Unique ecophysiology among U(VI)-reducing bacteria as revealed by evaluation of oxygen metabolism in anaeromyxobacter dehalogenans strain 2CP-C

Applied and Environmental Microbiology

Volumn 76, Issue 1, 2010, Pages 176-183

  Thomas, Sara H ^a   Sanford, Robert A ^b   Amos, Benjamin K ^a,e   Leigh, Mary Beth ^c   Cardenas, Erick ^d   Löffler, Frank E ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b ILLINOIS STATE GEOLOGICAL SURVEY   (United States)

^c UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e GEOSYNTEC CONSULTANTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBIC GROWTH; BIOMASS PRODUCTIONS; BIOREDUCTIONS; BIOSTIMULATION; ECOPHYSIOLOGY; ELECTRON DONOR OXIDATION; ENERGY GENERATIONS; FIELD RESEARCH; GEOBACTER; GROUNDWATER SAMPLING; HEXAVALENT URANIUM; IN-SITU; LABORATORY STUDIES; LINEAR CORRELATION; OXYGEN CONCENTRATIONS; OXYGEN PARTIAL PRESSURE; OXYGEN REDUCTION; OXYGEN RESPIRATION; PILOT SCALE; SOIL PARTICLES; SPECIFIC GROWTH RATE;

BACTERIOLOGY; ECOLOGY; ELECTROLYTIC REDUCTION; GROUNDWATER; HYDROGEOLOGY; INTERNET PROTOCOLS; OXYGEN; PHYSIOLOGY; POPULATION STATISTICS; SEDIMENTOLOGY; SOILS; TRANSURANIUM ELEMENTS; URANIUM;

CELLS;

OXYGEN; URANIUM;

ANAEROBIOSIS; CONTAMINATED LAND; ECOPHYSIOLOGY; GROWTH RATE; IMMOBILIZATION; IRON-REDUCING BACTERIUM; LABORATORY METHOD; OXIC CONDITIONS; RADIONUCLIDE; SOIL MICROORGANISM; URANIUM;

AEROBIC METABOLISM; ARTICLE; BACTERIAL COUNT; ELECTRON; ENERGY METABOLISM; GEOBACTER; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MYXOCOCCALES; OXIDATION REDUCTION REACTION;

AEROBIOSIS; COLONY COUNT, MICROBIAL; ELECTRONS; ENERGY METABOLISM; GEOBACTER; MYXOCOCCALES; OXIDATION-REDUCTION; OXYGEN; URANIUM; WATER MICROBIOLOGY;

ANAEROMYXOBACTER; ANAEROMYXOBACTER DEHALOGENANS; ANAEROMYXOBACTER DEHALOGENANS 2CP-C; GEOBACTER;

EID: 76149146392     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01854-09     Document Type: Article

References (60)

