DNA microarray analysis of nitrogen fixation and Fe(III) reduction in Geobacter sulfurreducens

Applied and Environmental Microbiology

Volumn 71, Issue 5, 2005, Pages 2530-2538

  Methé, Barbara A ^a   Webster, Jennifer ^a   Nevin, Kelly ^b   Butler, Jessica ^b   Lovley, Derek R ^b  

^a J CRAIG VENTER INSTITUTE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ELECTRONS; GENES; IRON; METABOLISM; PROTEINS; REDUCTION;

ELECTRON DONOR; GEOBACTER; MICROARRAYS;

NITROGEN FIXATION;

ACETIC ACID; CYTOCHROME C; FUMARIC ACID; IRON; NITROGEN;

NITROGEN FIXATION;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL METABOLISM; CONTROLLED STUDY; DNA MICROARRAY; ELECTRON TRANSPORT; GENE EXPRESSION; GENE EXPRESSION PROFILING; GEOBACTER; GEOBACTER SULFURREDUCENS; NITROGEN FIXATION; NONHUMAN; POLYMERASE CHAIN REACTION; REDUCTION;

FERRIC COMPOUNDS; FUMARATES; GEOBACTER; MICROARRAY ANALYSIS; NITROGEN FIXATION; OXIDATION-REDUCTION; POLYMERASE CHAIN REACTION;

GEOBACTER SULFURREDUCENS;

EID: 17644418853     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.5.2530-2538.2005     Document Type: Article

References (70)

