Transcriptome Analysis of Metal-Reducing Bacteria

Dwayne A. Elias; Matthew W. Fields

doi:10.1128/9781555817190.ch12

Chapter 12 : Transcriptome Analysis of Metal-Reducing Bacteria

Authors: Dwayne A. Elias¹, Matthew W. Fields²

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Affiliations: 1: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6036; 2: Department of Microbiology, Center for Biofilm Engineering, Montana State University, Bozeman, MT 59717

Content Type: Monograph

Publication Year: 2011

Category: Applied and Industrial Microbiology; Environmental Microbiology

Book DOI: 10.1128/9781555817190

Chapter DOI: 10.1128/9781555817190.ch12

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Abstract:

This chapter focuses on transcriptomic studies in the more well-studied systems of metal-reducing bacteria represented by Shewanella, Geobacter and Desulfovibrio that have both genome sequence data and postgenomic tools available. This review compares available data for more commonly studied bacteria that can transfer electrons to different metals in the context of carbon flow, electron flow, oxidative stress, and physiological states of the cell. A goal of the comparison is to identify similarities and differences in molecular mechanisms used by different metal-reducing bacteria to interact with metals and thus optimize their metabolism accordingly in order to tolerate “stressful” substrates. Microarrays have been a powerful tool for monitoring dynamic gene expression under various conditions and have been widely used for genome-wide transcriptional analyses in microorganisms. One important aspect to consider when investigating the metal-reduction mechanisms within a given species is the organization of vectoral electron transport. Transcriptome analysis indicated that increased oxygen levels upexpressed genes involved in cell-cell and cell-surface interactions, and the aggregated cells also upexpressed genes associated with anaerobic growth. Based upon the many different transcriptomic studies of stress and growth responses in three model metal-reducing bacteria, some similarities and differences can be discerned. Metal-reducing bacterias contain genes with homology to typical metalresponsive regulators. However, more work is needed to elucidate the respective regulatory networks for these regulators in anaerobic microorganisms and how the regulatory networks are coordinated.

Citation: Elias D, Fields M. 2011. Transcriptome Analysis of Metal-Reducing Bacteria, p 213-246. In Stolz J, Oremland R (ed), Microbial Metal and Metalloid Metabolism. ASM Press, Washington, DC. doi: 10.1128/9781555817190.ch12

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Transcriptome Analysis of Metal-Reducing Bacteria

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FIGURE 1

Transmission electron micrograph of D. vulgaris Hildenborough after 24 h of incubation with 200 mM U(VI). The cells are unstained and show the extracellular nature of U(IV), whereas none was present inside the cells (D. Elias, unpublished data). 10.1128/9781555817190.ch12.f1

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FIGURE 1

References

/content/book/10.1128/9781555817190.ch12

1. Afkar, E.,, G. Reguera,, M. Schiffer, and, D. R. Lovley. 2005. A novel Geobacteraceae-specific outer membrane protein J (OmpJ) is essential for electron transport to Fe(III) and Mn(IV) oxides in Geobacter sulfurreducens. BMC Microbiol. 5: 41.

2. Agency for Toxic Substances and Disease Registry (ATSDR). 2004. Toxicological Profile for Chromium. Agency for Toxic Substances and Disease Registry, Atlanta, GA.

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. Andreini, C.,, L. Banci,, I. Bertini,, S. Elmi, and, A. Rosato. 2007. Non-heme iron through the three domains of life. Proteins 67: 317– 324.

5. Barton, L. L.,, K. Choudhury,, B. M. Thomsom,, K. Steenhoudt, and, A. R. Groffman. 1996. Bacterial reduction of soluble uranium: the first step of in situ immobilization of uranium. Radioact. Waste Manage. Environ. Rest. 20: 141– 151.

6. Baumgarten, A.,, I. Redenius,, J. Kranczoch, and, H. Cypionka. 2001. Periplasmic oxygen reduction by Desulfovibrio species. Arch. Microbiol. 176: 306– 309.

7. Beech, I. B.,, C. W. S. Cheung,, D. B. Johnson, and, J. R. Smith. 1996. Comparative studies of bacterial biofilms on steel surfaces using atomic force microscopy and environmental scanning electron microscopy. Biofouling 10: 65.

8. Beliaev, A. S.,, D. M. Klingeman,, J. A. Klappen-bach,, L. Wu,, M. F. Romine,, J. M. Tiedje,, K. H. Nealson,, J. K. Fredrickson, and, J. Zhou. 2005. Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors. J. Bacteriol. 187: 7138– 7145.

9. Beliaev, A. S.,, D. A. Saffarini,, J. L. McLaughlin, and, D. Hunnicutt. 2001. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol. Microbiol. 39: 722– 730.

10. Beliaev, A. S.,, D. K. Thompson,, M. W. Fields,, L. Wu,, D. P. Lies,, K. H. Nealson, and, J. Zhou. 2002a. Microarray transcription profiling of a Shewanella oneidensis etr A mutant. J. Bacteriol. 184: 4612– 4616.

11. Beliaev, A. S.,, D. K. Thompson,, T. Khare,, H. Lim,, C. C. Brandt,, G. Li,, A. E. Murray,, J. F. Heidelberg,, C. S. Giometti,, J. Yates III,, K. H. Nealson,, J. M. Tiedje, and, J. Zhoui. 2002b. Gene and protein expression profiles of Shewanella oneidensis during anaerobic growth with different electron acceptors. OMICS 6: 39– 60.

12. Beller, H. R.,, T. C. Legler,, F. Bourguet,, T. E. Letain,, S. R. Kane, and, M. A. Coleman. 2009. Identification of c-type cytochromes involved in anaerobic, bacterial U(IV) oxidation. Biodegradation 20: 45– 53.

13. Beloin, C.,, and J. M. Ghigo. 2005. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol. 13: 16– 19.

14. Bencheikh-Latmani, R.,, S. M. Williams,, L. Haucke,, C. S. Criddle,, L. Wu,, J. Zhou, and, B. M. Tebo. 2005. Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr(VI) and U(VI) reduction. Appl. Environ. Microbiol. 71: 7453– 7460.

