Role of geobacter sulfurreducens outer surface c-type cytochromes in reduction of soil humic acid and anthraquinone-2,6-Disulfonate

Applied and Environmental Microbiology

Volumn 76, Issue 7, 2010, Pages 2371-2375

  Voordeckers, James W ^a   Kim, Byoung Chan ^a,b   Izallalen, Mounir ^a   Lovley, Derek R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

C-TYPE CYTOCHROME; EXTRACELLULAR; GEOBACTER SULFURREDUCENS; HUMIC ACID; HUMIC SUBSTANCES; OUTER SURFACE;

KETONES; ORGANIC ACIDS;

GENES;

ANTHRAQUINONE 2,6 DISULFONATE; ANTHRAQUINONE DERIVATIVE; ANTHRAQUINONE-2,6-DISULFONATE; BACTERIAL PROTEIN; CYTOCHROME;

BACTERIUM; CYTOCHROME; ESTER; GENE EXPRESSION; HUMIC ACID; INHIBITION; REDUCTION; SOIL CHEMISTRY;

ARTICLE; BACTERIAL GENE; GENE DELETION; GENETICS; GEOBACTER; HUMIC SUBSTANCE; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; SOIL;

ANTHRAQUINONES; BACTERIAL PROTEINS; CYTOCHROMES; GENE DELETION; GENES, BACTERIAL; GEOBACTER; HUMIC SUBSTANCES; OXIDATION-REDUCTION; SOIL; SOIL MICROBIOLOGY;

GEOBACTER SULFURREDUCENS;

EID: 77950283289     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02250-09     Document Type: Article

References (42)