1. Amos, B. K., Y. Sung, K. E. Fletcher, T. J. Gentry, W. M. Wu, C. S. Griddle, J. Zhou, and F. E. Löffler. 2007. Detection and quantification of Geobacter lovleyi strain SZ: implications for bioremediation at tetrachloroethene- and uranium-impacted sites. Appl. Environ. Microbiol. 73:6898-6904.
2. Arnold, R. G., M. R. Hoffmann, T. J. Dichristina, and F. W. Picardal. 1990. Regulation of dissimilatory Fe(III) reduction activity in Shewanella putrefaciens. Appl. Environ. Microbiol. 56:281.1-2817.
3. Baker, S. C., S. J. Ferguson, B. Ludwig, M. D. Page, O. M. H. Richter, and R. J. M. van Spanning. 1998. Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility. Microbiol. Mol. Biol. Rev. 62:1046-1078.
4. Brune, A., P. Frenzel, and H. Cypionka. 2000. Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol. Rev. 24:691710.
5. Cardenas, E., W. M. Wu, M. B. Leigh, J. Carley, L. S. Carrol, T. Gentry, J. Luo, D. Watson, B. Gu, M. Gínder-Vogel, P. K. Kitanidts, P. M. Jardine, J. Zhou, C. S. Criddle, T. L. Marsh, and J. M. Tiedje. 2008. Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl. Environ. Microbiol. 74:3718-3729.
6. Childers, S. E., S. Ciufo, and D. R. Lovley. 2002. Geobacter metallireducens accesses insoluble Fe(III) oxide by Chemotaxis. Nature 416:767-769.
7. Cole, J. R., A. L. Casearelli, W. W. Mohn, and J. M. Tiedje. 1994. Isolation and characterization of a novel bacterium growing via reductive dehalogenation of 2-chlorophenol. Appl. Environ. Microbiol. 60:3536-3542.
8. Cole, J. R., B. Z. Fathepure, and J. M. Tiedje. 1995. Tetrachloroethene and 3-chlorobenzoate dechlorination activities are co-induced in Desulfomonile tiedjei DCB-I. Biodegradation 6:167-172.
9. Criddle, C. S., L. A. Alvarez, and P. L. McCarty. 1991. Microbial processes in porous media, p. 639-691. In J. Bear and M. Y. Corapcioglu (ed.), Transport processes in porous media. Kluwer Academic Publishers, Dordrecht, The Netherlands.
10. Cummings, D. E., O. L. Snoeyenbos-West, D. T. Newby, A. M. Niggemyer, D. R. Lovley, L. A. Achenbach, and R. F. Rosenzweig. 2003. Diversity of Geobacleraceae species inhabiting metal-polluted freshwater lake sediments ascertained by 16S rDNA analyses. Microb. Ecol. 46:257-269.
11. DiChristina, T. J., J. K. Fredrickson, and J. M. Zachara. 2005. Enzymology of electron transport: energy generation with geochemical consequences. Rev. Mineral Geochem. 59:27-52.
12. Fournier, M., C. Aubert, Z. Dermoun, M. C. Durand, D. Moinier, and A. Dolla. 2006. Response of the anaerobe Desulfovibrio vulgaris Hildenborough to oxidative conditions: proteome and transcript analysis. Biochimie 88:85-94.
13. 13. Gadd, G. M. 2004. Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109-119. (Pubitemid 39204478)
14. Gorby, Y. A., and D. R. Lovley. 1991. Electron transport in the dissimilatory iron reducer, GS-15. Appl. Environ. Microbiol. 57:867-870.
15. He, J. Z. K. M. Ritalahti, M. R. Aiello, and F. E. Löffler. 2003. Complete detoxification of vinyl chloride by an anaerobic enrichment culture and identification of the reductively dechlorinating population as a Dehalococcoides species. Appl. Environ. Microbiol. 69:996-1003.
16. He, Q., and R. A. Sanford. 2004. Acetate threshold concentrations suggest varying energy requirements during anaerobic respiration by Anaeromyxobacter dehalogenans. Appl. Environ. Microbiol. 70:6940-6943.
17. He, Q., and R. A. Sanford. 2003. Characterization of Fe(III) reduction by chlororespiring Anaeromyxobacter dehalogenans. Appl. Environ. Microbiol. 69:2712-2718.
18. Holmes, D. E., R. A. O'Neil, H. A. Vrionis, L. A. N'Guessan, I. Ortiz-Bemad, M. J. Larrahondo, L. A. Adams, J. A. Ward, J. S. Nicoll, K. P. Nevin, M. A. Chavan, J. P. Johnson, P. E. Long, and D. R. Lovley. 2007. Subsurface clade of Geobacleraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J. 1:663-677.
19. Hutchinson, G. E. 1961. The paradox of the plankton. Am. Nat. 95:137-145.
20. Johnson, M. S., I. B. Zhulin, M.-E. R. Gapuzan, and B. L. Taylor. 1997. Oxygen-dependent growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 179:5598-5601.
