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Biochemistry (Moscow)

, Volume 79, Issue 13, pp 1584–1601 | Cite as

Structural and functional studies of multiheme cytochromes c involved in extracellular electron transport in bacterial dissimilatory metal reduction

  • T. V. TikhonovaEmail author
  • V. O. Popov
Review

Abstract

Bacteria utilizing insoluble mineral forms of metal oxides as electron acceptors in respiratory processes are widespread in the nature. The electron transfer from a pool of reduced quinones in the cytoplasmic membrane across the periplasm to the bacterial outer membrane and then to an extracellular acceptor is a key step in bacterial dissimilatory metal reduction. Multiheme cytochromes c play a crucial role in the extracellular electron transfer. The bacterium Shewanella oneidensis MR-1 was used as a model organism to study the mechanism of extracellular electron transport. In this review, we discuss recent data on the composition, structures, and functions of multiheme cytochromes c and their functional complexes responsible for extracellular electron transport in Shewanella oneidensis.

Key words

bacterial dissimilatory metal reduction extracellular electron transfer multiheme cytochrome c 

Abbreviations

BDMR

bacterial dissimilatory metal reduction

ETC

electron transport chain

Fe-NTA

iron nitrilotriacetate

OMC

outer-membrane cytochrome c

rmsd

root-meansquare deviation

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References

  1. 1.
    Balashova, V. V., and Zavarzin, G. A. (1980) Anaerobic reduction of ferric iron by hydrogen bacteria, Microbiology, 48, 635–639.Google Scholar
  2. 2.
    Lovley, D. R., and Phillips, E. J. (1987) Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments, Appl. Environ. Microbiol., 53, 2636–2641.PubMedCentralPubMedGoogle Scholar
  3. 3.
    Lovley, D. R., and Phillips, E. J. (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese, Appl. Environ. Microbiol., 54, 1472–1480.PubMedCentralPubMedGoogle Scholar
  4. 4.
    Gralnick, J. A., and Newman, D. K. (2007) Extracellular respiration, Mol. Microbiol., 65, 1–11.PubMedCentralPubMedGoogle Scholar
  5. 5.
    Chiorse, W. C. (1984) Biology of iron-depositing and manganese-depositing bacteria, Ann. Rev. Microbiol., 38, 515–550.Google Scholar
  6. 6.
    Myers, C. R., and Nealson, K. H. (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor, Science, 240, 1319–1321.PubMedGoogle Scholar
  7. 7.
    Lovley, D. R. (1991) Dissimilatory Fe(III) and Mn(IV) reduction, Microbiol. Rev., 55, 259–287.PubMedCentralPubMedGoogle Scholar
  8. 8.
    Lovley, D. R. (1993) Dissimilatory metalloreduction, Ann. Rev. Microbiol., 47, 263–290.Google Scholar
  9. 9.
    Nealson, K. H., and Saffarini, D. (1994) Iron and manganese in anaerobic respiration environmental significance, physiology, and regulation, Ann. Rev. Microbiol., 48, 311–343.Google Scholar
  10. 10.
    Weber, K. A., Achenbach, L. A., and Coates, J. D. (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction, Nature Rev. Microbiol., 4, 752–764.Google Scholar
  11. 11.
    Richardson, D. J., Fredrickson, J. K., and Zachara, J. M. (2012) Electron transport at the microbe-mineral interface: a synthesis of current research challenges, Biochem. Soc. Transact., 40, 1163–1166.Google Scholar
  12. 12.
    Thamdrup, B., Rossello-Mora, R., and Amann, R. (2000) Microbial manganese and sulfate reduction in Black Sea shelf sediments, Appl. Environ. Microbiol., 66, 2888–2897.PubMedCentralPubMedGoogle Scholar
  13. 13.
    Walker, J. C. (1987) Was the Archaean biosphere upside down? Nature, 329, 710–712.PubMedGoogle Scholar
  14. 14.
    Lovley, D. R., Holmes, D. E., and Nevin, K. P. (2004) Dissimilatory Fe(III) and Mn(IV) reduction, Adv. Microb. Physiol., 49, 219–286.PubMedGoogle Scholar
  15. 15.