1. Anderson, R. T., J. N. Rooney-Varga, C. V. Gaw, and D. R. Lovley. 1998 Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleumcontaminated aquifers. Environ. Sci. Technol. 32:1222-1229.
2. Bhushan, B., A. Halasz, and J. Hawari. 2006 Effect of iron(III), humic acids and anthraquinone-2,6-disulfonate on biodégradation of cyclic nitramines by Clostridium sp. EDB2. J. Appl. Microbiol. 100:555-563.
3. Bond, D. R., and D. R. Lovley. 2002 Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ. Microbiol. 4:115-124.
4. Bradley, P. M., and F. H. Chapelle. 1996 Anaerobic mineralization of vinyl chloride in Fe(III)-reducing, aquifer sediments. Environ. Sci. Technol. 30: 2084-2086.
5. Cervantes, F. J., F. A. de Bok, T. Duong-Dac, A. J. Stams, G. Lettinga, and J. A. Field. 2002 Reduction of humic substances by halorespiring, sulphatereducing and methanogenic microorganisms. Environ. Microbiol. 4:51-57.
6. Chen, J., B. Gu, R. A. Royer, and W. D. Burgos. 2003 The roles of natural organic matter in chemical and microbial reduction of ferric iron. Sci. Total Environ. 307:167-178.
7. Coates, J., D. Ellis, E. Blunt-Harris, C. Gaw, E. Roden, and D. R. Lovley. 1998 Recovery of humic-reducing bacteria from a diversity of environments. Appl. Environ. Microbiol. 64:1504-1509.
8. 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.
9. Finneran, K. T., H. M. Forbush, C. V. VanPraagh, and D. R. Lovley. 2002 Desulfltobacterium metallireduc.ens sp. nov., an anaerobic bacterium that couples growth to the reduction of metals and humic acids as well as chlorinated compounds. Int. J. Syst. Evol. Microbiol. 52:1929-1935.
10. Finneran, K. T., and D. R. Lovley. 2001 Anaerobic degradation of methyl tert-butyl ether (MTBE) and tert-butyl alcohol (TBA). Environ. Sci. Technol. 35:1785-1790.
11. He, Q., and R. A. Sanford. 2003 Characterization of Fe(III) reduction by chlororespiring Anaeromxyobacter dehalogenans. Appl. Environ. Microbioi. 69:2712-2718.
12. Holmes, D. E., S. K. Chaudhuri, K. P. Nevin, T. Mehta, B. A. Methé, 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.
13. 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.
14. Kim, B.-C., C. Leang, Y. H. Ding, R. H. Glaven, M. V. Coppi, and D. R. Lovley. 2005 OmcF, a putative c-type monoheme outer membrane cytochrome required for the expression of other outer membrane cytochromes in Geobacter sulfurreducens. J. Bacteriol. 187:4505-4813
15. Leang, C., L. A. Adams, K. J. Chin, K. P. Nevin, B. A. Methé, J. Webster, M. L. Sharma, and D. R. Lovley. 2005 Adaptation to disruption of the electron transfer pathway for Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 187:5918-5926.
16. 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.
17. 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.
18. Lloyd, J. R., C. Leang, A. L. Hodges-Myerson, M. V. Coppi, S. Ciufo, B. A. Metné, S. J. Sandler, and D. R. Lovley. 2003 Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem. J. 369:153-161.
19. Lovley, D. R., J. Coates, E. L. Blunt-Harris, E. J. P. Phillips, and J. C. Woodward. 1996 Humic substances as electron acceptors for microbial respiration. Nature 382:445-448.
20. Lovley, D. R., D. E. Holmes, and K. P. Nevin. 2004 Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49:219-286.
21. Lovley, D. R., K. Kashenfl, M. Vargas, J. M. Tor, and E. L. Blunt-Harris. 2000 Reduction of humic substances and Fe(III) by hyperthermophilic microorganisms. Chem. Geol. 169:289-298.
22. 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.
23. Lovley, D. R., R. Mahadevan, and K. P. Nevin. 2008 Systems biology approach to bioremediation with extracellular electron transfer, p. 71-96. In E. Diaz (ed.), Microbial biodegradation, genomics and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
24. Lovley, D. R., J. C. Woodward, and F. H. Chapelle. 1996 Rapid anaerobic benzene oxidation with a variety of chelated Fe(III) forms. Appl. Environ. Microbiol. 62:288-291.
25. Lujjten, M., S. Weelink, B. Godschalk, A. Langenhoff, M. van Eekert, G. Schraa, and A. Stams. 2004 Anaerobic reduction and oxidation of quinone moieties and the reduction of oxidized metals by halorespiring and related organisms. FEMS Microbiol. Ecol. 49:145-149.
26. Mahadevan, R., D. R. Bond, J. E. Butler, A. Esteve-Nunez, M. V. Coppi, B. O. Palsson, C. H. Schilling, and D. R. Lovley. 2006 Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl. Environ. Microbiol. 72:1558-1568.
27. Mehta, T., S. E. Childers, R. Glaven, D. R. Lovley, and T. Mester. 2006 A putative multicopper protein secreted by an atypical type II secretion system involved in the reduction of insoluble electron acceptors in Geobacter sulfurreducens. Microbiology 152:2257-2264.
28. Mehta, T., M. V. Coppi, S. E. Childers, and D. R. Lovley. 2005 Outer membrane c-type cytochromes required for Fe(III) and Mh(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71:86348641.
29. 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 Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302: 1967-1969.
30. Murphy, K. C., K. G. Campellone, and A. R. Poteete. 2000 PCR-mediated gene replacement in Escherichia coli. Gene 246:321-330.
31. 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-I. Appl. Environ. Microbiol. 68:5585-5594.
32. Nealson, K. H., and D. Saffarini. 1994 Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 48:311-343.
33. Nevin, K. P., B.-C. Kim, R. H. Glaven, J. P. Johnson, T. L. Woodard, B. A. Mettle, J. DiDonato, R. J. S. Covalla, A. Franks, A. Liu, and D. R. Lovley. 2009 Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 4:e5628.
34. Nevin, K. P., and D. R. Lovley. 2002 Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19:141-159.
35. Qian, X., G. Reguera, T. Mester, and D. R. Lovley. 2007 Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins. FEMS Microbiol. Lett. 277:21-27.
36. Reguera, G., K. D. McCarthy, T. Mehta, J. S. Nicoll, M. T. Tuominen, and D. R. Lovley. 2005 Extracellular electron transfer via microbial nanowires. Nature 435:1098-1101.
37. Richter, H., K. P. Nevin, H. 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.
38. Scott, D. T., D. M. McKnight, E. L. Blunt-Harris, S. E. Kolesar, and D. R. Lovley. 1998 Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ. Sci. Technol. 32:2984-2989.
39. 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.
40. Shyu, J. B., D. P. Lies, and D. K. Newman. 2002 Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. J. Bacteriol. 184:1806-1810.
41. Smith, P. K., R. I. Krohn, G. T. Hermanson, A. K. Mallia, F. H. Gartner, E. K. Provenzano, N. M. Fujimoto, B. J. Goeke, and D. C. Klenk. 1985 Measurement of protein using bicinchonic acid. Anal. Biochem. 150:76-85.
42. Weber, K. A., L. A. Achenbach, and J. D. Coates. 2006 Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat. Rev. Microbiol. 4:752-764.