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Respiration of metal (hydr)oxides by Shewanella and Geobacter : a key role for multihaem c ‐type cytochromes

Liang Shi, Thomas C. Squier, John M. Zachara and 1 more

Molecular Microbiology · 2007 · Review

doi:10.1111/j.1365-2958.2007.05783.x

Abstract

Summary Dissimilatory reduction of metal (e.g. Fe, Mn) (hydr)oxides represents a challenge for microorganisms, as their cell envelopes are impermeable to metal (hydr)oxides that are poorly soluble in water. To overcome this physical barrier, the Gram‐negative bacteria Shewanella oneidensis MR‐1 and Geobacter sulfurreducens have developed electron transfer (ET) strategies that require multihaem c ‐type cytochromes ( c ‐Cyts). In S. oneidensis MR‐1, multihaem c ‐Cyts CymA and MtrA are believed to transfer electrons from the inner membrane quinone/quinol pool through the periplasm to the outer membrane. The type II secretion system of S. oneidensis MR‐1 has been implicated in the reduction of metal (hydr)oxides, most likely by translocating decahaem c ‐Cyts MtrC and OmcA across outer membrane to the surface of bacterial cells where they form a protein complex. The extracellular MtrC and OmcA can directly reduce solid metal (hydr)oxides. Likewise, outer membrane multihaem c ‐Cyts OmcE and OmcS of G. sulfurreducens are suggested to transfer electrons from outer membrane to type IV pili that are hypothesized to relay the electrons to solid metal (hydr)oxides. Thus, multihaem c ‐Cyts play critical roles in S. oneidensis MR‐1‐ and G. sulfurreducens ‐mediated dissimilatory reduction of solid metal (hydr)oxides by facilitating ET across the bacterial cell envelope.

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References 47

  1. 1.

    Beliaev AS, Saffarini DA. Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol. 1998;180:6292-6297.

    Not in our library10.1128/jb.180.23.6292-6297.1998

  2. 2.

    Beliaev AS, Saffarini DA, McLaughlin JL, Hunnicutt D. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol. 2001;39:722-730.

    Not in our library10.1046/j.1365-2958.2001.02257.x

  3. 3.

    Biju V, Pan D, Gorby YA, Fredrickson J, McLean J, Saffarini D, Lu HP. Combined spectroscopic and topographic characterization of nanoscale domains and their distributions of a redox protein on bacterial cell surfaces. Langmuir. 2007;23:1333-1338.

    Not in our library10.1021/la061343z

  4. 4.

    Bouhenni R, Gehrke A, Saffarini D. Identification of genes involved in cytochrome c biogenesis in Shewanella oneidensis, using a modified mariner transposon. Appl Environ Microbiol. 2005;71:4935-4937.

    Not in our library10.1128/aem.71.8.4935-4937.2005

  5. 5.

    Clarke TA, Dennison V, Seward HE, Burlat B, Cole JA, Hemmings AM, Richardson DJ. Purification and spectropotentiometric characterization of Escherichia coli NrfB, a decaheme homodimer that transfers electrons to the decaheme periplasmic nitrite reductase complex. J Biol Chem. 2004;279:41333-41339.

    Not in our library10.1074/jbc.m407604200

  6. 6.

    Cunha CA, Macieira S, Dias JM, Almeida G, Goncalves LL, Costa C, et al. Cytochrome c nitrite reductase from Desulfovibrio desulfuricans ATCC 27774. The relevance of the two calcium sites in the structure of the catalytic subunit (NrfA). J Biol Chem. 2003;278:17455-17465.

    Not in our library10.1074/jbc.m211777200

  7. 7.

    DiChristina TJ, Moore CM, Haller CA. 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. 2002;184:142-151.

    Not in our library10.1128/jb.184.1.142-151.2002

  8. 8.

    Filloux A. The underlying mechanisms of type II protein secretion. Biochim Biophys Acta. 2004;1694:163-179.

    Not in our library10.1016/j.bbamcr.2004.05.003

  9. 9.

    Francetic O, Pugsley AP. Towards the identification of type II secretion signals in a nonacylated variant of pullulanase from Klebsiella oxytoca. J Bacteriol. 2005;187:7045-7055.

    Not in our library10.1128/jb.187.20.7045-7055.2005

  10. 10.

    Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA. 2006;103:11358-11363.

    Not in our library10.1073/pnas.0604517103

  11. 11.

    Gralnick JA, Vali H, Lies DP, Newman DK. Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci USA. 2006;103:4669-4674.

    Not in our library10.1073/pnas.0505959103

  12. 12.

    Han D, Morgan JE, Gennis RB. G204D, a mutation that blocks the proton-conducting d-channel of the aa3-type cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry. 2005;44:12767-12774.

    Not in our library10.1021/bi051141m

  13. 13.

    Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol. 2002;20:1118-1123.

    Not in our library10.1038/nbt749

  14. 14.

    Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, et al. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol. 2004;22:554-559.

    Not in our library10.1038/nbt959

  15. 15.

    Hernandez ME, Newman DK. Extracellular electron transfer. Cell Mol Life Sci. 2001;58:1562-1571.

    Not in our library10.1007/pl00000796

  16. 16.

    Leys D, Scrutton NS. Electrical circuitry in biology: emerging principles from protein structure. Curr Opin Struct Biol. 2004;14:642-647.

