. Cappenberg. 1991. DNA-synthesis and tritiated thymidine incorporation by heterotrophic freshwater bacteria in continuous culture. Appl. Environ. Microbiol. 57:1675-1682.
17. Felsenstein, J. 1984. Distance methods for inferring phylogenies: a justification. Evolution 38:16-24.
18. Fields, M. W., T. F. Yan, S. K. Rhee, S. L. Carroll, P. M. Jardine, D. B. Watson, C. S. Criddle, and J. Z. Zhou. 2005. Impacts on microbial communities and cultivable isolates from groundwater contaminated with high levels of nitric acid-uranium waste. FEMS Microbiol. Ecol. 53:417-428.
19. Finneran, K. T., C. V. Johnsen, and D. R. Lovley. 2003. Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe (III). Int. J. Syst. Evol. Microbiol. 53:669-673.
20. Francis, A. J., C. J. Dodge, F. L. Lu, G. P. Halada, and C. R. Clayton. 1994. Xps and Xanes studies of uranium reduction by Clostridium sp. Environ. Sci. Technol. 28:636-639.
21. Frank, J. A., C. I. Reich, S. Sharma, J. S. Weisbaum, B. A. Wilson, and G. J. Olsen. 2008. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl. Environ. Microbiol. 74:2461-2470.
22. Grimes, D. J., C. R. Woese, M. T. MacDonell, and R. R. Colwell. 1997. Systematic study of the genus Vogesella gen. nov. and its type species, Vogesella indigofera comb. nov. Int. J. Syst. Bacteriol. 47:19-27.
23. Gu, B., H. Yan, P. Zhou, D. B. Watson, M. Park, and J. Istok. 2005. Natural humics impact uranium bioreduction and oxidation. Environ. Sci. Technol. 39:5268-5275.
24. Gu, B. H., W. M. Wu, M. A. Ginder-Vogel, H. Yan, M. W. Fields, J. Zhou, S. Fendorf, C. S. Criddle, and P. M. Jardine. 2005. Bioreduction of uranium in a contaminated soil column. Environ. Sci. Technol. 39:4841-4847.
25. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
26. Hira, D., M. Nojiri, K. Yamaguchi, and S. Suzuki. 2007. Identification of a blue copper protein from Hyphomicrobium denitrificans and its functions in the periplasm. J. Biochem. 142:335-341.
27. Holmes, D. E., K. T. Finneran, R. A. O'Neil, and D. R. Lovley. 2002. Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Appl. Environ. Microbiol. 68:2300-2306.
28. Kashefi, K., and D. R. Lovley. 2000. Reduction of Fe (III), Mn (IV), and toxic metals at 100 degrees C by Pyrobaculum islandicum. Appl. Environ. Microbiol. 66:1050-1056.
29. Khijniak, T. V., A. I. Slobodkin, V. Coker, J. C. Renshaw, F. R. Livens, E. A. Bonch-Osmolovskaya, N. K. Birkeland, N. N. Medvedeva-Lyalikova, and J. R. Lloyd. 2005. Reduction of uranium (VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens. Appl. Environ. Microbiol. 71:6423-6426.
30. Küsel, K., T. Dorsch, G. Acker, E. Stackebrandt, and H. L. Drake. 2000. Clostridium scatologenes strain SL1 isolated as an acetogenic bacterium from acidic sediments. Int. J. Syst. Evol. Microbiol. 50:537-546.
31. Laanbroek, H. J., H. J. Geerligs, L. Sijtsma, and H. Veldkamp. 1984. Competition for sulfate and ethanol among Desulfobacter, Desulfobulbus, and Desulfovibrio species isolated from intertidal sediments. Appl. Environ. Microbiol. 47:329-334.
32. Lack, J. G., S. K. Chaudhuri, S. D. Kelly, K. M. Kemner, S. M. O'Connor, and J. D. Coates. 2002. Immobilization of radionuclides and heavy metals through anaerobic bio-oxidation of Fe (II). Appl. Environ. Microbiol. 68:2704-2710.
33. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 15-176. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics, 1st ed. John Wiley & Sons, Chichester, NY.
34. Lovley, D. R., J. L. Fraga, E. L. Blunt-Harris, L. A. Hayes, E. J. P. Phillips, and J. D. Coates. 1998. Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim. Hydrobiol. 26:152-157.
35. Lovley, D. R., J. L. Fraga, J. D. Coates, and E. L. Blunt-Harris. 1999. Humics as an electron donor for anaerobic respiration. Environ. Microbiol. 1:89-98.
