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.

Applied and Environmental Microbiology

Volumn 70, Issue 5, 2004, Pages 2959-2965

  Shelobolina, Evgenya S ^a   Sullivan, Sara A ^a   O'Neill, Kathleen R ^a   Nevin, Kelly P ^a   Lovley, Derek R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HYDROLYSIS; NITRATES; PH EFFECTS;

ACID-RESISTANT BACTERIUM; INDOLE PRODUCTION;

BACTERIA;

ACETOIN; ARGININE DEIMINASE; FUMARIC ACID; GELATIN; HYDROGEN; HYDROGEN SULFIDE; LYSINE DECARBOXYLASE; MALIC ACID; NITRATE; ORNITHINE DECARBOXYLASE; OXYGEN; PHENYLALANINE AMMONIA LYASE; RIBOSOME DNA; SULFATE; URANIUM; UREA;

MICROBIOLOGY;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOREMEDIATION; CONTROLLED STUDY; DNA SEQUENCE; ENTEROBACTER CLOACAE; HYDROLYSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PHYLOGENY; REDUCTION; SALMONELLA; SALMONELLA BONGORI; SALMONELLA SUBTERRANEA; SEDIMENT; SEQUENCE ANALYSIS; SOIL POLLUTION; UNITED STATES;

ANAEROBIOSIS; CULTURE MEDIA; DNA, RIBOSOMAL; FRESH WATER; GEOLOGIC SEDIMENTS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; NITRATES; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SALMONELLA; SEQUENCE ANALYSIS, DNA; URANIUM; WATER POLLUTION, CHEMICAL;

BACTERIA (MICROORGANISMS); ENTEROBACTER; ENTEROBACTER CLOACAE; NEGIBACTERIA; QUERCUS; SALMONELLA; SALMONELLA BONGORI; SALMONELLA SUBTERRANEA;

EID: 2542499758     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.5.2959-2965.2004     Document Type: Article

References (51)