    Lovley, D. R., Ueki, T., Zhang, T., Malvankar, N. S., Shrestha, P. M., Flanagan, K. A., Aklujkar, M., Butler, J. E., Giloteaux, L., Rotaru, A. E., Holmes, D. E., Franks, A. E., Orellana, R., Risso, C., and Nevin, K. P. (2011) Geobacter: the microbe electric’s physiology, ecology, and practical applications, Adv. Microb. Physiol., 59, 1–100.PubMedGoogle Scholar
  16. 16.
    Lovley, D. R. (2012) Electromicrobiology, Ann. Rev. Microbiol., 66, 391–409.Google Scholar
  17. 17.
    Logan, B. E. (2009) Exoelectrogenic bacteria that power microbial fuel cells, Nature Rev. Microbiol., 7, 375–381.Google Scholar
  18. 18.
    Logan, B. E., and Regan, J. M. (2006) Electricity-producing bacterial communities in microbial fuel cells, Trends Microbiol., 14, 512–518.PubMedGoogle Scholar
  19. 19.
    Logan, B. E., and Regan, J. M. (2006) Microbial fuel cells — challenges and applications, Environ. Sci. Technol., 40, 5172–5180.PubMedGoogle Scholar
  20. 20.
    Malvankar, N. S., and Lovley, D. R. (2014) Microbial nanowires for bioenergy applications, Curr. Opin. Biotechnol., 27, 88–95.PubMedGoogle Scholar
  21. 21.
    Williams, K. H., Bargar, J. R., Lloyd, J. R., and Lovley, D. R. (2013) Bioremediation of uranium-contaminated groundwater: a systems approach to subsurface biogeochemistry, Curr. Opin. Biotechnol., 24, 489–497.PubMedGoogle Scholar
  22. 22.
    Cutting, R. S., Coker, V. S., Telling, N. D., Kimber, R. L., Pearce, C. I., Ellis, B. L., Lawson, R. S., van der Laan, G., Pattrick, R. A., Vaughan, D. J., Arenholz, E., and Lloyd, J. R. (2010) Optimizing Cr(VI) and Tc(VII) remediation through nanoscale biomineral engineering, Environ. Sci. Technol., 44, 2577–2584.PubMedGoogle Scholar
  23. 23.
    Jiao, Y., Qian, F., Li, Y., Wang, G., Saltikov, C. W., and Gralnick, J. A. (2011) Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1, J. Bacteriol., 193, 3662–3665.PubMedCentralPubMedGoogle Scholar
  24. 24.
    Fredrickson, J. K., Kostandarithes, H. M., Li, S. W., Plymale, A. E., and Daly, M. J. (2000) Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1, Appl. Environ. Microbiol., 66, 2006–2011.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Slobodkin, A. I. (2005) Thermophilic microbial metal reduction, Mikrobiologiya, 74, 581–595.Google Scholar
  26. 26.
    Wrighton, K. C., Agbo, P., Warnecke, F., Weber, K. A., Brodie, E. L., DeSantis, T. Z., Hugenholtz, P., Andersen, G. L., and Coates, J. D. (2008) A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells, ISME J., 2, 1146–1156.PubMedGoogle Scholar
  27. 27.
    Iavarone, A. T., Gorur, A., Yeo, B. S., Tran, R., Melnyk, R. A., Mathies, R. A., Auer, M., Coates, J. D., and Carlson, H. K. (2012) Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria, Proc. Natl. Acad. Sci. USA, 109, 1702–1707.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Ibrahim, A. S., El-Tayeb, M. A., Elbadawi, Y. B., Al-Salamah, A. A., and Antranikian, G. (2012) Hexavalent chromate reduction by alkaliphilic Amphibacillus sp. KSUCr3 is mediated by copper-dependent membrane-associated Cr(VI) reductase, Extremophiles, 16, 659–668.PubMedGoogle Scholar
  29. 29.
    Gavrilov, S. N., Lloyd, J. R., Kostrikina, N. A., and Slobodkin, A. I. (2012) Fe(III) oxide reduction by a gram-positive thermophile: physiological mechanisms for dissimilatory reduction of poorly crystalline Fe(III) oxide by a thermophilic gram-positive bacterium Carboxydothermus ferrireducens, Geomicrobiol. J., 29, 804–819.Google Scholar
  30. 30.
    Nevin, K. P., and Lovley, D. R. (2002) Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans, Appl. Environ. Microbiol., 68, 2294–2299.PubMedCentralPubMedGoogle Scholar
  31. 31.
    Myers, J. M., and Myers, C. R. (2001) Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide, Appl. Environ. Microbiol., 67, 260–269.PubMedCentralPubMedGoogle Scholar
  32. 32.