21. Krekeler, D., A. Teske, and H. Cypionka. 1998. Strategies of sulfatc-reducing bacteria to escape oxygen stress in a cyanobacteria! mat. FEMS Microbiol. Ecol. 25:89-96.
22. Langmuir, D. 1978. Uranium solution-mineral equilibria at low temperatures with applications to sedimentary ore deposits. Geochim. Cosmochim. Acta 42:547-569.
23. Lemos, R. S., C. M. Gomes, M. Santana, J. LeGaIl, A. V. Xavier, and M. Teixeira. 2001. The 'strict' anaerobe Desulfovibrio gigas contains a membrane-bound oxygen-reducing respiratory chain. FEBS Lett. 496:40-43.
24. LIn, W. C., M. V. Coppi, and D. R. Lovley. 2004. Geobacter sulfurreducens can. grow with oxygen as a terminal electron acceptor. Appl. Environ. Microbiol. 70:2525-2528.
25. Lloyd, J. R., and J. C. Renshaw. 2005. Bioremediation of radioactive waste: radionuclide-microbe interactions in laboratory and field-scale studies. Curr. Opin. Biotechnol. 16:254-260.
26. Lobo, S. A. L, A. M. P. Melo, J. N. Carita, M. Teixeira, and L. M. Saraiva. 2007. The anaerobe Desulfovibrio desulfuricans ATCC 27774 grows at nearly atmospheric oxygen levels. FEBS Lett. 581:433-436.
27. Löffler, F. E., R. A. Sanford, and J. M. Tiedje. 1996. Initial characterization of a reductive dehalogenase from Desulfitobacterium chlororespirans Co23. Appl. Environ. Microbiol. 62:3809-3813.
28. Löffler, F. E., J. M. Tiedje, and R. A. Sanford. 1999. Fraction of electrons consumed in electron acceptor reduction and hydrogen thresholds as indicators of halorespiratory physiology. Appl. Environ. Microbiol. 65:4049-4056.
29. 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.
30. Lovley, D. R., P. K. Widman, J. C. Woodward, and E. J. P. Phillips. 1993. Reduction of uranium by cytochrome-c, oí Desulfovibrio vulgaris. Appl. Environ. Microbiol. 59:3572-3576.
31. Luo, J., F.-A. Weber, O. A. Cirpka, W.-M. Wu, J. L. Nyman, J. Carley, P. M. Jardine, C. S. Criddle, and P. K. Kitanidis. 2007. Modeling in situ uranium(VI) bioreduction by sulfate-reducing bacteria. J. Contam. Hydrol. 92:129-148.
32. McCarty, P. L. 1988. Bioengineering issues related to in situ remediation of contaminated soils and groundwater, p. 143-162. In G. S. Omenn (ed.), Environmental biotechnology: reducing risks from environmental chemicals through, biotechnology. Plenum Press, New York, NY.
33. McCarty, P. L. 1971. Energetics and bacterial growth, p. 495-531. In S. D. Faust and J. V. Hunter (ed.), Organic compounds in aquatic environments. Marcel Dekker, New York, NY.
34. Mukhopadhyay, A., A. M. Redding, M. P. Joachimiak, A. P. Arkin, S. E. Borglin, P. S. Dehal, R. Chakraborty, J. T. Geller, T. C. Hazen, Q. He, D. C. Joyner, V. J. J. Martin, J. D. Wall, Z. K. Yang, J. Zhou, and J. D. Keasling. 2007. Cell-wide responses to low-oxygen exposure in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 189:5996-6010.
35. Nealson, K. H., A. BeIz, and B. McKee http://McKee. 2002. Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek 81:215-222.
36. 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 cocontaminated with uranium and nitrate. Appl. Environ. Microbiol. 70:4911-4920.
37. Okutman Tas, D., and S. G. Pavlostathis. 2005. Microbial reductive transformation of pentachloronitrobenzene under methanogenic conditions. Environ. Sci. Technol. 39:8264-8272.
38. Pereira, P. M., Q. He, A. V. Xavier, J. Z. Zhou, I. A. C. Perlera, and R. O. Louro. 2008. Transcriptional response of Desulfovibrio vulgaris Hildenborough to oxidative stress mimicking environmental conditions. Arch. Microbiol. 189:451-461.
39. 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.
40. 3 oxidases. Biochim. Biophys. Acta 1655:388-399.
41. 3-type cytochrome oxidase terminates the symbiosisspecific respiratory chain of Bradyrhizobium japonicum. J. Bacteriol. 178: 1532-1538.
42. Roden, E. E., and D. R. Lovley. 1993. Dissimilatory Fe(III) reduction by the marine microorganism Desulfuromonas acetoxidans. Appl. Environ. Microbiol. 59:734-742.