1. Abdelouas, A., Y. Lu, W. Lutze, and H. E. Nuttall. 1998. Reduction of U(VI) to U(IV) by indigenous bacteria in contaminated ground water. J. Contam. Hydrol. 35:217-233.
2. Abdelouas, A., W. Lutze, W. Gong, E. H. Nuttall, B. A. Strietelmeier, and B. J. Travis. 2000. Biological reduction of uranium in groundwater and subsurface soil. Sci. Total Environ. 250:21-35.
3. Anderson, R. T., and D. R. Lovley. 2002. Microbial redox interactions with uranium: an environmental perspective, p. 205-223. In M. J. Keith-Roach and F. R. Livens (ed.), Interactions of microorganisms with radionuclides. Elsevier, Amsterdam, The Netherlands.
4. Anderson, R. T., H. A. Vrionis, I. Ortiz-Bernard, 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.
5. Balch, W. E., G. E. Gox, I. J. Magrum, C. R. Woese, and R. S. Wolfe. 1979. Methanogens: reevaluation of a unique biological group. Microbiol. Rev. 43:260-296.
6. Barton, L. L., K. Choudhury, B. M. Thomson, K. Steenhoudt, and A. R. Groffman. 1996. Bacterial reduction of soluble uranium: the first step of in situ immobilization of uranium. Radioact. Waste Manag. Environ. Restoration 20:141-151.
7. Brooks, S. C. 2001. Waste characteristics of the former S-3 ponds and outline of uranium chemistry relevant to NABIR Field Research Center studies. NABIR Field Research Center, Oak Ridge, Tenn.
8. Cherry, W. B., J. B. Hanks, B. M. Thomason, A. M. Murlin, J. W. Biddle, and J. M. Croom. 1972. Salmonellae as an index of pollution of surface waters. Appl. Microbiol. 24:334-340.
9. Clark, D. P., and J. E. Cronan. 1996. Two-carbon compounds and fatty acids as carbon sources, p. 343-357. In R. Curtiss, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella, vol. 1. ASM Press, Washington, D.C.
10. Davies, R. H., and C. Wray. 1996. Seasonal variations in the isolation of Salmonella typhimurium, Salmonella enteritidis, Bacillus cereus and Clostridium perfringens from environmental samples. J. Vet. Med. Ser. B 43:119-127.
11. Edwards, P. R., and W. H. Ewing. 1972. Identification of Enterobacteriaceae, 3rd ed. Burgess Publishing Co., Minneapolis, Minn.
12. Farmer, J. J., III, B. R. Davis, F. W. Hickman-Brenner, A. McWhorter, G. P. Huntley-Carter, M. A. Asbury, C. Riddle, H. G. Wathen-Grady, C. Elias, G. R. Fanning, A. G. Steigerwalt, C. M. O'Hara, G. K. Morris, P. B. Smith, and D. J. Brenner. 1985. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. J. Clin. Microbiol. 21:46-76.
13. 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.
14. Francis, A. J. 1998. Biotransformation of uranium and other actinides in radioactive wastes. J. Alloys Compounds 271-273:78-84.
15. Francis, A. J., C. J. Dodge, J. B. Gillow, and J. E. Cline. 1991. Microbial transformations of uranium in wastes. Radiochim. Acta 52-53:311-316.
16. Gorby, Y. A., and D. R. Lovley. 1992. Enzymatic uranium reduction. Environ. Sci. Technol. 26:205-207.
17. Goverd, K. A., F. W. Beech, R. P. Hobbs, and R. Shannon. 1979. The occurrence and survival of coliforms and salmonellas in apple juice and cider. J. Appl. Bacteriol. 46:521-530.
18. Hendricks, C. W. 1971. Increased recovery rate of salmonellae from stream bottom sediments versus surface waters. Appl. Microbiol. 21:379-380.
19. Hobbie, J. E., R. J. Daley, and S. Jasper. 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33:1225-1228.
20. 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.
21. Holt, J. G., N. R. Krieg, P. H. A. Sneath, J. T. Staley, and S. T. Williams. 1994. Bergey's manual of determinative bacteriology, 9th ed. Williams & Wilkins, Baltimore, Md.
22. Höltje, J.-V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
23. Isaac, L., and G. C. Ware. 1974. The flexibility of bacterial cell walls. J. Appl. Bacteriol. 37:335-339.
24. Kashefi, K., and D. R. Lovley. 2000. Reduction of Fe(III), Mn(IV), and toxic metals at 100°C by Pyrobaculum islandicum. Appl. Environ. Microbiol. 66:1050-1056.
25. Liao, C.-H., and G. M. Sapers. 2000. Attachment and growth of Salmonella Chester on apple fruits and in vivo response of attached bacteria to sanitizer treatments. J. Food Prot. 63:876-883.
