Mind the gap: Diversity and reactivity relationships among multihaem cytochromes of the MtrA/DmsE family

Biochemical Society Transactions

Volumn 40, Issue 6, 2012, Pages 1267-1273

  Bewley, Kathryn D ^a   Firer Sherwood, Mackenzie A ^a   Mock, Jee Young ^a   Ando, Nozomi ^b   Drennan, Catherine L ^b   Elliott, Sean J ^a  

^a Boston University   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Anaerobic respiration; Cytochrome; Electron transfer; Haem; Shewanella oneidensis

Indexed keywords

CYTOCHROME; DECAHAEM CYTOCHROME DMSE; DECAHAEM CYTOCHROME MTRA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYTOCHROME C; CYTOCHROME C(3); DIMETHYL SULFOXIDE; DIMETHYL SULFOXIDE REDUCTASE; HEME; IRON SULFUR PROTEIN; OXIDOREDUCTASE;

AMINO ACID SEQUENCE; CONFERENCE PAPER; ELECTROCHEMISTRY; ELECTRON; ELECTRON ACCEPTOR; ELECTRON TRANSPORT; NONHUMAN; OXIDATION REDUCTION POTENTIAL; POTENTIOMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; SHEWANELLA ONEIDENSIS; CHEMICAL STRUCTURE; CHEMISTRY; CYTOPLASM; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; REVIEW; SEQUENCE HOMOLOGY; SHEWANELLA;

SHEWANELLA ONEIDENSIS; SHEWANELLA ONEIDENSIS MR-1;

BACTERIAL PROTEINS; CYTOCHROME C GROUP; DIMETHYL SULFOXIDE; ELECTRON TRANSPORT; HEME; IRON-SULFUR PROTEINS; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES; PERIPLASM; SEQUENCE HOMOLOGY, AMINO ACID; SHEWANELLA;

EID: 84870209084     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120106     Document Type: Conference Paper

References (40)