15. Bender, K. S.,, H.-C. Yen,, C. L. Hemme,, Z. Yang,, Z. He,, Q. He,, J. Zhou,, K. H. Huang,, E. J. Alm,, T. C. Hazen,, A. P. Arkin, and, J. D. Wall. 2007. Analysis of a ferric uptake regulator (Fur) mutant of Desulfovibrio vulgaris Hildenborough. Appl. Environ. Microbiol. 73: 5389– 5400.

16. Berks, B. C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22: 393– 404.

17. Berks, B. C.,, T. Palmer, and, F. Sargent. 2003. The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47: 187– 254.

18. Berks, B. C.,, F. Sargent, and, T. Palmer. 2000. The TAT protein export pathway. Mol. Microbiol. 35: 260– 274.

19. Boyd, E. S.,, D. E. Cummings, and, G. G. Geesey. 2007. Mineralogy influences structure and diversity of bacterial communities associated with geological substrata in a pristine aquifer. Microb. Ecol. 54: 170– 182.

20. Bretschger, O.,, A. Obraztsova,, C. A. Sturm,, I. S. Chang,, Y. A. Gorby,, S. B. Reed,, D. E. Culley,, C. L. Reardon,, S. Barua,, M. F. Romine,, J. Zhou,, A. S. Beliaev,, R. Bouhenni,, D. Saffarini,, F. Mansfeld,, B. H. Kim,, J. K. Fredrickson, and, K. H. Nealson. 2007. Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl. Environ. Microbiol. 73: 7003– 7012.

21. Brown, S. D.,, M. Martin,, S. Deshpande,, S. Seal,, K. Huang,, E. Alm,, Y. Yang,, L. Wu,, T. Yan,, X. Liu,, A. P. Arkin,, K. Chourey,, J. Zhou, and, D. K. Thompson. 2006. Cellular response of Shewanella oneidensis to strontium stress. Appl. Environ. Microbiol. 72: 890– 900.

22. Brown, S. D.,, M. R. Thompson,, N. C. VerBerkmoes,, K. Chourey,, M. Shah,, J. Zhou,, R. L. Hettich, and, D. K. Thompson. 2006. Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol. Cell. Proteomics 5: 1054– 1071.

23. Caffrey, S. M.,, H.-S. Park,, J. Been,, P. Gordon,, C. W. Sensen, and, G. Voordouw. 2008. Gene expression by the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough grown on an iron electrode under cathodic protection conditions. Appl. Environ. Microbiol. 74: 2404– 2413.

24. Caffrey, S. M.,, and G. Voordouw. 2010. Effect of sulfide on growth physiology and gene expression of Desulfovibrio vulgaris Hildenborough. Antonie van Leeuwenhoek 97: 11– 20.

25. Caffrey, S. M.,, H.-S. Park,, J. K. Voordouw,, Z. He,, J. Zhou, and, G. Voordouw. 2007. Function of periplasmic hydrogenases in the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 189: 6159– 6167.

26. Cervantes, C.,, J. Campos-Garca,, S. Devars,, F. Gutierrez-Corona,, H. Loza-Tavera,, J. C. Torres-Guzman, and, R. Moreno-Sanchez. 2001. Interactions of chromium with microorganisms and plants. FEMS Microbiol. Rev. 25: 335– 347.

27. Chang, Y.,, A. D. Peacock,, P. E. Long,, J. R. Shephen,, J. P. McKinley,, S. J. MacNaughton,, A. K. M. Anwar-Hussain,, A. M. Saxton, and, D. C. White. 2001. Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl. Environ. Microbiol. 67: 3149– 3160.

28. Chapelle, F. H.,, and D. R. Lovley. 1992. Competitive exclusion of sulfate-reduction by iron(III)-reducing bacteria: a mechanism for producing discrete zones of high-iron ground water. Ground Water 30: 29– 36.

29. Charania, M. A.,, K. L. Brockman,, Y. Zhang,, A. Banerjee,, G. E. Pinchuk,, J. K. Fredrickson,, A. S. Beliaev, and, D. A. Saffarini. 2009. Involvement of a membrane-bound class III adenylate cyclase in regulation of anaerobic respiration in Shewanella oneidensis MR-1. J. Bacteriol. 191: 4298– 4306.

30. Chardin, B.,, A Dolla,, F. Chaspoul,, M. L. Fardeau,, P. Gallice, and, M. Bruschi. 2002. Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulfate-reducing bacteria. Appl. Microbiol. Biotechnol. 60: 352– 360.

31. Chen, L.,, L. Keramati, and, J. D. Helmann. 1995. Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions. Proc. Natl. Acad. Sci. USA 92: 8190– 8194.

32. Chhabra, S. R.,, Q. He,, K. H. Huang,, S. P. Gaucher,, E. J. Alm,, Z. He,, M. Z. Hadi,, T. C. Hazen,, J. D. Wall,, J. Zhou,, A. P. Arkin, and, A. K. Singh. 2006. Global analysis of heat shock response in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 188: 1817– 1828.

33. Chin, K. J.,, A. Esteve-Nunez,, C. Leang, and, D. R. Lovley. 2004. Direct correlation between rates of anaerobic respiration and levels of mRNA for key respiratory genes in Geobacter sulfurreducens. Appl. Environ. Microbiol. 70: 5183– 5189.

34. Chourey, K.,, M. R. Thompson,, J. Morrell-Falvey,, N. C. VerBerkmoes,, S. D. Brown,, M. Shah,, J. Zhou,, M. Doktycz,, R. L. Hettich, and, D. K. Thompson. 2006. Global molecular and morphological effects of 24-hour chromium(VI) exposure on Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 72: 6331– 6344.

35. Chourey, K.,, W. Wei,, X.-F. Wan, and, D. K. Thompson. 2008. Transcriptome analysis reveals response regulator SO2426-mediated gene expression in Shewanella oneidensis MR-1 under chromate challenge. BMC Genomics 9: 395.

36. Clark, M. E.,, R. E. Edelmann,, M. L. Duley,, J. D. Wall, and, M. W. Fields. 2007. Biofilm formation in Desulfovibrio vulgaris Hildenborough is dependent upon protein filaments. Environ. Microbiol. 9: 2844– 2854.

37. Clark, M. E.,, Q. He,, Z. He,, E. J. Alm,, K. H. Huang,, T. C. Hazen,, A. P. Arkin,, J. D. Wall,, J. Zhou, and, M. W. Fields. 2006. Temporal transcriptomic analyses of Desulfovibrio vulgaris Hildenborough during electron donor depletion. Appl. Environ. Microbiol. 72: 5578– 5588.