36. 0 reduction by Pelobacter carbinolicus. Appl. Environ. Microbiol. 61:2132-2138.
37. Lovley, D. R., E. J. P. Phillips, Y. A. Gorby, and E. R. Landa. 1991. Microbial reduction of uranium. Nature 350:413-416.
38. Lozupone, C., M. Hamady, and R. Knight. 2006. UniFrac: an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371-385.
39. Lozupone, C., and R. Knight. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228-8235.
40. Luo, W., and B. Gu. 2009. Dissolution and mobilization of uranium in a reduced sediment by natural humic substances under anaerobic conditions. Environ. Sci. Technol. 43:152-156.
41. Luo, W. S., W. M. Wu, T. F. Yan, C. S. Criddle, P. M. Jardine, J. Z. Zhou, and B. H. Gu. 2007. Influence of bicarbonate, sulfate, and electron donors on biological reduction of uranium and microbial community composition. Appl. Microbiol. Biotechnol. 77:713-721.
42. Madden, A. S., A. V. Palumbo, B. Ravel, T. A. Vishnivetskaya, T. J. Phelps, C. W. Schadt, and C. C. Brandt. 2009. Donor-dependent extent of uranium reduction for bioremediation of contaminated sediment microcosms. J. Environ. Qual. 38:53-60.
43. Madden, A. S., A. C. Smith, D. L. Balkwill, L. A. Fagan, and T. J. Phelps. 2007. Microbial uranium immobilization independent of nitrate reduction. Environ. Microbiol. 9:2321-2330.
44. Mohanty, S. R., B. Kollah, D. B. Hedrick, A. D. Peacock, R. K. Kukkadapu, and E. E. Roden. 2008. Biogeochemical processes in ethanol stimulated uraniumcontaminated subsurface sediments. Environ. Sci. Technol. 42:4384-4390.
45. Moon, J. W., Y. Roh, T. J. Phelps, D. H. Phillips, D. B. Watson, Y. J. Kim, and S. C. Brooks. 2006. Physicochemical and mineralogical characterization of soil-saprolite cores from a field research site, Tennessee. J. Environ. Qual. 35:1731-1741.
46. Nevin, K. P., D. E. Holmes, T. L. Woodard, S. F. Covalla, and D. R. Lovley. 2007. Reclassification of Trichlorobacter thiogenes as Geobacter thiogenes comb. nov. Int. J. Syst. Evol. Microbiol. 57:463-466.
47. North, N. N., S. L. Dollhopf, L. Petrie, J. D. Istok, D. L. Balkwill, and J. E. Kostka. 2004. Change in bacterial community structure during in situ biostimulation of subsurface sediment contaminated with uranium and nitrate. Appl. Environ. Microbiol. 70:4911-4920.
48. Nyman, J. L., T. L. Marsh, M. A. Ginder-Vogel, M. Gentile, S. Fendorf, and C. Criddle. 2006. Heterogeneous response to biostimulation for U (VI) reduction in replicated sediment microcosms. Biodegradation 17:303-316.
49. Palumbo, A. V., S. M. Pfiffner, L. Fagan, M. McNeilly, S. Rishell, J. E. Kostka, and C. C. Brandt. 2005. Conf. Proc. 3rd Eur. Bioremed. Conf., p. 81. Department of Environmental Engineering, Technical University of Crete, Chania, Crete.
50. Pankratov, T. A., Y. M. Serkebaeva, I. S. Kulichevskaya, W. Liesack, and S. N. Dedysh. 2008. Substrate-induced growth and isolation of Acidobacteria from acidic sphagnum peat. ISME J. 2:551-560.
51. Petrie, L., N. N. North, S. L. Dollhopf, D. L. Balkwill, and J. E. Kostka. 2003. Enumeration and characterization of iron (III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium (VI). Appl. Environ. Microbiol. 69:7467-7479.
52. Raes, J., J. Korbel, M. Lercher, C. von Mering, and P. Bork. 2007. Prediction of effective genome size in metagenomic samples. Genome Biol. 8: R10.
53. Reinhold-Hurek, B., and T. Hurek. 2000. Reassessment of the taxonomic structure of the diazotrophic genus Azoarcus sensu lato and description of three new genera and new species, Azovibrio restrictus gen. nov., sp nov., Azospira oryzae gen. nov., sp nov. and Azonexus fungiphilus gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 50:649-659.