26. Lieser, K. H. 1995. Radionuclides in the geosphere: sources, mobility, reactions in natural waters and interactions with solids. Radiochim. Acta 70-71:355-375.
27. Lin, J., I. S. Lee, J. Frey, J. L. Slonczewski, and J. W. Foster. 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J. Bacteriol. 177:4097-4104.
28. Lloyd, J. R., J. Chesnes, S. Glasauer, D. J. Bunker, F. R. Livens, and D. R. Lovley. 2002. Reduction of actinides and fusion products by Fe(III) -reducing bacteria. Geomicrobiol. J. 19:103-120.
29. Lloyd, J. R., and I. E. Macaskie. 2000. Bioremediation of radionuclide-containing wastewaters, p. 277-327. In D. R. Lovley (ed.), Environmental microbe-metal interaction. ASM Press, Washington, D.C.
30. Lovley, D. R., S. J. Giovannoni, D. C. White, J. E. Champine, E. J. P. Philips, 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. Lovley, D. R., and E. J. P. Phillips. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53:1536-1540.
32. Lovley, D. R., and E. J. P. Phillips. 1992. Reduction of uranium by Desulfovibrio desulfuricans. Appl. Environ. Microbiol. 58:850-856.
33. Lovley, D. R., E. J. P. Phillips, Y. A. Gorby, and E. R. Landa. 1991. Microbial reduction of uranium. Nature 350:413-416.
34. 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.
35. McWhorter, A. C., R. L. Haddock, F. A. Nocon, A. G. Steigerwalt, D. J. Brenner, S. Aleksic, J. Bockemühl, and J. J. Farmer. 1991. Trabulsiella guamensis, a new genus and species of the family Enterobacteriaceae that resembles Salmonella subgroups 4 and 5. J. Clin. Microbiol. 29:1480-1485.
36. Miller, T. L., and M. J. Wolin. 1974. A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl. Microbiol. 27:985-987.
37. Pietzsch, K., B. C. Hard, and W. Babel. 1999. A Desulfovibrio sp. capable of growing by reducing U(VI). J. Basic Microbiol. 39:365-372.
38. Pohl, P., E. Robaye, and J. Thomas. 1970. Comportement de Salmonella et Escherichia dans le milieu exterieur. Rev. Ferment. Ind. Aliment. 25:22-28.
39. Prokšová, M., E. Mogonová, P. Ferianc, and J. Harichová. 2002. The occurrence of Salmonella spp. in natural environment confirmed by biochemical and molecular methods. Biologia 57:797-803.
40. Rao, S. S. (ed.). 1989. Acid stress and aquatic microbial interactions. CRC Press, Inc., Boca Raton, Fla.
41. Rhodes, M. W., and H. Kator. 1988. Survival of Escherichia coli and Salmonella spp. in estuarine environments. Appl. Environ. Microbiol. 54:2902-2907.
42. Saunders, J. A., and L. E. Toran. 1995. Modelling of radionuclide and heavy metal sorption around low- and high-pH waste disposal sites at Oak Ridge, Tennessee. Appl. Geochem. 10:673-684.
43. Shelobolina, E. S., C. Gaw Van Praagh, and D. R. Lovley. 2003. Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri. Geomicrobiol. J. 20:143-156.
44. Shelobolina, E. S., K. O'Neill, K. T. Finneran, L. A. Hayes, and D. R. Lovley. 2003. Potential for in situ bioremediation of a low-pH, high-nitrate uranium-contaminated groundwater. Soil Sediment Contam. 12:865-884.
45. Silva, R. J., and H. Nitsche. 1995. Actinide environmental chemistry. Radiochim. Acta 70-71:377-396.
46. 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.
47. Thomason, B. M., D. J. Dodd, and W. B. Cherry. 1977. Increased recovery of salmonellae from environmental samples enriched with buffered peptone water. Appl. Environ. Microbiol. 34:270-273.
48. Valinsky, L., G. D. Vedova, A. J. Scupham, S. Alvey, A. Figueroa, B. Yin, R. J. Hartin, M. Chrobak, D. E. Crowley, T. Jiang, and J. Borneman. 2002. Analysis of bacterial community composition by oligonucleotide fingerprinting of rRNA genes. Appl. Environ. Microbiol. 68:3243-3250.
49. Winfield, M. D., and E. A. Groisman. 2003. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl. Environ. Microbiol. 69:3687-3694.
50. Wronkiewicz, D. J., and E. C. Buck. 1999. Uranium mineralogy and the geologic disposal of spent nuclear fuel, p. 475-497. In P. C. Burns and R. Finch (ed.), Uranium: mineralogy, geochemistry and the environment, vol. 38. Mineralogical Society of America, Washington, D.C.
51. Zhuang, R.-Y., L. R. Beuchat, and F. J. Angulo. 1995. Fate of Salmonella montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Appl. Environ. Microbiol. 61:2127-2131.