43. Sanford, R. A., J. R. Cole, and J. M. Tiedje. 2002. Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl halorespiring facultative anaerobic myxobacterium. Appl. Environ. Microbiol. 68:893-900.
44. Sanford, R. A., Q. Wu, Y. Sung, S. H. Thomas, B. K. Amos, E. K. Prince, and F. E. Löffler. 2007. Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields. Environ. Microbiol. 9:2885-2893.
45. Santana, M. 2008. Presence and expression of terminal oxygen reductases in strictly anaerobic sulfate-reducing bacteria isolated from salt-marsh sediments. Anaerobe 14:1.45-156.
46. Stein, L. Y., M. T. La Due, T. J. Grundl, and K. H. Nealson. 2001. Bacterial and archaeal populations associated with freshwater ferromanganous micronodules. and sediments. Environ. Microbiol. 3:10-18.
47. Sung, Y., K. F. Fletcher, K. M. Ritalaliti, R. P. Apkarian, N. Ramos-Hernandez, R. A. Sanford, N. M. Mesbah, and F. E. Löffler. 2006. Geobacter lovleyi sp. nov. strain SZ, a novel, metal-reducing and tetrachloroethenedechlorinating bacterium. Appl. Environ. Microbiol. 72:2775-2782.
48. Thomas, S. H., E. P. Crespo, P. M. Jardine, R. A. Sanford, and F. E. Löffler. 2009. Diversity and distribution of Anaeromyxobacter strains in a uraniumcontaminated subsurface environment with nonuniform flow. Appl. Environ. Microbiol. 75:3679-3687.
49. Thomas, S. H., R. D. Wagner, A. K. Arakaki, J. Skolnick, J. R. Kirby, L. J. Shimkets, R. A. Sanford, and F. E. Löffler. 2008. The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-Proteobacteria. PLoS One 3:e2103.
50. Treude, N., D. Rosencrantz, W. Liesack, and S. Schnell. 2003. Strain FAc12, a dissimilatoiy iron-reducing member of the Anaeromyxobacter subgroup of Myxococcales. FEMS Microbiol. Ecol. 44:261-269.
51. Wall, J. D., and I. R. Krumholz. 2006. Uranium reduction. Annu. Rev. Microbiol. 60:149-166.
52. Wan, J. M., T. K. Tokunaga, E. Brodie, Z. M. Wang, Z. P. Zheng, D. Herman, T. C. Hazen, M. K. Firestone, and S. R. Sutton. 2005. Reoxidation of bioreduced uranium, under reducing conditions. Environ. Sei. Technol. 39:6162-6169.
53. Weber, K. A., M. M. Urrutia, P. F. Churchill, R. K. Kukkadapu, and E. E. Roden. 2006. Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ. Microbiol. 8:1.00-1.13.
54. Wu, Q., R. A. Sanford, and F. E. Löffler. 2006. Uranium(VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Appl. Environ. Microbiol. 72: 3608-3614.
55. Wu, W.-M., J. Carley, M. Fienen, T. Mehlhorn, K. Lowe, J. Nyman, J. Luo, M. E. Gentile, R. Rajan, D. Wagner, R. F. Hickey, B. H. Gu, D. Watson, O. A. Cirpka, P. K. Kitanidis, P. M. Jardine, and C. S. Criddle. 2006. Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone. Environ. Sci. Technol. 40:3978-3985.
56. Wu, W.-M., J. Carley, J. Luo, M. A. Ginder-Vogel, E. Cardenas, M. B. Leigh, C. A. C. Hwang, S. D. Kelly, C. M. Kuan, L. Wu, J. V. Nostrand, T. Gentry, K. Lowe, T. Mehlhorn, S. Carroll, W. Luo, M. W. Fields, B. H. Gu, D. Watson, K. M. Kemner, T. Marsh, J. Tiedje, J. 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. Sei. Technol. 41:5716-5723.
57. Wu, W. M., J. Carley, T. Gentry, M. A. Ginder-Vogel, M. Fienen, T. Mehlhorn, H. Yan, S. Caroll, M. N. Pace, J. Nyman, J. Luo, M. E. Gentile, M. W. Fields, R. F. Hickey, B. H. Gu, D. Watson, O. A. Cirpka, J. Z. Zhou, S. Fendorf, P. K. Kitanidis, P. M. Jardine, and C. S. Criddle. 2006. Pilot-scale in situ bioremedation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability. Environ. Sci. Technol. 40:3986-3995.
58. Yabusaki, S. B., Y. Fang, P. E. Long, C. T. Reseh, A. D. Peacock, J. Komlos, P. R. Jaffe, S. J. Morrison, R. D. Dayvault, D. C. White, and R. T. Anderson. 2007. Uranium removal from groundwater via in situ biostimulation: fieldscale modeling of transport and biological processes. J. Contam.. Hydrol. 93:216-235.
59. Zhang, W. W., D. E. Culley, M. Hogan, L. Vitiritti, and F. J. Brockman. 2006. Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Antonie Van Leeuwenhoek 90:41.-55.
60. Zhou, J., M. A. Bruns, and J. M. Tiedje. 1996. DNA recoveiy from soils of diverse composition. Appl. Environ. Microbiol. 62:31.6-322.