    Beliaev, A. S., and Saffarini, D. A. (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction, J. Bacteriol., 180, 6292–6297.PubMedCentralPubMedGoogle Scholar
  33. 33.
    Yang, Y., Chen, J., Qiu, D., and Zhou, J. (2013) Roles of UndA and MtrC of Shewanella putrefaciens W3-18-1 in iron reduction, BMC Microbiol., 13, 267; doi: 10.1186/1471-2180-13-267.PubMedCentralPubMedGoogle Scholar
  34. 34.
    Smith, J. A., Lovley, D. R., and Tremblay, P. L. (2013) Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens, Appl. Environ. Microbiol., 79, 901–907.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Nissen, S., Liu, X., Chourey, K., Hettich, R. L., Wagner, D. D., Pfiffner, S. M., and Loffler, F. E. (2012) Comparative c-type cytochrome expression analysis in Shewanella oneidensis strain MR-1 and Anaeromyxobacter dehalogenans strain 2CP-C grown with soluble and insoluble oxidized metal electron acceptors, Biochem. Soc. Transact., 40, 1204–1210.Google Scholar
  36. 36.
    Fredrickson, J. K., and Zachara, J. M. (2008) Electron transfer at the microbe-mineral interface: a grand challenge in biogeochemistry, Geobiology, 6, 245–253.PubMedGoogle Scholar
  37. 37.
    Richter, K., Schicklberger, M., and Gescher, J. (2012) Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration, Appl. Environ. Microbiol., 78, 913–921.PubMedCentralPubMedGoogle Scholar
  38. 38.
    Coursolle, D., and Gralnick, J. A. (2012) Reconstruction of extracellular respiratory pathways for iron(III) reduction in Shewanella oneidensis strain MR-1, Front. Microbiol., 3, 56; doi: 10.3389/fmicb.2012.00056.PubMedCentralPubMedGoogle Scholar
  39. 39.
    Shi, L., Squier, T. C., Zachara, J. M., and Fredrickson, J. K. (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multiheme c-type cytochromes, Mol. Microbiol., 65, 12–20.PubMedCentralPubMedGoogle Scholar
  40. 40.
    Hartshorne, R. S., Reardon, C. L., Ross, D., Nuester, J., Clarke, T. A., Gates, A. J., Mills, P. C., Fredrickson, J. K., Zachara, J. M., Shi, L., Beliaev, A. S., Marshall, M. J., Tien, M., Brantley, S., Butt, J. N., and Richardson, D. J. (2009) Characterization of an electron conduit between bacteria and the extracellular environment, Proc. Natl. Acad. Sci. USA, 106, 22169–22174.PubMedCentralPubMedGoogle Scholar
  41. 41.
    Richardson, D. J., Edwards, M. J., White, G. F., Baiden, N., Hartshorne, R. S., Fredrickson, J., Shi, L., Zachara, J., Gates, A. J., Butt, J. N., and Clarke, T. A. (2012) Exploring the biochemistry at the extracellular redox frontier of bacterial mineral Fe(III) respiration, Biochem. Soc. Transact., 40, 493–500.Google Scholar
  42. 42.
    Shi, L., Rosso, K. M., Clarke, T. A., Richardson, D. J., Zachara, J. M., and Fredrickson, J. K. (2012) Molecular underpinnings of Fe(III) oxide reduction by Shewanella oneidensis MR-1, Front. Microbiol., 3, 50; doi: 10.3389/fmicb.2012.00050.PubMedCentralPubMedGoogle Scholar
  43. 43.
    Coursolle, D., and Gralnick, J. A. (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1, Mol. Microbiol., 77, 995–1008.Google Scholar
  44. 44.
    Paquete, C. M., and Louro, R. O. (2010) Molecular details of multielectron transfer: the case of multiheme cytochromes from metal respiring organisms, Dalton Transact., 39, 4259–4266.Google Scholar
  45. 45.
    Moser, C. C., Chobot, S. E., Page, C. C., and Dutton, P. L. (2008) Distance metrics for heme protein electron tunneling, Biochim. Biophys. Acta, 1777, 1032–1037.PubMedCentralPubMedGoogle Scholar
  46. 46.
    Childers, S. E., Ciufo, S., and Lovley, D. R. (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis, Nature, 416, 767–769.PubMedGoogle Scholar
  47. 47.
    Harris, H. W., El-Naggar, M. Y., Bretschger, O., Ward, M. J., Romine, M. F., Obraztsova, A. Y., and Nealson, K. H. (2010) Electrokinesis is a microbial behavior that requires extracellular electron transport, Proc. Natl. Acad. Sci. USA, 107, 326–331.PubMedCentralPubMedGoogle Scholar
  48. 48.
