Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella
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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.
KeywordsShewanella Flavin Respiration Electron shuttle
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).
- Albert, A. (1950) The metal-binding properties of riboflavin. Biochem J 47(3):xxviiGoogle Scholar
- 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
- 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
- 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
- Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008Google Scholar
- Furia T (1972) CRC handbook of food additives. CRC Press, Boca Raton, FlGoogle Scholar
- 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
- Hernandez ME (2004) Mechanisms of indirect mineral reduction by bacteria. PhD Dissertation, California Institute of TechnologyGoogle Scholar
- Nealson K, Scott J (2006) The prokayotes. Springer Science, New YorkGoogle Scholar
- 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