38. Craft, E. S.,, A. W. Abu-Qare,, M. M. Flaherty,, M. C. Garofolo,, H. L. Rincavage, and, M. B. Abou-Donia. 2004. Depleted and natural uranium: chemistry and toxicological effects. J. Toxicol. Environ. Health Part B: Crit. Rev. 7: 297– 317.

39. Cunningham, A.,, W. G. Characklis,, F. Abedeen, and, D. Crawford. 1991. Influence of biofilm accumulation on porous media hydrodynamics. Environ. Sci. Technol. 25: 1305– 1311.

40. Cypionka, J. 2000. Oxygen respiration by Desulfovibrio species. Annu. Rev. Microbiol. 54: 827– 848.

41. DeRisi, J. L.,, V. R. Iyer, and, P. O. Brown. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680– 686.

42. DiChristina, T. J.,, C. M. Moore, and, C. A. Haller. 2002. Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE ( gspE) type II protein secretion gene. J. Bacteriol. 184: 142– 151.

43. DiDonato, L. N.,, S. A. Sullivan,, B. A. Methé,, K. P. Nevin,, R. England, and, D. R. Lovley. 2006. Role of Rel Gsu in stress response and Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 188: 8469– 8478.

44. Dilks, K.,, R. W. Rose,, E. Hartmann, and, M. Pohlschroder. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185: 1478– 1483.

45. Dolla, A.,, B. K. Pohorelic,, J. K. Voordouw, and, G. Voordouw. 2000. Deletion of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough hampers hydrogen metabolism and low-redox-potential niche establishment. Arch. Microbiol. 174: 143– 151.

46. Dolla, A.,, M. Fourniera, and, Z. Dermoun. 2006. Oxygen defense in sulfate-reducing bacteria. J. Biotechnol. 126: 87– 100.

47. Elias, D. A.,, E. C. Drury,, A. M. Redding,, A. Mukhopadyay,, H.-C. B. Yen,, M. W. Fields,, T. C. Hazen,, A. P. Arkin,, J. D. Keasling, and, J. D. Wall. 2009. Expression profiling of hypothetical genes in Desulfovibrio vulgaris leads to improved functional annotation. Nucleic Acids Res. 37: 2926– 2939.

48. Elias, D. A.,, M. E. Monroe,, M. J. Marshall,, M. F. Romine,, A. S. Belieau,, J. K. Fredrickson,, G. A. Anderson,, R. D. Smith, and, M. S. Lipton. 2005. Global detection and characterization of hypothetical proteins in Shewanella oneidensis MR-1 using LC-MS-based proteomics. Proteomics 5: 3120– 3130.

49. Elias, D. A.,, M. E. Monroe,, R. D. Smith,, J. K. Fredrickson, and, M. S. Lipton. 2006. Confirmation of the expression of a large set of conserved hypothetical proteins in Shewanella oneidensis MR-1. J. Microbiol. Methods 66: 223– 233.

50. Elias, D. A.,, L. R. Krumholz,, D. Wong,, P. E. Long, and, J. M. Suflita. 2003. Characterization of microbial activities and U reduction in a shallow aquifer contaminated by uranium mill tailings. Microb. Ecol. 46: 83– 91.

51. Elias, D. A.,, J. M. Suflita,, M. J. Mcinerney, and, L. R. Krumholz. 2004. Periplasmic cytochrome c3 of Desulfovibrio vulgaris is directly involved in H 2-mediated metal but not sulfate reduction. Appl. Environ. Microbiol. 70: 413– 420.

52. Elias, D. A.,, S. L. Tollakson,, D. W. Kennedy,, H. M. Mottaz,, C. S. Giometti,, J. S. McLean,, E. A. Hill,, G. E. Pinchuk,, M. S. Lipton,, J. K. Fredrickson, and, Y. A. Gorby. 2008. The influence of cultivation methods on Shewanella oneidensis physiology and proteome expression. Arch. Microbiol. 189: 313– 324.

53. 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.

54. Galushko, A. S.,, and B. Schink. 2000. Oxidation of acetate through reactions of the citric acid cycle by Geobacter sulfurreducens in pure culture and in syntrophic coculture. Arch. Microbiol. 174: 314– 321.

55. Goulhen, F.,, A. Gloter,, F. Guyot, and, M. Bruschi. 2005. Cr(VI) detoxification by Desulfovibrio vulgaris strain Hildenborough: microbe–metal interactions studies. Appl. Microbiol. Biotechnol. 71: 892– 897.

56. Gourion, B.,, S. Sulser,, J. Frunzke,, A. Francez-Charlot,, P. Stiefel,, G. Pessi,, J. A. Vorholt, and, H. M. Fischer. 2009. The PhyR-sigma(EcfG) signalling cascade is involved in stress response and symbiotic efficiency in Bradyrhizobium japonicum. Mol. Microbiol. 73: 291– 305.

57. Guedon, E.,, C. M. Moore,, Q. Que,, T. Wang,, R. W. Ye, and, J. D. Helmann. 2003. The global transcriptional response of Bacillus subtilis to manganese involves the MntR, Fur, TnrA and σB regulons. Mol. Microbiol. 49: 1477– 1491.

58. Harvey, R. W.,, R. L. Smith, and, L. George. 1984. Effect of organic contamination upon microbial distributions and heterotrophic uptake in a Cape Cod, Mass, aquifer. Appl. Environ. Microbiol. 48: 1197– 1202.

59. Haveman, S. A.,, V. Brunelle,, J. K. Voordouw,, G. Voordouw,, J. F. Heidelberg, and, R. Rabus. 2003. Gene expression analysis of energy metabolism mutants of Desulfovibrio vulgaris Hildenborough indicates an important role for alcohol dehydrogenase. J. Bacteriol. 185: 4345– 4353.

60. Hazen, T. C.,, L. Jimenez,, G. L. d. Victoria, and, C. B. Fliermans. 1991. Comparison of bacteria from deep subsurface sediment and adjacent groundwater. Microbial Ecol. 22: 293– 304.

