Advertisement

Applied Microbiology and Biotechnology

, Volume 93, Issue 1, pp 41–48 | Cite as

Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella

  • Evan D. Brutinel
  • Jeffrey A. GralnickEmail author
Mini-Review

Abstract

The genus Shewanella contains Gram negative γ-proteobacteria capable of reducing a wide range of substrates, including insoluble metals and carbon electrodes. The utilization of insoluble respiratory substrates by bacteria requires a strategy that is quite different from a traditional respiratory strategy because the cell cannot take up the substrate. Electrons generated by cellular metabolism instead must be transported outside the cell, and perhaps beyond, in order to reduce an insoluble substrate. The primary focus of research in model organisms such as Shewanella has been the mechanisms underlying respiration of insoluble substrates. Electrons travel from the menaquinone pool in the cytoplasmic membrane to the surface of the bacterial cell through a series of proteins collectively described as the Mtr pathway. This review will focus on respiratory electron transfer from the surface of the bacterial cell to extracellular substrates. Shewanella sp. secrete redox-active flavin compounds able to transfer electrons between the cell surface and substrate in a cyclic fashion—a process termed electron shuttling. The production and secretion of flavins as well as the mechanisms of cell-mediated reduction will be discussed with emphasis on the experimental evidence for a shuttle-based mechanism. The ability to reduce extracellular substrates has sparked interest in using Shewanella sp. for applications in bioremediation, bioenergy, and synthetic biology.

Keywords

Shewanella Flavin Respiration Electron shuttle 

Notes

Acknowledgments

The authors would like to thank D. Richardson (University of East Anglia), Z. Summers (University of Minnesota), D. Newman (Caltech), L. Bird (Caltech), and one anonymous reviewer for helpful comments on this manuscript. This work was funded by the Office of Naval Research (award N000140810166 to JAG).