    Not in our library10.1016/j.sbi.2004.10.002

  17. 17.

    Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK. 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. 2005;71:4414-4426.

    Not in our library10.1128/aem.71.8.4414-4426.2005

  18. 18.

    Lovley DR. Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol. 2006;4:497-508.

    Not in our library10.1038/nrmicro1442

  19. 19.

    Lovley DR, Phillips EJ. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol. 1988;54:1472-1480.

    Not in our library10.1128/aem.54.6.1472-1480.1988

  20. 20.

    Lower BH, Shi L, Yongsunthon R, Droubay TC, McCready DE, Lower SK. Dynamic force spectroscopy of individual bonds that form between an iron oxide surface and outer membrane cytochromes OmcA and MtrC from Shewanella oneidensis. J Bacteriol. 2007.

    Not in our library10.1128/jb.01518-06

  21. 21.

    Maier TM, Myers JM, Myers CR. Identification of the gene encoding the sole physiological fumarate reductase in Shewanella oneidensis MR-1. J Basic Microbiol. 2003;43:312-327.

    Not in our library10.1002/jobm.200390034

  22. 22.
  23. 23.

    Mehta T, Coppi MV, Childers SE, Lovley DR. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol. 2005;71:8634-8641.

    Not in our library10.1128/aem.71.12.8634-8641.2005

  24. 24.

    Mehta T, Childers SE, Glaven R, Lovley DR, Mester T. A putative multicopper protein secreted by an atypical type II secretion system involved in the reduction of insoluble electron acceptors in Geobacter sulfurreducens. Microbiology. 2006;152:2257-2264.

    Not in our library10.1099/mic.0.28864-0

  25. 25.

    Methe BA, Nelson KE, Eisen JA, Paulsen IT, Nelson W, Heidelberg JF, et al. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science. 2003;302:1967-1969.

    Not in our library10.1126/science.1088727

  26. 26.

    Mowat CG, Chapman SK. Multi-heme cytochromes – new structures, new chemistry. Dalton Trans. 2005;7:3381-3389.

    Not in our library10.1039/b505184c

  27. 27.

    Myers CR, Myers JM. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J Bacteriol. 1997;179:1143-1152.

    Not in our library10.1128/jb.179.4.1143-1152.1997

  28. 28.

    Myers CR, Myers JM. MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl Environ Microbiol. 2002b;68:5585-5594.

    Not in our library10.1128/aem.68.11.5585-5594.2002

  29. 29.

    Myers CR, Myers JM. Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett Appl Microbiol. 2003a;37:254-258.

    Not in our library10.1046/j.1472-765x.2003.01389.x

  30. 30.

    Myers CR, Myers JM. The outer membrane cytochromes of Shewanella oneidensis MR-1 are lipoproteins. Lett Appl Microbiol. 2004;39:466-470.

    Not in our library10.1111/j.1472-765x.2004.01611.x

  31. 31.

    Myers CR, Nealson KH. Bacterial manganese reduction and growth with manganese oxides as the sole electron acceptor. Science. 1988;240:1319-1321.

    Not in our library10.1126/science.240.4857.1319

  32. 32.

    Myers JM, Myers CR. Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J Bacteriol. 2000;182:67-75.

    Not in our library10.1128/jb.182.1.67-75.2000

  33. 33.

    Myers JM, Myers CR. Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol. 2001;67:260-269.

    Not in our library10.1128/aem.67.1.260-269.2001

  34. 34.

    Myers JM, Myers CR. Genetic complementation of an outer membrane cytochrome omcB mutant of Shewanella putrefaciens MR-1 requires omcB plus downstream DNA. Appl Environ Microbiol. 2002a;68:2781-2793.

    Not in our library10.1128/aem.68.6.2781-2793.2002

  35. 35.

    Myers JM, Myers CR. Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese(IV) oxide. Lett Appl Microbiol. 2003b;37:21-25.

    Not in our library10.1046/j.1472-765x.2003.01338.x

  36. 36.

    Pitts KE, Dobbin PS, Reyes-Ramirez F, Thomson AJ, Richardson DJ, Seward HE. 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. 2003;278:27758-27765.

    Not in our library10.1074/jbc.m302582200

  37. 37.

    Prescott LM, Harley JP, Klein DA. The prokaryotic cell wall. Microbiology. 1996;51.

    Not in our library

  38. 38.

    Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. Extracellular electron transfer via microbial nanowires. Nature. 2005;435:1098-1101.

    Not in our library10.1038/nature03661

  39. 39.

    Riegler D, Shroye L, Pokalsky C, Zaslavsky D, Gennis R, Prochaska LJ. Characterization of steady-state activities of cytochrome c oxidase at alkaline pH: mimicking the effect of K-channel mutations in the bovine enzyme. Biochim Biophys Acta. 2005;1706:126-133.

    Not in our library10.1016/j.bbabio.2004.10.002

  40. 40.

    Rodrigues ML, Oliveira TF, Pereira IA, Archer M. X-ray structure of the membrane-bound cytochrome c quinol dehydrogenase NrfH reveals novel haem coordination. EMBO J. 2006;25:5951-5960.

    Not in our library10.1038/sj.emboj.7601439

All 47 references

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