1. Anderson, R. T., H. A. Vrionis, I. Ortiz-Bernad, C. T. Resch, A. D. Peacock, 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.
2. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richrdson, M. Ringwald, G. M. Rubin, and G. Sherlock. 2000. Gene ontology: tool for the unification of biology. Nat. Genet. 25:25-29.
3. 2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environ. Microbiol. 2:266-273.
4. Bond, D. R., D. E. Holmes, L. M. Tender, and D. R. Lovley. 2002. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483-485.
5. Bond, D. R., and D. R. Lovley. 2003. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69:1548-1555.
6. Brazma, A., P. Hingamp, J. Quackenbush, G. Sherlock, P. Spellman, C. Stoeckert, J. Aach, W. Ansorge, C. A. Ball, H. C. Causton, T. Gaasterland, P. Glenisson, F. C. P. Holstege, I. F. Kim, V. Markowitz, J. C. Matese, H. Parkinson, A. Robinson, U. Sarkans, S. Schulze-Kremer, J. Stewart, R. Taylor, J. Vilo, and M. Vingron. 2001. Minimum information about a microarray experiment (MIAME) - towards standards for microarray data. Nat. Genet. 29:365-371.
7. Brocklehurst, K. R., S. J. Megit, and A. P. Morby. 2003. Characterisation of CadR from Pseudomonas aeruginosa: a Cd(II)-responsive MerR homologue. Biochem. Biophys. Res. Commun. 308:234-239.
8. Butler, J., and D. R. Lovley. Unpublished data.
9. Butler, J. E., F. Kaufmann, M. V. Coppi, C. Núñez, and D. R. Lovley. 2004. MacA, a diheme c-type cytochrome involved in Fe(III) reduction by Geobacter sulfurreducens. J. Bacteriol. 186:4042-4045.
10. Capone, D. G. 1993. Determination of nitrogenase activity in aquatic samples using the acetylene reduction procedure, p. 621-631. In P. Kemp, B. Sherr, and J. Cole (ed.), Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, Fla.
11. Causton, H., J. Quackenbush, and A. Brazma. 2003. Microarray gene expression data analysis: a beginner's guide, p. 71-130. Blackwell Publishing, Oxford, United Kingdom.
12. Childers, S. E., S. Ciufo, and D. R. Lovley. 2002. Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416:767-769.
13. Chin, K.-J., A. Esteve-Núñez, C. Leang, and D. 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.
14. Coppi, M. V., C. Leang, S. J. Sandler, and D. R. Lovley. 2001. Development of a genetic system for Geobacter sulfurreducens. Appl. Environ. Microbiol. 67:3180-3187.
15. Coppi, M. V., R. A. O'Neil, and D. R. Lovley. 2004. Identification of an uptake hydrogenase required for hydrogen-dependent reduction of Fe(III) and other electron acceptors by Geobacter sulfurreducens. J. Bacteriol. 186:3022-3028.
16. Dixon, R., and D. Kahn. 2004. Genetic regulation of biological nitrogen fixation. Nat. Rev. Microbiol. 2:621-631.
17. Escolar, L., J. Pérez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
18. Esteve-Núñez, A., M. M. Rothermich, M. Sharma, and D. R. Lovley. Growth of Geobacter sulfurreducens under nutrient-limiting conditions in continuous culture. Environ. Microbiol., in press.
19. Franke, S., G. Grass, and D. H. Nies. 2001. The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147:965-972.
20. Goldberg, M., T. Pribyl, S. Juhnke, and D. H. Nies. 1999. Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. J. Biol. Chem. 274:26065-26070.
21. Gottschalk, G. 1986. Bacterial metabolism, 2nd ed. Springer-Verlag, New York, N.Y.
22. Gregory, K., D. Bond, and D. Lovley. 2004. Graphite electrodes as electron donors for anaerobic respiration. Env. Microbiol. 6:596-604.
23. Griggs, D. W., and J. Konisky. 1989. Mechanism for iron-regulated transcription of the Escherichia coli cir gene: metal-dependent binding of Fur protein to the promoters. J. Bacteriol. 171:1048-1054.
24. Gruidl, M. E., T. C. Chen, S. Gargano, A. Storlazzi, A. Cascino, and G. Mosig. 1991. Two bacteriophage T4 base plate genes (25 and 26) and the DNA repair gene uvsY belong to spatially and temporally overlapping transcription units. Virology 184:359-369.
25. Hoch, J. A. 2000. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 3:165-170.
26. Holmes, D., D. Bond, R. A. O'Neil, C. Reimers, L. Tender, and D. R. Lovley. 29 June 2004, posting date. Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb. Ecol. [Online.] http://link.springer.de/link/service/journals/00248/index.htm.
27. Holmes, D., K. T. Finneran, R. A. O'Neil, and D. R. Lovley. 2002. Enrichment of members of the family Geobacteraceae associated with stimulation of dissilmilatory metal reduction in uranium-contaminated aquifer sediments. Appl. Environ. Microbiol. 68:2300-2306.
28. Holmes, D. E., K. P. Nevin, and D. R. Lovley. In situ expression of Geobacteraceae nifD in subsurface sediments. Appl. Environ. Microbiol., in press.
29. Holmes, D. E., J. S. Nicolls, D. R. Bond, and D. R. Lovley. 2004. Potential role of a novel psychrotolerant Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by the marine sediment fuel cell. Appl. Environ. Microbiol., in press.
30. Hosack, D., G. Dennis, Jr., B. Sherman, H. Lane, and R. Lempicki. 11 September 2003, posting date. Identifying biological themes within lists of genes with EASE. Genome Biol. 4:R70. [Online.] doi:10.1186/gb-2003-4-10-r70.
31. Jansen, R., J. van Embden, W. Gaastra, and L. Schouls. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565-1575.
32. Jung, H. 2002. The sodium/substrate symporter family: structural and functional features. FEBS Lett. 529:73-77.