    Harris, H. W., El-Naggar, M. Y., and Nealson, K. H. (2012) Shewanella oneidensis MR-1 chemotaxis proteins and electron-transport chain components essential for congregation near insoluble electron acceptors, Biochem. Soc. Transact., 40, 1167–1177.Google Scholar
  49. 49.
    Lies, D. P., Hernandez, M. E., Kappler, A., Mielke, R. E., Gralnick, J. A., and Newman, D. K. (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.PubMedCentralPubMedGoogle Scholar
  50. 50.
    Newman, D. K., and Kolter, R. (2000) A role for excreted quinones in extracellular electron transfer, Nature, 405, 93–97.Google Scholar
  51. 51.
    Von Canstein, H., Ogawa, J., Shimizu, S., and Lloyd, J. R. (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer, Appl. Environ. Microbiol., 74, 615–623.Google Scholar
  52. 52.
    Marsili, E., Baron, D. B., Shikhare, I. D., Coursolle, D., Gralnick, J. A., and Bond, D. R. (2008) Shewanella secretes flavins that mediate extracellular electron transfer, Proc. Natl. Acad. Sci. USA, 105, 3968–3973.PubMedCentralPubMedGoogle Scholar
  53. 53.
    Kotloski, N. J., and Gralnick, J. A. (2013) Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis, mBio, 4, e00553–12; doi: 10.1128/mBio.00553-12.PubMedCentralPubMedGoogle Scholar
  54. 54.
    Coursolle, D., Baron, D. B., Bond, D. R., and Gralnick, J. A. (2010) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis, J. Bacteriol., 192, 467–474.PubMedCentralPubMedGoogle Scholar
  55. 55.
    Ross, D. E., Brantley, S. L., and Tien, M. (2009) Kinetic characterization of OmcA and MtrC, terminal reductases involved in respiratory electron transfer for dissimilatory iron reduction in Shewanella oneidensis MR-1, Appl. Environ. Microbiol., 75, 5218–5226.PubMedCentralPubMedGoogle Scholar
  56. 56.
    Wu, C., Cheng, Y. Y., Li, B. B., Li, W. W., Li, D. B., and Yu, H. Q. (2013) Electron acceptor dependence of electron shuttle secretion and extracellular electron transfer by Shewanella oneidensis MR-1, Bioresource Technol., 136, 711–714.Google Scholar
  57. 57.
    Malvankar, N., Vargas, M., Nevin, K. P., Franks, A. E., Leang, C., Kim, B.-C., Inoue, K., Mester, T., Covalla, S. F., Johnson, J. P., Rotello, V. M., Tuominen, M. T., and Lovley, D. R. (2011) Tunable metallic-like conductivity in nanostructured biofilms comprised of microbial nanowires, Nature Nanotechnol., 6, 573–579.Google Scholar
  58. 58.
    Lovley, D. R. (2012) Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity, Biochem. Soc. Transact., 40, 1186–1190.Google Scholar
  59. 59.
    Malvankar, N. S., and Lovley, D. R. (2012) Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics, ChemSusChem, 5, 1039–1046.PubMedGoogle Scholar
  60. 60.
    Reguera, G., McCarthy, K. D., Mehta, T., Nicoll, J. S., Tuominen, M. T., and Lovley, D. R. (2005) Extracellular electron transfer via microbial nanowires, Nature, 435, 1098–1101.PubMedGoogle Scholar
  61. 61.
    Lovley, D. R. (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more, Geobiology, 6, 225–231.PubMedGoogle Scholar
  62. 62.
    Leang, C., Qian, X., Mester, T., and Lovley, D. R. (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens, Appl. Environ. Microbiol., 76, 4080–4084.PubMedCentralPubMedGoogle Scholar
  63. 63.
    Lovley, D. R. (2011) Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination, Energy Environ. Sci., 4, 4896–4906.Google Scholar
  64. 64.
    Esteve-Nunez, A., Sosnik, J., Visconti, P., and Lovley, D. R. (2008) Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens, Environ. Microbiol., 10, 497–505.PubMedGoogle Scholar
  65. 65.
    Mitchell, A. C., Peterson, L., Reardon, C. L., Reed, S. B., Culley, D. E., Romine, M. R., and Geesey, G. G. (2012) Role of outer membrane c-type cytochromes MtrC and OmcA in Shewanella oneidensis MR-1 cell production, accumulation, and detachment during respiration on hematite, Geobiology, 10, 355–370.PubMedGoogle Scholar