54. Saeki, K., M. K. Jain, G. J. Shen, R. C. Prince, and J. G. Zeikus. 1989. Purification and properties of ferredoxin and rubredoxin from Butyribacterium methylotrophicum. J. Bacteriol. 171:4736-4741.
55. Sanford, R. A., Q. Wu, Y. Sung, S. H. Thomas, B. K. Amos, E. K. Prince, and F. E. Loffler. 2007. Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields. Environ. Microbiol. 9:2885-2893.
56. Schink, B., T. J. Phelps, B. Eichler, and J. G. Zeikus. 1985. Comparison of ethanol degradation pathways in anoxic fresh-water environments. J. Gen. Microbiol. 131:651-660.
57. Schloss, P. D., and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71:1501-1506.
58. Schryver, J. C., C. C. Brandt, S. M. Pfiffner, A. V. Palumbo, A. D. Peacock, D. C. White, J. P. McKinley, and P. E. Long. 2006. Application of nonlinear analysis methods for identifying relationships between microbial community structure and groundwater geochemistry. Microb. Ecol. 51:177-188.
59. Shelobolina, E. S., S. A. Sullivan, K. R. O'Neill, K. P. Nevin, and D. R. Lovley. 2004. Isolation, characterization, and U (VI)-reducing potential of a facultatively anaerobic, acid-resistant bacterium from low-pH, nitrate-and U (VI)-contaminated subsurface sediment and description of Salmonella subterranea sp. nov. Appl. Environ. Microbiol. 70:2959-2965.
60. Spain, A. M., A. D. Peacock, J. D. Istok, M. S. Elshahed, F. Z. Najar, B. A. Roe, D. C. White, and L. R. Krumholz. 2007. Identification and isolation of a Castellaniella species important during biostimulation of an acidic nitrate-and uranium-contaminated aquifer. Appl. Environ. Microbiol. 73:4892-4904.
61. Spear, J. R., L. A. Figueroa, and B. D. Honeyman. 2000. Modeling reduction of uranium U (VI) under variable sulfate concentrations by sulfate-reducing bacteria. Appl. Environ. Microbiol. 66:3711-3721.
62. Sung, Y., K. F. Fletcher, K. M. Ritalaliti, R. P. Apkarian, N. Ramos-Hernandez, R. A. Sanford, N. M. Mesbah, and F. E. Loffler. 2006. Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethenedechlorinating bacterium. Appl. Environ. Microbiol. 72:2775-2782.
63. Suzuki, Y., S. D. Kelly, K. M. Kemner, and J. F. Banfield. 2004. Enzymatic U (VI) reduction by Desulfosporosinus species. Radiochim. Acta 92:11-16.
64. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
65. Thauer, R. K., K. Jungermann, and K. Decker. 1977. Energy-conservation in chemotropic anaerobic bacteria. Bacteriol. Rev. 41:100-180.
66. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 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.
67. Wall, J. D., and L. R. Krumholz. 2006. Uranium reduction. Annu. Rev. Microbiol. 60:149-166.
68. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
69. Weber, K. A., D. B. Hedrick, A. D. Peacock, J. C. Thrash, D. C. White, L. A. Achenbach, and J. D. Coates. 2009. Physiological and taxonomic description of the novel autotrophic, metal oxidizing bacterium, Pseudogulbenkiania sp. strain 2002. Appl. Microbiol. Biotechnol. 83:555-565.
70. Weber, K. A., J. Pollock, K. A. Cole, S. M. O'Connor, L. A. Achenbach, and J. D. Coates. 2006. Anaerobic nitrate-dependent iron (II) bio-oxidation by a novel lithoautotrophic betaproteobacterium, strain 2002. Appl. Environ. Microbiol. 72:686-694.
71. Wu, Q., R. A. Sanford, and F. E. Loffler. 2006. Uranium (VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Appl. Environ. Microbiol. 72:3608-3614.
72. Wu, W. M., J. Carley, J. Luo, M. A. Ginder-Vogel, E. Cardenas, M. B. Leigh, C. C. Hwang, S. D. Kelly, C. M. Ruan, L. Y. Wu, J. Van Nostrand, T. Gentry, K. Lowe, T. Mehlhorn, S. Carroll, W. S. Luo, M. W. Fields, B. H. Gu, D. Watson, K. M. Kemner, T. Marsh, J. Tiedje, J. Z. Zhou, S. Fendorf, P. K. Kitanidis, P. M. Jardine, and C. S. Criddle. 2007. In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ. Sci. Technol. 41:5716-5723.