61. He, Q.,, Z. He,, D. C. Joyner,, M. Joachimiak,, M. N. Price,, Z. K. Yang,, H.-C. Yen,, C. L. Hemme,, R. Chakraborty,, W. Chen,, M. W. Fields,, D. A. Stahl,, J. D. Keasling,, M. Keller,, A. P. Arkin,, T. C. Hazen,, J. D. Wall, and, J. Zhou. Impact of elevated nitrate on sulfate-reducing bacteria: implications of inhibitory mechanisms in addition to osmotic stress. J. Bacteriol., in review.

62. He, Q., et al. 2010. Impact of elevated nitrate on sulfate-reducing bacteria: a comparative study of Desulfovibrio vulgaris. ISME J. 4: 1386– 1397.

63. He, Q.,, K. H. Huang,, Z. He,, E. J. Alm,, M. W. Fields,, T. C. Hazen,, A. P. Arkin,, J. D. Wall, and, J. Zhou. 2006. Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough, inferred from global transcriptional analysis. Appl. Environ. Microbiol. 72: 4370– 4381.

64. He, Z.,, L. Wu,, M. W. Fields, and, J. Zhou. 2005. Comparison of microarrays with different probe sizes for monitoring gene expression. Appl. Environ. Microbiol. 71: 5154– 5162.

65. Heidelberg, J. F., et al. 2004. The genome sequence of the anaerobic sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat. Biotechnol. 22: 554– 559.

66. Hoffmann, T.,, N. Frankenberg,, M. Marino, and, D. Jahn. 1998. Ammonification in Bacillus subtilis utilizing dissimilatory nitrite reductase is dependent on resDE. J. Bacteriol. 180: 186– 189.

67. Holman, H. Y. N.,, E. Wozei,, L. Comolli,, Z. Lin,, S. Boglin,, K. H. Downing,, M. W. Fields, and, T. C. Hazen. 2009. Real-time monitoring of hydrogen-bond dynamics during oxygen-stress adaptive response in strict anaerobes. Proc. Natl. Acad. Sci. USA 106: 12599– 12604.

68. Holmes, D. E.,, S. K. Chaudhuri,, K. P. Nevin,, T. Mehta,, B. A. Methe,, A. Liu,, J. E. Ward,, T. L. Woodard,, J. Webster, and, D. R. Lovley. 2006. Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ. Microbiol. 8: 1805– 1815.

69. Holmes, D. E.,, T. Mester,, R. A. O’Neil,, L. A. Perpetua,, M. J. Larrahondo,, R. Glaven,, M. L. Sharma,, J. E. Ward,, K. P. Nevin, and, D. R. Lovley. 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.

70. Holmes, D. E.,, K. P. Nevin, and, D. R. Lovley. 2004. In situ expression of nif D in Geobacteraceae in subsurface sediments. Appl. Environ. Microbiol. 70: 7251– 7259.

71. Holmes, D. E.,, R. A. O’Neil,, M. A. Chavan,, L. A. N’Guessan,, H. A. Vrionis,, L. A. Perpetua,, M. J. Larrahondo,, R. DiDonato,, A. Liu, and, D. R. Lovley. 2009. Transcriptome of Geobacter uraniireducens growing in uranium-contaminated subsurface sediments. ISME J. 3: 216– 230.

72. Hu, P.,, E. L. Brodie,, Y. Suzuki,, H. H. McAdams, and, G. L. Andersen. 2005. Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J. Bacteriol. 187: 8437– 8449.

73. Jin, Y. H.,, P. E. Dunlap,, S. J. McBride,, H. Al-Refai,, P. R. Bushel, and, J. H. Freedman. 2008. Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet. 4: e1000053

74. 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.

75. Karlin, S.,, L. Brocchieri,, J. Mrazek, and, D. Kaiser. 2006. Distinguishing features of δ- Proteo-bacterial genomes. Proc. Natl. Acad. Sci. USA 103: 11352– 11357.

76. Kasprzak, K. S. 2002. Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radic. Biol. Med. 32: 958– 967.

77. Kerr-Wall, P.,, J. Leebens-Mack,, A. S. Chanderbali,, A. Barakat,, E. Wolcott,, H. Liang,, L. Landherr,, L. P. Tomsho,, Y. Hu,, J. E. Carlson,, H. Ma,, S. C. Schuster,, D. E. Soltis,, P. S. Soltis,, N. Altman, and, C. W. dePamphilis. 2009. Comparison of next generation sequencing technologies for transcriptome characterization. BMC Genomics 10: 347.

78. Khare, T.,, A. Esteve-Núñez,, K. P. Nevin,, W. Zhu,, J. R. Yates,, D. Lovley and, C. S. Giometti. 2006. Differential protein expression in the metal-reducing bacterium Geobacter sulfurreducens strain PCA grown with fumarate or ferric citrate. Proteomics 6: 632– 640.

79. Klonowska, A.,, M. E. Clark,, S. B. Thieman,, B. J. Giles,, J. D. Wall, and, M. W. Fields. 2008. Hexavalent chromium reduction in Desulfovibrio vulgaris Hildenborough causes transitory inhibition of sulfate reduction and cell growth. Appl. Microbiol. Biotechnol. 78: 1007– 1016.

80. Klonowska, A.,, Z. He,, Q. He,, M. E. Clark,, S. B. Thieman,, T. C. Hazen,, E. J. Alm,, H.-Y. Holman,, A. P. Arkin,, J. D. Wall,, J. Zhou, and, M. W. Fields. 2006. Global transcriptomic analysis of chromium(VI) exposure of Desulfovibrio vulgaris Hildenborough under sulfate-reducing conditions. Abstract K-052. Gen. Meet. Am. Soc. Microbiol. American Society for Microbiology, Washington, DC.

81. Kolbel-Boelke, J.,, E. M. Anders, and, A. Nehrkorn. 1988. Microbial communities in the saturated groundwater environment. Diversity of bacterial communities in a pleistocene sand aquifer and their in vitro activities. Microb. Ecol. 16: 31– 48.

82. Kolker, E.,, K. S. Makarova,, S. Shabalina,, A. F. Picone,, S. Purvine,, T. Holzman,, T. Cherny,, D. Armbruster,, R. S. Munson,, G. Kolesov,, D. Frishman, and, M. Y. Galperin. 2004. Identification and functional analysis of hypothetical genes expressed in Haemophilus influenzae. Nucleic Acids Res. 32: 2353– 2361.