33. Junneman, S. 1997. Cytochrome bd terminal oxidase. Biochim. Biophys. Acta 1321:107-127.
34. Kidd, S. P., and N. L. Brown. 2003. ZccR - a MerR-like regulator from Bordetella pertussis which responds to zinc, cadmium and colbalt. Biochem. Biophys. Res. Commun. 302:697-702.
35. Kim, Se. H., A. B. Chang, and M. H. Saier. 2004. Sequence similarity between multidrug resistance efflux pumps of the ABC and RND superfamilies. Microbiology 150:2493-2495.
36. Kondrashov, F. A., I. B. Rogozin, Y. I. Wolf, and E. V. Koonin. 14 January 2002, posting date. Selection in the evolution of gene duplications. Genome Biol. 3:research0008.1-0008.9. [Online.] doi:10.1186/gb-2002-3-2- research0008.
37. 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.
38. Leang, C., C. Nunez, and D. R. Lovley. Submitted for publication.
39. Lovley, D. R. 1991. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55:259-287.
40. Lovley, D. R. 1995. Microbial reduction of iron, manganese, and other metals. Adv. Agron. 54:175-231.
41. Lovley, D. R. 2003. Cleaning up with genomics: applying molecular biology to bioremediation. Nat. Microbiol. 1:35-44.
42. Lovley, D. R., D. E. Holmes, and K. P. Nevin. 2004. Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49:219-286.
43. Lovley, D. R., and E. J. P. Phillips. 1988. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54:1472-1480.
44. Lovley, D. R., E. J. P. Phillips, Y. A. Gorby, and E. R. Landa. 1991. Microbial reduction of uranium. Nature 350:413-416.
45. 3+ reducing bacterium Geobacter sulfurreducens. FEMS Microbiol. Lett. 185:205-211.
46. Methé, 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. The genome of Geobacter sulfurreducens: insights into metal reduction in subsurface environments. Science 302:1967-1969.
47. Miller, E. S., E. Kutter, G. Mosig, F. Arisaka, T. Kunisawa, and W. Rüger. 2003. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67:86-156.
48. Nascimento, A. M. A., and E. Chartone-Souza. 2003. Operon mer: bacterial resistance to mercury and potential for bioremediation of contaminated environments. Genet. Mol. Res. 2:92-101.
49. Nevin, K., and D. R. Lovley. 2002. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19:141-159.
50. Nevin, K. P., and D. R. Lovley. 2002. Novel mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl. Environ. Microbiol. 68:2294-2299.
51. Newman, D. K., and R. Kolter. 2000. A role for excreted quinones in extracellular electron transfer. Nature 405:93-97.
52. Nies, D. H. 1995. The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J. Bacteriol. 177:2707-2712.
53. Nies, D. H. 1999. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 51:730-750.
54. North, N. N., S. 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.
55. Ortiz-Bernad, I., R. T. Anderson, H. A. Vrionis, and D. R. Lovley. 2004. Vanadium respiration by Geobacter metallireducens: novel strategy for in situ removal of vanadium from groundwater. Appl. Environ. Microbiol. 70:3091-3095.
56. Reitzer, L. 2003. Nitrogen assimilation and global regulation in Escherichia coli. Annu. Rev. Microbiol. 57:155-176.
57. Roling, W. F. M., B. M. van Breukelen, M. Braster, B. Lin, and H. W. van Verseveld. 2001. Relationships between microbial community structure and hydrochemistry in a landfill leachate-polluted aquifer. Appl. Environ. Microbiol. 67:4619-4629.
58. Rooney-Varga, J. N., R. T. Anderson, J. L. Fraga, D. Ringelberg, and D. R. Lovley. 1999. Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 65:3056-3064.
59. Rozen, S., and H. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers, p. 365-386. in S. Krawetz and S. Misener (ed.), Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, N.J.
60. Saier, M. H., and I. T. Paulsen. 2001. Phylogeny of multidrug transporters. Cell Dev. Biol. 12:205-213.
61. Shelobolina, E. S., S. A. Sullivan, M. V. Coppi, C. Leang, L. DiDonato, J. E. Butler, and D. R. Lovley. Unpublished data.
62. Snoeyenbos-West, O., K. Nevin, R. Anderson, and D. R. Lovley. 2000. Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb. Ecol. 39:153-167.
63. Stein, L., M. La Duc, T. Grundl, and K. Nealson. 2001. Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments. Environ. Microbiol. 3:10-18.
64. Storey, J., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100:9440-9445.
65. Tender, L. M., C. E. Reimers, H. A. Stecher, D. E. Holmes, D. R. Bond, D. A. Lowy, K. Pilobello, S. J. Fertig, and D. R. Lovley. 2002. Harnessing microbially generated power on the seafloor. Nat. Biotechnol. 20:821-825.
66. Tseng, T.-T., K. S. Gatwick, J. Kollman, D. Park, D. H. Nies, A. Goffeau, and M. H. Saier. 1999. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol. 1:107-125.
67. Tusher, V., R. Tibshirani, and C. Gilbert. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98:5116-5121.
68. Wang, Y.-D., S. Zhao, and C. W. Hill. 1998. Rhs elements comprise three subfamilies which diverged prior to acquisition by Escherichia coli. J. Bacteriol. 180:4102-4110.
69. Wei, Y., J.-M. Lee, D. Smulski, and R. LaRossa. 2001. Global impact of sdiA amplification revealed by comprehensive gene expression profiling of Escherichia coli. J. Bacteriol. 183:2265-2272.
70. White, D. 2000. The physiology and biochemistry of prokaryotes, 2nd ed. Oxford University Press, New York, N.Y.