References

  1. Abbas CA, Sibirny AA (2011) Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev 75:321–360CrossRefGoogle Scholar
  2. Albert, A. (1950) The metal-binding properties of riboflavin. Biochem J 47(3):xxviiGoogle Scholar
  3. Baron D, LaBelle E, Coursolle D, Gralnick JA, Bond DR (2009) Electrochemical measurement of electron transfer kinetics by Shewanella oneidensis MR-1. J Biol Chem 284:28865–28873CrossRefGoogle Scholar
  4. Beliaev AS, Saffarini DA (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180:6292–6297Google Scholar
  5. Beliaev AS, Saffarini DA, McLaughlin JL, Hunnicutt D (2001) MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 39:722–730CrossRefGoogle Scholar
  6. Biffinger JC, Pietron J, Ray R, Little B, Ringeisen BR (2007) A biofilm enhanced miniature microbial fuel cell using Shewanella oneidensis DSP10 and oxygen reduction cathodes. Biosens Bioelectron 22:1672–1679CrossRefGoogle Scholar
  7. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555CrossRefGoogle Scholar
  8. Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485CrossRefGoogle Scholar
  9. Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF, Zhou J, Beliaev AS, Bouhenni R, Saffarini D, Mansfeld F, Kim BH, Fredrickson JK, Nealson KH (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012CrossRefGoogle Scholar
  10. Bücking C, Popp F, Kerzenmacher S, 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 306:144–151CrossRefGoogle Scholar
  11. Clarke TA, Edwards MJ, Gates AJ, Hall A, White GF, Bradley J, Reardon CL, Shi L, Beliaev AS, Marshall MJ, Wang Z, Watmough NJ, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci USA 108:9384–9389CrossRefGoogle Scholar
  12. Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008Google Scholar
  13. Coursolle D, Baron DB, Bond DR, Gralnick JA (2010) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 192:467–474CrossRefGoogle Scholar
  14. Covington ED, Gelbmann CB, Kotloski NJ, Gralnick JA (2010) An essential role for UshA in processing of extracellular flavin electron shuttles by Shewanella oneidensis. Mol Microbiol 78:519–532CrossRefGoogle Scholar
  15. Furia T (1972) CRC handbook of food additives. CRC Press, Boca Raton, FlGoogle Scholar
  16. Gralnick JA, Newman DK (2007) Extracellular respiration. Mol Microbiol 65:1–11CrossRefGoogle Scholar
  17. Hartshorne RS, Reardon CL, Ross D, Nuester J, Clarke TA, Gates AJ, Mills PC, Fredrickson JK, Zachara JM, Shi L, Beliaev AS, Marshall MJ, Tien M, Brantley S, Butt JN, Richardson DJ (2009) Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci USA 106:22169–22174CrossRefGoogle Scholar
  18. Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258CrossRefGoogle Scholar
  19. Hernandez ME (2004) Mechanisms of indirect mineral reduction by bacteria. PhD Dissertation, California Institute of TechnologyGoogle Scholar
  20. Hernandez ME, Newman DK (2001) Extracellular electron transfer. Cell Mol Life Sci 58:1562–1571CrossRefGoogle Scholar
  21. Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70:921–928CrossRefGoogle Scholar
  22. Hubbard TJ, Ailey B, Brenner SE, Murzin AG, Chothia C (1999) SCOP: a structural classification of proteins database. Nucleic Acids Res 27:254–256CrossRefGoogle Scholar
  23. Hunt KA, Flynn JM, Naranjo B, Shikhare ID, Gralnick JA (2010) Substrate-level phosphorylation is the primary source of energy conservation during anaerobic respiration of Shewanella oneidensis strain MR-1. J Bacteriol 192:3345–3351CrossRefGoogle Scholar
  24. Jensen HM, Albers AE, Malley KR, Londer YY, Cohen BE, Helms BA, Weigele P, Groves JT, Ajo-Franklin CM (2010) Engineering of a synthetic electron conduit in living cells. Proc Natl Acad Sci USA 107:19213–19218CrossRefGoogle Scholar
  25. Jiang X, Hu J, Fitzgerald LA, Biffinger JC, Xie P, Ringeisen BR, Lieber CM (2010) Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging. Proc Natl Acad Sci USA 107:16806–16810CrossRefGoogle Scholar
  26. Leys D, Tsapin AS, Nealson KH, Meyer TE, Cusanovich MA, Van Beeumen JJ (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1. Nat Struct Biol 6:1113–1117CrossRefGoogle Scholar
  27. Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK (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 71:4414–4426CrossRefGoogle Scholar
  28. Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19:564–571CrossRefGoogle Scholar
  29. Lovley D, Coates J, Blunt-Harris E, Phillips E, Woodward J (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448CrossRefGoogle Scholar
  30. Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286CrossRefGoogle Scholar
  31. Lower SK, Hochella MF, Beveridge TJ (2001) Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and alpha-FeOOH. Science 292:1360–1363CrossRefGoogle Scholar
  32. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA 105:3968–3973CrossRefGoogle Scholar
  33. Myers CR, Myers JM (2004) Shewanella oneidensis MR-1 restores menaquinone synthesis to a menaquinone-negative mutant. Appl Environ Microbiol 70:5415–5425CrossRefGoogle Scholar
  34. Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240:1319–1321CrossRefGoogle Scholar
  35. Nealson K, Scott J (2006) The prokayotes. Springer Science, New YorkGoogle Scholar
  36. Nevin KP, Lovley DR (2000) Lack of production of electron-shuttling compounds or solubilization of Fe(III) during reduction of insoluble Fe(III) oxide by Geobacter metallireducens. Appl Environ Microbiol 66:2248–2251CrossRefGoogle Scholar
  37. Nevin KP, Lovley DR (2002) Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl Environ Microbiol 68:2294–2299CrossRefGoogle Scholar
  38. Newman DK, Kolter R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405:94–97CrossRefGoogle Scholar
  39. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716CrossRefGoogle Scholar
  40. Ringeisen BR, Henderson E, Wu PK, Pietron J, Ray R, Little B, Biffinger JC, Jones-Meehan JM (2006) High power density from a miniature microbial fuel cell using Shewanella oneidensis DSP10. Environ Sci Technol 40:2629–2634CrossRefGoogle Scholar
  41. Ross DE, Brantley SL, 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 75:5218–5226CrossRefGoogle Scholar
  42. Ross, D. E., J. M. Flynn, D. B. Baron, J. A. Gralnick & D. R. Bond (2011) Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS One, 6, e16649.Google Scholar
  43. Shi L, Squier TC, Zachara JM, Fredrickson JK (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65:12–20CrossRefGoogle Scholar
  44. Srikanth S, Marsili E, Flickinger MC, Bond DR (2008) Electrochemical characterization of Geobacter sulfurreducens cells immobilized on graphite paper electrodes. Biotechnol Bioeng 99:1065–1073CrossRefGoogle Scholar
  45. Stams AJ, de Bok FA, Plugge CM, van Eekert MH, Dolfing J, Schraa G (2006) Exocellular electron transfer in anaerobic microbial communities. Environ Microbiol 8:371–382CrossRefGoogle Scholar
  46. Straub KL, Schink B (2004) Ferrihydrite-dependent growth of Sulfurospirillum deleyianum through electron transfer via sulfur cycling. Appl Environ Microbiol 70:5744–5749CrossRefGoogle Scholar
  47. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2002) Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res 30:3141–3151CrossRefGoogle Scholar
  48. von Canstein H, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623CrossRefGoogle Scholar
  49. Wang Y, Kern SE, Newman DK (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365–369CrossRefGoogle Scholar
  50. Winkler WC, Cohen-Chalamish S, Breaker RR (2002) An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci USA 99:15908–15913CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.BioTechnology InstituteUniversity of Minnesota-Twin CitiesSt. PaulUSA
  2. 2.Department of MicrobiologyUniversity of Minnesota-Twin CitiesSt. PaulUSA

Personalised recommendations