  66. 66.
    Meyer, T. E., Tsapin, A. I., Vandenberghe, I., de Smet, L., Frishman, D., Nealson, K. H., Cusanovich, M. A., and van Beeumen, J. J. (2004) Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes, Omics, 8, 57–77.PubMedGoogle Scholar
  67. 67.
    Myers, C. R., and Myers, J. M. (1997) 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., 179, 1143–1152.PubMedCentralPubMedGoogle Scholar
  68. 68.
    Myers, C. R., and Myers, J. M. (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.PubMedCentralPubMedGoogle Scholar
  69. 69.
    Beliaev, A. S., Saffarini, D. A., McLaughlin, J. L., and Hunnicutt, D. (2001) MtrC, an outer membrane decaheme c cytochrome required for metal reduction in Shewanella putrefaciens MR-1, Mol. Microbiol., 39, 722–730.PubMedGoogle Scholar
  70. 70.
    Pitts, K. E., Dobbin, P. S., Reyes-Ramirez, F., Thomson, A. J., Richardson, D. J., and Seward, H. E. (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.PubMedGoogle Scholar
  71. 71.
    Marritt, S. J., McMillan, D. G. G., Shi, L., Fredrickson, J. K., Zachara, J. M., Richardson, D. J., Jeuken, L. J. C., and Butt, J. N. (2012) The roles of CymA in support of the respiratory flexibility of Shewanella oneidensis MR-1, Biochem. Soc. Transact., 40, 1217–1221.Google Scholar
  72. 72.
    Marritt, S. J., Lowe, T. G., Bye, J., McMillan, D. G. G., Shi, L., Fredrickson, J., Zachara, J., Richardson, D. J., Cheesman, M. R., Jeuken, L. J. C., and Butt, J. N. (2012) A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella, Biochem. J., 444, 465–474.PubMedGoogle Scholar
  73. 73.
    Louro, R. O., and Paquete, C. M. (2012) The quest to achieve the detailed structural and functional characterization of CymA, Biochem. Soc. Transact., 40, 1291–1294.Google Scholar
  74. 74.
    McMillan, D. G. G., Marritt, S. J., Butt, J. N., and Jeuken, L. J. C. (2012) Menaquinone-7 is specific cofactor in tetraheme quinol dehydrogenase CymA, J. Biol. Chem., 287, 14215–14225.PubMedCentralPubMedGoogle Scholar
  75. 75.
    Zargar, K., and Saltikov, C. W. (2009) Lysine-91 of the tetraheme c-type cytochrome CymA is essential for quinone interaction and arsenate respiration in Shewanella sp. strain ANA-3, Arch. Microbiol., 191, 797–806.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Rodrigues, M. L., Scott, K. A., Sansom, M. S. P., Pereira, I. A. C., and Archer, M. (2008) Quinol oxidation by c-type cytochromes: structural characterization of the menaquinol binding site of NrfHA, J. Mol. Biol., 381, 341–350.PubMedGoogle Scholar
  77. 77.
    Bewley, K. D., Ellis, K. E., Firer-Sherwood, M. A., and Elliott, S. J. (2013) Multi-heme proteins: nature’s electronic multi-purpose tool, Biochim. Biophys. Acta, 1827, 938–948.PubMedGoogle Scholar
  78. 78.
    Myers, J. M., and Myers, C. R. (2000) Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone, J. Bacteriol., 182, 67–75.PubMedCentralPubMedGoogle Scholar
  79. 79.
    Schwalb, C., Chapman, S. K., and Reid, G. A. (2003) The tetraheme cytochrome CymA is required for anaerobic respiration with dimethyl sulfoxide and nitrite in Shewanella oneidensis, Biochemistry, 42, 9491–9497.PubMedGoogle Scholar
  80. 80.
    Gao, H. C., Yang, Z. K., Barua, S., Reed, S. B., Romine, M. F., Nealson, K. H., Fredrickson, J. K., Tiedje, J. M., and Zhou, J. Z. (2009) Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA, ISME J., 3, 966–976.PubMedGoogle Scholar
  81. 81.
    Gao, H., Barua, S., Liang, Y., Wu, L., Dong, Y., Reed, S., Chen, J., Culley, D., Kennedy, D., Yang, Y., He, Z., Nealson, K. H., Fredrickson, J. K., Tiedje, J. M., Romine, M., and Zhou, J. (2010) Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration, Microb. Biotechnol., 3, 455–466.PubMedCentralPubMedGoogle Scholar
  82. 82.