83. Kreuzer, C. S.,, M. Blackledge,, A. Dolla,, D. Marion, and, F. Guerlesquin. 1998. Tyrosine 64 of cytochrome c553 is required for electron exchange with formate dehydrogenase in Desulfovibrio vulgaris Hildenborough. Biochemistry 37: 8331– 8340.

84. Krushkal, J.,, B. Yan,, L. N. DiDonato,, M. Puljic,, K. P. Nevin,, T. L. Woodard,, R. M. Adkins,, B. A. Methé, and, D. R. Lovley. 2007. Genome-wide expression profiling in Geobacter sulfurreducens: identification of Fur and RpoS transcription regulatory sites in a relGsu mutant. Funct. Integr. Genomics 7: 229– 255.

85. Leang, C.,, M. V. Coppi, and, D. R. Lovley. 2003. OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 185: 2096– 2103.

86. Lehman, R. M.,, and S. P. O’Connell. 2002. Comparison of extracellular enzyme activities and community composition of attached and free-living bacteria in porous medium columns. Appl. Environ. Microbiol. 68: 1569– 1575.

87. Lies, D. P.,, M. E. Hernandez,, A. Kappler,, R. E. Mielke,, J. A. Gralnick, and, D. K. Newman. 2005. Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl. Environ. Microbiol. 71: 4414– 4426.

88. 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.

89. Lloyd, J. R. 2003. Microbial reduction of metals and radionuclides. FEMS Microbiol. Rev. 27: 411– 425.

90. 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.

91. Lourenco, R. F.,, and S. L. Gomes. 2009. The transcriptional response to cadmium, organic hydroperoxide, singlet oxygen and UV-A mediated by the sigma(E)-ChrR system in Caulobacter crescentus. Mol. Microbiol. 72: 1159– 1170.

92. Lovley, D. R.,, E. E. Roden,, E. J. P. Phillips, and, J. C. Woodward. 1993a. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Marine Geol. 113: 41– 53.

93. Lovley, D. R.,, P. K. Widman,, J. C. Woodward, and, E. J. P. Phillips. 1993b. Reduction of uranium by cytochrome c 3 of Desulfovibrio vulgaris. Appl. Environ. Microbiol. 59: 3572– 3576.

94. Mahadevan, R.,, B. Yan,, B. Postier,, K. P. Nevin,, T. L. Woodard,, R. O’Neil,, M. V. Coppi,, B. A. Methé, and, J. Krushkal. 2008. Characterizing regulation of metabolism in Geobacter sulfurreducens through genome-wide expression data and sequence analysis. OMICS 12: 33– 59.

95. Marshall, K. C. 1992. Planktonic versus sessile life of prokaryotes, p. 262–275. In A. Balows,, H. G. Truper,, M. Dworkin,, W. Harder, and, K.-H. Schleifer (ed.), The Prokaryotes: a Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications. Springer-Verlag, Berlin, Germany.

96. Masse, E.,, C. K. Vanderpool, and, S. Gottesman. 2005. Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol. 187: 6962– 6971.

97. McLean, J. S.,, P. D. Majors,, C. L. Reardon,, C. L. Bilskis,, S. B. Reed,, M. F. Romine, and, J. K. Fredrickson. 2008. Investigations of structure and metabolism within Shewanella oneidensis MR-1 biofilms. J. Microbiol. Methods 74: 47– 56.

98. McKinley, J. P.,, J. M. Zachara,, S. Smith, and, G. D. Turner. 1995. The influence of uranyl hydrolysis and multiple site-binding reactions on adsorption of U(VI) to montmorillonite. Clays Clay Miner. 43: 586– 598.

99. Mehta, T.,, M. V. Coppi,, S. E. Childers, and, D. R. Lovley. 2005. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71: 8634– 8641.

100. Methe, B. A.,, K. E. Nelson,, J. A. Eisen,, I. T. Paulsen,, W. Nelson,, J. F. Heidelberg,, D. Wu,, M. Wu,, N. Ward,, M. J. Beanan,, R. J. Dodson,, R. Madupu,, L. M. Brinkac,, S. C. Daugherty,, R. T. DeBoy,, A. S. Durkin,, M. Gwinn,, J. F. Kolonay,, S. A. Sullivan,, D. H. Haft,, J. Selengut,, T. M. Davidsen,, N. Zafar,, O. White,, B. Tran,, C. Romero,, H. A. Forberger,, J. Weidman,, H. Khouri,, T. V. Feldblyum,, T. R. Utterback,, S. E. Van Aken,, D. R. Lovley, and, C. M. Fraser. 2003. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302: 1967– 1969.

101. Methe, B. A.,, J. Webster,, K. P. Nevin,, J. Butler, and, D. R. Lovley. 2005. DNA microarray analysis of nitrogen fixation and Fe(III) reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71: 2530– 2538.

102. Mouser, P. J.,, D. E. Holmes,, L. A. Perpetua,, R. DiDonato,, B. Postier,, A. Liu, and, D. R. Lovley. 2009. Quantifying expression of Geobacter spp. oxidative stress genes in pure culture and during in situ uranium bioremediation. ISME J. 3: 454– 465.

103. Mugerfeld, I.,, B. A. Law,, G. S. Wickham, and, D. K. Thompson. 2009. A putative azoreductase gene is involved in the Shewanella oneidensis response to heavy metal stress. Appl. Microbiol. Biotechnol. 82: 1131– 1141.

104. Mukhopadhyay, A.,, Z. He,, E. J. Alm,, A. P. Arkin,, E. E. Baidoo,, S. C. Borglin,, W. Chen,, T. C. Hazen,, Q. He,, H. Y. Holman,, K. Huang,, R. Huang,, D. C. Joyner,, N. Katz,, M. Keller,, P. Oeller,, A. Redding,, J. Sun,, J. D. Wall,, J. Wei,, Z. Yang,, H.-C. Yen,, J. Zhou, and, J. D. Keasling. 2006. Salt stress in Desulfovibrio vulgaris Hildenborough: an integrated genomics approach. J. Bacteriol. 188: 4068– 4078.

105. 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.

106. Mukhopadhyay, P.,, M. Zheng,, L. A. Bedzyk,, R. A. LaRossa, and, G. Storz. 2004. Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc. Natl. Acad. Sci. USA 101: 745– 750.