1. Shi, L., Richardson, D.J., Wang, Z., Kerisit, S.N., Rosso, K.M., Zachara, J.M. and Fredrickson, J.K. (2009) The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ. Microbiol. Rep. 1, 220-227
2. Nealson, K.H. (2006) Ecophysiology of the genus Shewanella. In Prokaryotes, pp. 1133-1151, Springer, Berlin
3. 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 (Pubitemid 19301162)
4. Myers, C.R. and Nealson, K.H. (1990) Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciens MR-1. J. Bacteriol. 172, 6232-6238 (Pubitemid 20372760)
5. Myers, C.R., Carstens, B.P., Antholine, W.E. and Myers, J.M. (2000) Chromium(VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J. Appl. Microbiol. 88, 98-106 (Pubitemid 30140187)
6. Lovley, D.R. (1993) Dissimilatory metal reduction. Annu. Rev. Microbiol. 47, 263-290
7. Lovley, D.R., Phillips, E.J.P., Gorby, Y.A. and Landa, E.R. (1991) Microbial reduction of uranium. Nature 350, 413-416 (Pubitemid 21912240)
8. Gao, H., Yang, Z.K., Barua, S., Reed, S.B., Romine, M.F., Nealson, K.H., Fredrickson, J.K., Tiedje, J.M. and Zhou, J. (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
9. Gralnick, J.A., Vali, H., Lies, D.P. and Newman, D.K. (2006) Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc. Natl. Acad. Sci. U.S.A. 103, 4669-4674
10. 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 (Pubitemid 27076577)
11. 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 (Pubitemid 30004559)
12. 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 (Pubitemid 36959257)
13. Beliaev, A.S., Saffarini, D.A., McLaughlin, J.L. and Hunnicutt, D. (2001) MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol. Microbiol. 39, 722-730 (Pubitemid 32158150)
14. 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. J. Biol. Chem. 278, 27758-27765
15. Firer-Sherwood, M.A., Bewley, K.D., Mock, J.-Y. and Elliott, S.J. (2011) Tools for resolving complexity in the electron transfer networks of multiheme cytochromes c. Metallomics 3, 344-348
16. 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 (Pubitemid 47462991)
17. 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
18. 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. et al. (2009) Characterization of an electron conduit between bacteria and the extracellular environment. Proc. Natl. Acad. Sci. U.S.A. 106, 22169-22174
19. Zhang, H., Tang, X., Munske, G.R., Zakharova, N., Yang, L., Zheng, C., Wolff, M.A., Tolic, N., Anderson, G.A., Shi, L. et al. (2008) In vivo identification of the outer membrane protein OmcA-MtrC interaction network in Shewanella oneidensis MR-1 cells using novel hydrophobic chemical cross-linkers. J. Proteome Res. 7, 1712-1720
20. 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 (Pubitemid 43956069)
21. Dohnalkova, A.C., Marshall, M.J., Arey, B.W., Williams, K.H., Buck, E.C. and Fredrickson, J.K. (2011) Imaging hydrated microbial extracellular polymers: comparative analysis by electron microscopy. Appl. Environ. Microbiol. 77, 1254-1262
22. Matias, V.R., Al-Amoudi, A., Dubochet, J. and Beveridge, T.J. (2003) Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J. Bacteriol. 185, 6112-6118 (Pubitemid 37248464)
23. Hartshorne, R., Jepson, B., Clarke, T., Field, S., Fredrickson, J., Zachara, J., Shi, L., Butt, J. and Richardson, D. (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 (Pubitemid 47353552)
24. McMillan, D.G. G., Marritt, S.J., Butt, J.N. and Jeuken, L.J.C. (2012) Menaquinone-7 is a specific co-factor in the tetraheme quinol dehydrogenase CymA. J. Biol. Chem. 287, 14215-14225
25. 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, 11208-11214
26. Liu, J., Wang, Z., Belchik, S.M., Edwards, M.J., Liu, C., Kennedy, D.W., Merkley, E.D., Lipton, M.S., Butt, J.N., Richardson, D.J. et al. (2012) Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front. Microbiol. 3, 37
27. Gralnick, J.A., Brown, C.T. and Newman, D.K. (2005) Anaerobic regulation by an atypical Arc system in Shewanella oneidensis. Mol. Microbiol. 56, 1347-1357 (Pubitemid 40756015)
28. Coursolle, D. and Gralnick, J.A. (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol. Microbiol. 77, 995-1008
29. 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
30. 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
31. Firer-Sherwood, M., Pulcu, G. and Elliott, S. (2008) Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J. Biol. Inorg. Chem. 13, 849-854
32. Bilous, P.T., Cole, S.T., Anderson, W.F. and Weiner, J.H. (1988) Nucleotide sequence of the dmsABC operon encoding the anaerobic dimethylsulphoxide reductase of Escherichia coli. Mol. Microbiol. 2, 785-795
33. Cammack, R. and Weiner, J.H. (1990) Electron paramagnetic resonance spectroscopic characterization of dimethyl sulfoxide reductase of Escherichia coli. Biochemistry 29, 8410-8416 (Pubitemid 20307820)
34. Sharma, S., Cavallaro, G. and Rosato, A. (2010) A systematic investigation of multiheme c-type cytochromes in prokaryotes. J. Biol. Inorg. Chem. 15, 559-571
35. 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. et al. (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc. Natl. Acad. Sci. U.S.A. 108, 9384-9389
36. Clarke, T.A., Dennison, V., Seward, H.E., Burlat, B., Cole, J.A., Hemmings, A.M. and Richardson, D.J. (2004) Purification and spectropotentiometric characterization of Escherichia coli NrfB, a decaheme homodimer that transfers electrons to the decaheme periplasmic nitrite reductase complex. J. Biol. Chem. 279, 41333-41339 (Pubitemid 39313571)
37. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B. and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (Pubitemid 37428274)
38. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
39. Gao, H., Obraztova, A., Stewart, N., Popa, R., Fredrickson, J.K., Tiedje, J.M., Nealson, K.H. and Zhou, J. (2006) Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean. Int. J. Syst. Evol. Microbiol. 56, 1911-1916 (Pubitemid 44288420)
40. Jiao, Y. and Newman, D.K. (2007) The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765-1773 (Pubitemid 46446139)