    Field, S. J., Dobbin, P. S., Cheesman, M. R., Watmough, N. J., Thomson, A. J., and Richardson, D. J. (2000) Purification and magneto-optical spectroscopic characterization of cytoplasmic membrane and outer membrane multiheme c-type cytochromes from Shewanella frigidimarina NCIMB400, J. Biol. Chem., 275, 8515–8522.PubMedGoogle Scholar
  83. 83.
    Schwalb, C., Chapman, S. K., and Reid, G. A. (2002) The membrane-bound tetraheme c-type cytochrome CymA interacts directly with the soluble fumarate reductase in Shewanella, Biochem. Soc. Transact., 30, 658–662.Google Scholar
  84. 84.
    Youngblut, M., Judd, E. T., Srajer, V., Sayyed, B., Goelzer, T., Elliott, S. J., Schmidt, M., and Pacheco, A. A. (2012) Laue crystal structure of Shewanella oneidensis cytochrome c nitrite reductase from a high-yield expression system, J. Biol. Inorg. Chem., 17, 647–662.PubMedCentralPubMedGoogle Scholar
  85. 85.
    Bretschger, O., Obraztsova, A., Sturm, C. A., Chang, I. S., Gorby, Y. A., Reed, S. B., Culley, D. E., Reardon, C. L., Barua, S., Romine, M. F., Zhou, J., Beliaev, A. S., Bouhenni, R., Saffarini, D., Mansfeld, F., Kim, B. H., Fredrickson, J. K., and Nealson, K. H. (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants, Appl. Environ. Microbiol., 73, 7003–7012.PubMedCentralPubMedGoogle Scholar
  86. 86.
    Schuetz, B., Schicklberger, M., Kuermann, J., Spormann, A. M., and Gescher, J. (2009) Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1, Appl. Environ. Microbiol., 75, 7789–7796.PubMedCentralPubMedGoogle Scholar
  87. 87.
    Clarke, T. A., Cole, J. A., Richardson, D. J., and Hemmings, A. M. (2007) The crystal structure of the pentaheme c-type cytochrome NrfB and characterization of its solution-state interaction with the pentaheme nitrite reductase NrfA, Biochem. J., 406, 19–30.PubMedCentralPubMedGoogle Scholar
  88. 88.
    Mowat, C. G., and Chapman, S. K. (2005) Multi-heme cytochromes — new structures, new chemistry, Dalton Transact., 21, 3381–3389.Google Scholar
  89. 89.
    Richardson, D. J., Butt, J. N., Fredrickson, J. K., Zachara, J. M., Shi, L., Edwards, M. J., White, G., Baiden, N., Gates, A. J., Marritt, S. J., and Clarke, T. A. (2012) The “porin-cytochrome” model for microbe-to-mineral electron transfer, Mol. Microbiol., 85, 201–212.PubMedGoogle Scholar
  90. 90.
    Ross, D. E., Ruebush, S. S., Brantley, S. L., Hartshorne, R. S., Clarke, T. A., Richardson, D. J., and Tien, M. (2007) Characterization of protein-protein interactions involved in iron reduction by Shewanella oneidensis MR-1, Appl. Environ. Microbiol., 73, 5797–5808.PubMedCentralPubMedGoogle Scholar
  91. 91.
    Schicklberger, M., Bucking, C., Schuetz, B., Heide, H., and Gescher, J. (2011) Involvement of the Shewanella oneidensis decaheme cytochrome MtrA in the periplasmic stability of the barrel protein MtrB, Appl. Environ. Microbiol., 77, 1520–1523.PubMedCentralPubMedGoogle Scholar
  92. 92.
    Firer-Sherwood, M. A., Ando, N., Drennan, C. L., and Elliott, S. J. (2011) Solution-based structural analysis of the decaheme cytochrome, MtrA, by small-angle X-ray scattering and analytical ultracentrifugation, J. Phys. Chem. B, 115, 1208–1214.Google Scholar
  93. 93.
    White, G. F., Shi, Z., Shi, L., Wang, Z., Dohnalkova, A. C., Marshall, M. J., Fredrickson, J. K., Zachara, J. M., Butt, J. N., Richardson, D. J., and Clarke, T. A. (2013) Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals, Proc. Natl. Acad. Sci. USA, 110, 6346–6351.PubMedCentralPubMedGoogle Scholar
  94. 94.
    Gralnick, J. A. (2012) On conducting electron traffic across the periplasm, Biochem. Soc. Transact., 40, 1178–1180.Google Scholar
  95. 95.
    Taylor, P., Pealing, S. L., Reid, G. A., Chapman, S. K., and Walkinshaw, M. D. (1999) Structural and mechanistic mapping of a unique fumarate reductase, Nature Struct. Biol., 6, 1108–1112.PubMedGoogle Scholar
  96. 96.
    Leys, D., Tsapin, A. S., Nealson, K. H., Meyer, T. E., Cusanovich, M. A., and Van Beeumen, J. J. (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1, Nature Struct. Biol., 6, 1113–1117.PubMedGoogle Scholar