107. Myers, C. R.,, and J. M. Myers. 1997. Cloning and sequence of cym A, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J. Bacteriol. 179: 1143– 1152.

108. Myers, C. R.,, and J. M. Myers. 2002. MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl. Environ. Microbiol. 68: 5585– 5594.

109. Nealson, K. H.,, A. Belz, and, B. McKee. 2002. Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek. 81: 215– 222.

110. Nie, L.,, G. Wu, and, W. Zhang. 2006. Correlation between mRNA and protein abundance in Desulfovibrio vulgaris: a multiple regression to identify sources of variations. Biochem. Biophys. Res. Commun. 339: 603– 610.

111. Nunez, C.,, A. Esteve-Nunez,, C. Giometti,, S. Tollaksen,, T. Khare,, W. Lin,, D. R. Lovley, and, B. A. Methe. 2006. DNA microarray and proteomic analyses of the RpoS regulon in Geobacter sulfurreducens. J. Bacteriol. 188: 2792– 2800.

112. Odom, J. M.,, and H. D. Peck. 1981. Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp. FEMS Microbiol. Lett. 12: 47– 50.

113. Odom, J. D.,, and H. D. Peck. 1984. Hydrogenase, electron transfer proteins, and energy coupling in the sulfate-reducing bacteria Desulfovibrio. Annu. Rev. Microbiol. 38: 551– 592.

114. O’Neil, R. A.,, D. E. Holmes,, M. V. Coppi,, L. A. Adams,, M. J. Larrahondo,, J. E. Ward,, K. P. Nevin,, T. L. Woodard,, H. A. Vrionis,, A. L. N’Guessan, and, D. R. Lovley. 2008. Gene transcript analysis of assimilatory iron limitation in Geobacteraceae during groundwater bioremediation. Environ. Microbiol. 10: 1218– 1230.

115. Park, H. S.,, S. Lin, and, G. Voordouw. 2008. Ferric iron reduction by Desulfovibrio vulgaris Hildenborough wild type and energy metabolism mutants. Antonie Van Leeuwenhoek 93: 79– 85.

116. Payne, R. B.,, L. Casalot,, T. Rivere,, J. H. Terry,, L. Larsen,, B. J. Giles, and, J. D. Wall. 2004. Interaction between uranium and the cytochrome c 3 of Desulfovibrio desulfuricans strain G20. Arch. Microbiol. 181: 398– 406.

117. Pereira, P. M.,, Q. He,, F. M. A. Valente,, A. V. Xavier,, J. Zhou,, I. A. C. Pereira, and, R. O. Louro. 2008a. Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis. Antonie Van Leeuwenhoek 93: 347– 362.

118. Pereira, P. M.,, Q. He,, A. V. Xavier,, J. Zhou,, I. A. C. Pereira, and, R. O. Louro. 2008b. Transcriptional response of Desulfovibrio vulgaris Hildenborough to oxidative stress mimicking environmental conditions. Arch. Microbiol. 189: 451– 461.

119. Pitts, K. E.,, P. S. Dobbin,, F. Reyes-Ramirez,, A. J. Thomson,, D. J. Richardson, and, H. E. Seward. 2003. Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA: expression in Escherichia coli confers the ability to reduce soluble Fe(III) chelates. J. Biol. Chem. 278: 27758– 27765.

120. Pohorelic, B. K. J.,, J. K. Voordoouw,, E. Lojou,, A. Dolla,, J. Harder, and, G. Voordouw. 2002. Effects of deletion of genes encoding Fe-only hydrogenase of Desulfovibrio vulgaris Hildenborough on hydrogen and lactate metabolism. J. Bacteriol. 184: 679– 686.

121. Reardon, C. L.,, D. E. Cummings,, L. M. Petzke,, B. L. Kinsall,, D. B. Watson,, B. M. Peyton, and, G. G. Geesey. 2004. Composition and diversity of microbial communities recovered from surrogate minerals incubated in an acidic uranium-contaminated aquifer. Appl. Environ. Microbiol. 70: 6037– 6046.

122. Rhee, S. K.,, X. Liu,, L. Wu,, S. C. Chong,, X. Wan, and, J. Zhou. 2004. Detection of biodegradation and biotransformation genes in microbial communities using 50-mer oligonucleotide micro-arrays. Appl. Environ. Microbiol. 70: 4303– 4317.

123. Richter, H.,, K. P. Nevin,, H. F. Jia,, D. A. Lowy,, D. R. Lovley, and, L. M. Tender. 2009. Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer. Energy Environ. Sci. 2: 506– 516.

124. Risso, C.,, B. A. Methe,, H. Elifantz,, D. E. Holmes, and, D. R. Lovley. 2008. Highly conserved genes in Geobacter species with expression patterns indicative of acetate limitation. Microbiology 154: 2589– 2599.

125. Rittman, B. E. 1993. The significance of biofilms in porous media. Water Res. 29: 2195– 2202.

126. Robey, M.,, and N. P. Cianciotto. 2002. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 70: 5659– 5669.

127. Rodionov, D. A.,, I. Dubchak,, A. P. Arkin,, E. Alm, and, M. S. Gelfand. 2004. Reconstruction of regulatory and metabolic pathways in metal-reducing δ-proteobacteria. Genome Biol. 5: R90.

128. Rollefson, J. B.,, C. E. Levar, and, D. R. Bond. 2009. Identification of genes involved in biofilm formation and respiration via mini-Himar transposon mutagenesis of Geobacter sulfurreducens. J. Bacteriol. 191: 4207– 4217.

129. Rose, R. W.,, T. Bruser,, J. C. Kissinger, and, M. Pohlschroder. 2002. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol. 45: 943– 950.

130. Saeed, A. I.,, V. Sharov,, J. White,, J. Li,, W. Liang,, N. Bhagabati,, J. Braisted,, M. Klapa,, T. Currier,, M. Thiagarajan,, A. Sturn,, M. Snuffin,, A. Rezantsev,, D. Popov,, A. Ryltsov,, E. Kostukovich,, I. Borisovsky,, Z. Liu,, A. Vinsavich,, V. Trush, and, J. Quackenbush. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374– 378.