  97. 97.
    Pessanha, M., Rothery, E. L., Miles, C. S., Reid, G. A., Chapman, S. K., Louro, R. O., Turner, D. L., Salgueiro, C. A., and Xavier, A. V. (2009) Tuning of functional heme reduction potentials in Shewanella fumarate reductases, Biochim. Biophys. Acta, 1787, 113–120.PubMedGoogle Scholar
  98. 98.
    Leys, D., Meyer, T. E., Tsapin, A. I., Nealson, K. H., Cusanovich, M. A., and Van Beeumen, J. J. (2002) Crystal structures at atomic resolution reveal the novel concept of “electron-harvesting” as a role for the small tetraheme cytochrome c, J. Biol. Chem., 277, 35703–35711.PubMedGoogle Scholar
  99. 99.
    Fonseca, B. M., Paquete, C. M., Neto, S. E., Pacheco, I., Soares, C. M., and Louro, R. O. (2013) Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1, Biochem. J., 449, 101–108.PubMedGoogle Scholar
  100. 100.
    Firer-Sherwood, M., Pulcu, G. S., and Elliott, S. J. (2008) Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window, J. Biol. Inorg. Chem., 13, 849–854.PubMedGoogle Scholar
  101. 101.
    Schutz, B., Seidel, J., Sturm, G., Einsle, O., and Gescher, J. (2011) Investigation of the electron transport chain to and the catalytic activity of the diheme cytochrome c peroxidase CcpA of Shewanella oneidensis, Appl. Environ. Microbiol., 77, 6172–6180.PubMedCentralPubMedGoogle Scholar
  102. 102.
    Shi, L., Chen, B., Wang, Z., Elias, D. A., Mayer, M. U., Gorby, Y. A., Ni, S., Lower, B. H., Kennedy, D. W., Wunschel, D. S., et al. (2006) Isolation of a 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.PubMedCentralPubMedGoogle Scholar
  103. 103.
    Bucking, C., Popp, F., Kerzenmacher, S., and Gescher, J. (2010) Involvement and specificity of Shewanella oneidensis outer membrane cytochromes in the reduction of soluble and solid-phase terminal electron acceptors, FEMS Microbiol. Lett., 306, 144–151.PubMedGoogle Scholar
  104. 104.
    Myers, J. M., and Myers, C. R. (2001) Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide, Appl. Environ. Microbiol., 67, 260–269.PubMedCentralPubMedGoogle Scholar
  105. 105.
    Clarke, T. A., Edwards, M. J., Gates, A. J., Hall, A., White, G. F., Bradley, J., Reardon, C. L., Shi, L., Beliaev, A. S., Marshall, M. J., Wang, Z., Watmough, N. J., Fredrickson, J. K., Zachara, J. M., Butt, J. N., and Richardson, D. J. (2011) Structure of a bacterial cell surface decaheme electron conduit, Proc. Natl. Acad. Sci. USA, 108, 9384–9389.PubMedCentralPubMedGoogle Scholar
  106. 106.
    Hartshorne, R. S., Jepson, B. N., Clarke, T. A., Field, S. J., Fredrickson, J., Zachara, J., Shi, L., Butt, J. N., and Richardson, D. J. (2007) Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors, J. Biol. Inorg. Chem., 12, 1083–1094.PubMedGoogle Scholar
  107. 107.
    Lower, B. H., Shi, L., Yongsunthon, R., Droubay, T. C., McCready, D. E., and Lower, S. K. (2007) Specific bonds between an iron oxide surface and outer membrane cytochromes MtrC and OmcA from Shewanella oneidensis MR-1, J. Bacteriol., 189, 4944–4952.PubMedCentralPubMedGoogle Scholar
  108. 108.
    Eggleston, C. M., Voros, J., Shi, L., Lower, B. H., Droubay, T. C., and Colberg, P. J. S. (2008) Binding and direct electrochemistry of OmcA, an outer membrane cytochrome from an iron reducing bacterium, with oxide electrodes: a candidate biofuel cell system, Inorg. Chim. Acta, 361, 769–777.Google Scholar
  109. 109.
    Xiong, Y., Shi, L., Chen, B., Mayer, M. U., Lower, B. H., Londer, Y., Bose, S., Hochella, M. F., Fredrickson, J. K., and Squier, T. C. (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.PubMedGoogle Scholar
  110. 110.
    Lower, B. H., Lins, R. D., Oestreicher, Z., Straatsma, T. P., Hochella, M. F., Jr., Shi, L., and Lower, S. K. (2008) In vitro evolution of a peptide with a hematite binding motif that may constitute a natural metal-oxide binding archetype, Environ. Sci. Technol., 42, 3821–3827.PubMedGoogle Scholar