131. Saffarini, D. A.,, R. Schultz, and, A. Beliaev. 2003. Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J. Bacteriol. 185: 3668– 3671.

132. 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.

133. Shelobolina, E. S.,, M. V. Coppi,, A. A. Korenevsky,, L. N. DiDonato,, S. A. Sullivan,, H. Konishi,, H. Xu,, C. Leang,, J. E. Butler,, B. C. Kim, and, D. R. Lovley. 2007. Importance of c-type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiol. 7: 16.

134. Shi, L.,, B. Chen,, Z. Wang,, D. A. Elias,, M. U. Mayer,, Y. A. Gorby,, S. Ni,, B. H. Lower,, D. W. Kennedy,, D. S. Wunschel,, H. M. Mottaz,, M. J. Marshall,, E. A. Hill,, A. S. Beliaev,, J. M. Zachara,, J. K. Fredrickson, and, T. C. Squier. 2006. Isolation of high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J. Bacteriol. 188: 4705– 4714.

135. Shi, L.,, S. Deng,, M. J. Marshall,, Z. Wang,, D. W. Kennedy,, A. Dohnalkova,, H. M. Mottaz,, E. A. Hill,, Y. A. Gorby,, A. S. Beliaev,, D. J. Richardson,, J. M. Zachara, and, J. K. Fredrickson. 2008. Direct involvement of type II secretion system in extracellular translocation of Shewanella oneidensis outer membrane cytochromes MtrC and OmcA. J Bacteriol. 190: 5512– 5516.

136. Shi, L.,, T. C. Squier,, J. M. Zachara, and, J. K. Fredrickson. 2007. Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65: 12– 20.

137. Smith, R. L. 2002. Determining the terminal electron-accepting reaction in the saturated subsurface, p. 743–752. In C. J. Hurst (ed.), Manual of Environmental Microbiology, 2nd ed. American Society for Microbiology, Washington, DC.

138. Stams, A. J. M.,, and C. M. Plugge. 2009. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7: 568– 577.

139. Stearns, D. M.,, L. J. Kennedy,, K. D. Courtney,, P. H. Giangrande,, L. S. Phieffer, and, K. E. Wetterhahn. 1995. Reduction of chromium(V1) by ascorbate leads to chromium–DNA binding and DNA strand breaks in vitro. Biochemistry 34: 910– 919.

140. Stolyar, S.,, S. Van Dien,, K. L. Hillesland,, N. Pinel,, T. J. Lie,, J. A. Leigh, and, D. A. Stahl. 2007. Metabolic modeling of a mutualistic microbial community. Mol. Syst. Biol. 3: 92.

141. Sumner, E. R.,, A. Shanmuganathan,, T. C. Sideri,, S. A. Willetts,, J. E. Houghton, and, S. V. Avery. 2005. Oxidative protein damage causes chromium toxicity in yeast. Microbiology 151: 1939– 1948.

142. Suzuki, Y.,, S. D. Kelly,, K. M. Kemner, and, J. F. Banfield. 2005. Direct microbial reduction and subsequent preservation of uranium in natural near-surface sediment. Appl. Environ. Microbiol. 71: 1790– 1797.

143. Suzuki, Y.,, and T. Suko. 2006. Geomicrobiological factors that control uranium mobility in the environment: update on recent advances in the bioremediation of uranium-contaminated sites. J. Mineral. Petrol. Sci. 101: 299– 307.

144. Tang, Y. J.,, A. L. Meadows,, J. Kirby, and, J. D. Keasling. 2007. Anaerobic central metabolic pathways in Shewanella oneidensis MR-1 reinterpreted in the light of isotopic metabolite labeling. J. Bacteriol. 189: 894– 901.

145. Taroncher-Oldedburg, G.,, E. M. Griner,, C. A. Francis, and, B. B. Ward. 2003. Oligonucleotide microarray for the study of functional gene diversity in the nitrogen cycle in the environment. Appl. Environ. Microbiol. 69: 1159– 1171.

146. Taylor, S. W.,, and P. R. Jaffe. 1990. Biofilm growth and the related changes in the physical properties of a porous medium. 1. Experimental investigation. Water Res. 26: 2153– 2159.

147. Teal, T. K.,, D. P. Lies,, B. J. Wold, and, D. K. Newman. 2006. Spatiometabolic stratification of Shewanella oneidensis biofilms. Appl. Environ. Microbiol. 72: 7324– 7330.

148. Thompson, D. K.,, A. S. Beliaev,, C. S. Giometti,, S. L. Tollaksen,, T. Khare,, D. P. Lies,, K. H. Nealson,, H. Lim,, J. Yates III,, C. C. Brandt, and, J. M. Tiedje. 2002. Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis: possible involvement of fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl. Environ. Microbiol. 68: 881– 892.

149. Thöny-Meyer, L. 1997. Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 61: 337– 376.

150. Thormann, K. M.,, R. M. Saville,, S. Shukla,, D. A. Pelletier, and, A. M. Spormann. 2004. Initial phases of biofilm formation in Shewanella oneidensis MR-1. J. Bacteriol. 186: 8096– 8104.

151. Toes, A.-C. M.,, M. H. Daleke,, J. G. Kuenen, and, G. Muyzer. 2008. Expression of copA and cusA in Shewanella during copper stress. Microbiology 154: 2709– 2718.

152. Torres, T. T.,, M. Metta,, B. Ottenwalder, and, C. Schlotterer. 2007. Gene expression profiling by massively parallel sequencing. Genome Res. 18: 172– 77.

153. Valente, F. M.,, A. S. F. Oliveira,, N. Gnadt,, I. Pacheco,, A. V. Coelho,, A. V. Xavier,, M. Teixeira,, C. M. Soares, and, I. A. C. Pereira. 2005. Hydrogenases in Desulfovibrio vulgaris Hildenborough: structural and physiologic characterisation of the membrane-bound [NiFeSe] hydrogenase. J. Biol. Inorg. Chem. 10: 667– 682.

154. Van Loosdrecht, M. C. M.,, J. Lyklema,, W. Norde, and, A. J. B. Zehnder. 1990. Influence of interfaces on microbial activity. Microbiol. Rev. 54: 75– 87.

155. Vargas, M.,, K. Kashefi,, E. L. Blunt-Harris, and, D. R. Lovley. 1998. Microbiological evidence for Fe(III) reduction on early Earth. Nature 395: 65– 67.