  111. 111.
    Wigginton, N. S., Rosso, K. M., and Hochella, M. F. (2007) Mechanisms of electron transfer in two decaheme cytochromes from a metal-reducing bacterium, J. Phys. Chem. B, 111, 12857–12864.PubMedGoogle Scholar
  112. 112.
    Shi, L., Chen, B. W., Wang, Z. M., Elias, D. A., Mayer, M. U., Gorby, Y. A., Ni, S., Lower, B. H., Kennedy, D. W., Wunschel, D. S., et al. (2006) Isolation of a 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.PubMedCentralPubMedGoogle Scholar
  113. 113.
    Edwards, M. J., Baiden, N. A., Johs, A., Tomanicek, S. J., Liang, L., Shi, L., Fredrickson, J. K., Zachara, J. M., Gates, A. J., Butt, J. N., Richardson, D. J., and Clarke, T. A. (2014) The X-ray crystal structure of Shewanella oneidensis OmcA reveals new insight at the microbe?mineral interface, FEBS Lett., 588, 1886–1890.PubMedGoogle Scholar
  114. 114.
    Edwards, M. J., Fredrickson, J. K., Zachara, J. M., Richardson, D. J., and Clarke, T. A. (2012) Analysis of structural MtrC models based on homology with the crystal structure of MtrF, Biochem. Soc. Transact., 40, 1181–1185.Google Scholar
  115. 115.
    Moser, C. C., Chobot, S. E., Page, C. C., and Dutton, P. L. (2008) Distance metrics for heme protein electron tunneling, Biochim. Biophys. Acta, 1777, 1032–1037.PubMedCentralPubMedGoogle Scholar
  116. 116.
    Edwards, M. J., Hall, A., Shi, L., Fredrickson, J. K., Zachara, J. M., Butt, J. N., Richardson, D. J., and Clarke, T. A. (2012) The crystal structure of the extracellular 11-heme cytochrome UndA reveals a conserved 10-heme motif and defined binding site for soluble iron chelates, Structure, 20, 1275–1284.PubMedGoogle Scholar
  117. 117.
    Yang, Y., Chen, J., Qiu, D., and Zhou, J. (2013) Roles of UndA and MtrC of Shewanella putrefaciens W3-18-1 in iron reduction, BMC Microbiol., 13, 267.PubMedCentralPubMedGoogle Scholar
  118. 118.
    Breuer, M., Rosso, K. M., and Blumberger, J. (2014) Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials, Proc. Natl. Acad. Sci. USA, 111, 611–616.PubMedCentralPubMedGoogle Scholar
  119. 119.
    Breuer, M., Zarzycki, P., Blumberger, J., and Rosso, K. M. (2012) Thermodynamics of electron flow in the bacterial decaheme cytochrome MtrF, J. Am. Chem. Soc., 134, 9868–9871.PubMedGoogle Scholar
  120. 120.
    Breuer, M., Zarzycki, P., Shi, L., Clarke, T. A., Edwards, M. J., Butt, J. N., Richardson, D. J., Fredrickson, J. K., Zachara, J. M., Blumberger, J., and Rosso, K. M. (2012) Molecular structure and free energy landscape for electron transport in the decaheme cytochrome MtrF, Biochem. Soc. Transact., 40, 1198–1203.Google Scholar
  121. 121.
    Okamoto, A., Hashimoto, K., Nealson, K. H., and Nakamura, R. (2013) Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones, Proc. Natl. Acad. Sci. USA, 110, 7856–7861.PubMedCentralPubMedGoogle Scholar
  122. 122.
    Shi, L., Rosso, K. M., Zachara, J. M., and Fredrickson, J. K. (2012) Mtr extracellular electron-transfer pathways in Fe(III)-reducing or Fe(II)-oxidizing bacteria: a genomic perspective, Biochem. Soc. Transact., 40, 1261–1267.Google Scholar
  123. 123.
    Bucking, C., Piepenbrock, A., Kappler, A., and Gescher, J. (2012) Outer-membrane cytochrome-independent reduction of extracellular electron acceptors in Shewanella oneidensis, Microbiology, 158, 2144–2157.PubMedGoogle Scholar
  124. 124.
    Bewley, K. D., Firer-Sherwood, M. A., Mock, J. Y., Ando, N., Drennan, C. L., and Elliott, S. J. (2012) Mind the gap: diversity and reactivity relationships among multiheme cytochromes of the MtrA/DmsE family, Biochem. Soc. Transact., 40, 1268–1273.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Bach Institute of BiochemistryRussian Academy of SciencesMoscowRussia

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