156. Vasant, C.,, K. Balamurugan,, R. Rajaram, and, T. Ramasami. 2001. Apoptosis of lymphocytes in the presence of Cr(V) complexes: role in Cr(VI)-induced toxicity. Biochem. Biophys. Res. Commun. 285: 1354– 1360.

157. Viamajala, S.,, B. M. Peyton,, R. K. Sani,, W. A. Apel, and, J. N. Petersen. 2004. Toxic effects of chromium(VI) on anaerobic and aerobic growth of Shewanella oneidensis MR-1. Biotechnol. Prog. 20: 87– 95.

158. Voordouw, G. 2002. Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 184: 5903– 5911.

159. Wackett, L. P.,, A. G. Dodge, and, L. B. M. Ellis. 2004. Microbial genomics and the periodic table. Appl. Environ. Microbiol. 70: 647– 655.

160. Walker, C. B.,, Z. He,, Z. K. Yang,, J. A. Ringbauer,, Q. He,, J. Zhou,, G. Voordouw,, J. D. Wall,, A. P. Arkin,, T. C. Hazen,, S. Stolyar, and, D. A. Stahl. 2009. The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J. Bacteriol. 191: 5793– 5801.

161. Wall, J. D.,, and L. R. Krumholz. 2006. Uranium reduction. Annu. Rev. Microbiol. 60: 149– 166.

162. Wan, X.-F.,, N. C. VerBerkmoes,, L. A. McCue,, D. Stanek,, H. Connelly,, L. J. Hauser,, L. Wu,, X. Liu,, T. Yan,, A. Leaphart,, R. L. Hettich,, J. Zhou, and, D. K. Thompson. 2004. Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J. Bacteriol. 186: 8385– 8400.

163. Washburn, M. P.,, A. Koller,, G. Oshiro,, R. R. Ulaszek,, D. Plouffe,, C. Deciu,, E. Winzeler, and, J. R. Yates III. 2003. Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 100: 3107– 3112.

164. Whitman, W. B.,, D. C. Coleman, and, W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA. 95: 6578– 6583.

165. Wilhelm, B. T.,, and J.-R. Landry. 2009. RNA-Seq—quantitative measurement of expression through massively parallel RNA-sequencing. Methods 48: 249– 257.

166. Wilkins, M. J.,, N. C. VerBerkmoes,, K. H. William,, S. J. Callister,, P. J. Mouser,, H. Elifantz,, A. L. N’Guessan,, B. C. Thomas,, C. D. Nicora,, M. B. Shah,, P. Abraham,, M. S. Lipton,, D. R. Lovley,, R. L. Hettich,, P. E. Long, and, J. F. Banfield. 2009. Proteogenomic monitoring of Geobacter physiology during stimulated uranium bioremediation. Appl. Environ. Microbiol. 75: 6591– 6599.

167. Wilkins, M. J.,, P. L. Wincott,, D. J. Vaughan,, F. R. Livens, and, J. R. Lloyd. 2007. Growth of Geobacter sulfurreducens on poorly crystalline Fe(III) oxyhydroxide coatings. Geomicrobiol. J. 24: 199– 204.

168. Wu, W.,, J. Carley,, T. J. Gentry,, M. A. Ginder-Vogel,, M. Fienen,, T. Mehlhorn,, S. L. Carroll,, M. N. Pace,, J. Nyman,, J. Luo,, M. Gentile,, M. W. Fields,, R. F. Hickey,, B. Gu,, D. B. Watson,, O. Cirpka,, J. Zhou,, S. Fendorf,, P. 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.

169. Wu, W.,, J. Carley,, J. Luo,, M. A. Ginder-Vogel,, E. Cardenas,, M. Leigh,, C. Hwang,, S. D. Kelly,, C. Ruan,, L. Wu,, T. J. Gentry,, K. Lowe,, T. Mehlhorn,, S. L. Carroll,, M. W. Fields,, B. Gu,, D. B. Watson,, K. M. Kemner,, T. Marsh,, J. Tiedje,, J. Zhou,, S. Fendorf,, P. Kitanidis,, P. M. Jardine, and, C. S. Criddle. 2007. Bioreduction of uranium (VI) in situ and stability of immobilized uranium: impact of dissolved oxygen. Environ. Sci. Technol. 41: 5716– 5723.

170. Xiong, Y.,, L. Shi,, B. Chen,, M. U. Mayer,, B. H. Lower,, Y. Londer,, S. Bose,, M. F. Hochella,, J. K. Fredrickson, and, T. C. Squier. 2006. High-affinity binding and direct electron transfer to solid metals by the Shewanella oneidensis MR-1 outer membrane c-type cytochrome OmcA. J. Am. Chem. Soc. 128: 13978– 13979.

171. Yang, Y.,, D. P. Harris,, F. Luo,, W. Xiong,, M. Joachimiak,, L. Wu,, P. Dehal,, J. Jacobsen,, Z. Yang,, A. V. Palumbo,, A. P. Arkin, and, J. Zhou. 2009. Snapshot of iron response in Shewanella oneidensis by gene network reconstruction. BMC Genomics 10: 131.

172. Ye, Q.,, Y. Roh,, B. B. Blair,, C. Zhang,, J. Zhou, and, M. W. Fields. 2004. Isolation and characterization of a novel, alkaliphilic, metal-reducing bacterium, and possible implications for alkaline chemotrophy. Appl. Environ. Microbiol. 70: 5595– 5602.

173. Zhang, W.,, D. E. Culley,, M. Hogan,, L. Vitiritti, and, F. J. Brockman. 2006a. Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Antonie Van Leeuwenhoek 90: 41– 55.

174. Zhang, W.,, D. E. Culley,, L. Nie, and, J. C. M. Scholten. 2007. Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface. Appl. Microbiol. Biotechnol. 76: 447– 457.

175. Zhang, W.,, D. E. Culley,, J. C. M. Scholten,, M. Hogan,, L. Vitiritti, and, F. J. Brockman. 2006b. Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors. Antonie Van Leeuwenhoek 89: 221– 237.

176. Zhou, J.,, and D. K. Thompson. 2002. Challenge in applying microarrays to environmental studies. Curr. Opin. Biotechnol. 13: 204– 207.