Mind the gap: Cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1

Biochemical Journal

Volumn 449, Issue 1, 2013, Pages 101-108

  Fonseca, Bruno M ^a   Paquete, Catarina M ^a   Neto, Sónia E ^a   Pacheco, Isabel ^a   Soares, Cláudio M ^a   Louro, Ricardo O ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Binding site; Chemical shift; Dissociation constant; Electrostatics; Periplasmic cytochrome; Shewanella oneidensis MR 1

Indexed keywords

CYTOCHROME C; FLAVOCYTOCHROME C; SMALL TETRAHAEM CYTOCHROME C; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CYTOPLASM; DISSOCIATION CONSTANT; ELECTRON TRANSPORT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SHEWANELLA ONEIDENSIS; STATIC ELECTRICITY;

BIOLOGICAL TRANSPORT, ACTIVE; CYTOCHROME C GROUP; CYTOCHROMES C; ELECTRON TRANSPORT; EXTRACELLULAR SPACE; OXIDATION-REDUCTION; OXIDOREDUCTASES; PERIPLASM; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STABILITY; PROTONS; SHEWANELLA; SIGNAL TRANSDUCTION; SURFACE PROPERTIES;

SHEWANELLA ONEIDENSIS MR-1;

EID: 84870912011     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121467     Document Type: Article

References (50)

1. Lovley, D. R. (2006) Bug juice: harvesting electricity with microorganisms. Nat. Rev. Microbiol. 4, 497-508
2. Summers, Z. M., Fogarty, H. E., Leang, C., Franks, A. E., Malvankar, N. S. and Lovley, D. R. (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413-1415
3. Logan, B. E. and Rabaey, K. (2012) Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical technologies. Science 337, 686-690
4. Biffinger, J. C., Fitzgerald, L. A., Ray, R., Little, B. J., Lizewski, S. E., Petersen, E. R., Ringeisen, B. R., Sanders, W. C., Sheehan, P. E., Pietron, J. J. et al. (2011) The utility of Shewanella japonica for microbial fuel cells. Bioresour. Technol. 102, 290-297
5. 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)
6. Hau, H. H. and Gralnick, J. A. (2007) Ecology and biotechnology of the genus Shewanella . Annu. Rev. Microbiol. 61, 237-258 (Pubitemid 350058208)
7. Richter, K., Schicklberger, M. and Gescher, J. (2012) Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl. Environ. Microb. 78, 913-921
8. 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
9. Gralnick, J. A. and Newman, D. K. (2007) Extracellular respiration. Mol. Microbiol. 65, 1-11 (Pubitemid 46934492)
10. 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)
11. 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
12. 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
13. 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
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. 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. et al. (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl. Environ. Microb. 73, 7003-7012 (Pubitemid 350076822)
16. Coursolle, D. and Gralnick, J. A. (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol. Microbiol. 77, 995-1008
17. 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
18. 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. Microb. 77, 1254-1262
19. Tsapin, A. I., Vandenberghe, I., Nealson, K. H., Scott, J. H., Meyer, T. E., Cusanovich, M. A., Harada, E., Kaizu, T., Akutsu, H., Leys, D. and Van Beeumen, J. J. (2001) Identification of a small tetraheme cytochrome c and a flavocytochrome c as two of the principal soluble cytochromes c in Shewanella oneidensis strain MR1. Appl. Environ. Microb. 67, 3236-3244 (Pubitemid 33644797)
20. 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 (Pubitemid 38481155)
21. Rosenbaum, M. A., Bar, H. Y., Beg, Q. K., Segre, D., Booth, J., Cotta, M. A. and Angenent, L. T. (2012) Transcriptional analysis of Shewanella oneidensis MR-1 with an electrode compared to Fe(III)-citrate or oxygen as terminal electron acceptor. Plos ONE 7, 1-13
22. Gao, H., Barua, S., Liang, Y., Wu, L., Dong, Y., Reed, S., Chen, J., Culley, D., Kennedy, D., Yang, Y. et al. (2010) Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration. Microb. Biotechnol. 3, 455-466
23. 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
24. 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. Microb. 73, 5797-5808 (Pubitemid 47462991)
25. 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. Microb. 77, 6172-6180
26. Gordon, E. H., Pealing, S. L., Chapman, S. K., Ward, F. B. and Reid, G. A. (1998) Physiological function and regulation of flavocytochrome c3, the soluble fumarate reductase from Shewanella putrefaciens NCIMB 400. Microbiology 144, 937-945 (Pubitemid 28187919)
27. 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. Microb. 75, 7789-7796
28. 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
29. Prudencio, M. and Ubbink, M. (2004) Transient complexes of redox proteins: structural and dynamic details from NMR studies. J. Mol. Recognit. 17, 524-539 (Pubitemid 39484220)
30. Diaz-Moreno, I., Diaz-Quintana, A., Ubbink, M. and De la Rosa, M. A. (2005) An NMR-based docking model for the physiological transient complex between cytochrome f and cytochrome c6. FEBS Lett. 579, 2891-2896 (Pubitemid 40731503)
31. Marritt, S. J., Lowe, T. G., Bye, J., McMillan, D. G., Shi, L., Fredrickson, J., Zachara, J., Richardson, D. J., Cheesman, M. R., Jeuken, L. J. 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
32. Fonseca, B. M., Saraiva, I. H., Paquete, C. M., Soares, C. M., Pacheco, I., Salgueiro, C. A. and Louro, R. O. (2009) The tetraheme cytochrome from Shewanella oneidensis MR-1 shows thermodynamic bias for functional specificity of the hemes. J. Biol. Inorg. Chem. 14, 375-385
33. 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
34. Bartalesi, I., Bertini, I., Hajieva, P., Rosato, A. and Vasos, P. R. (2002) Solution structure of a monoheme ferrocytochrome c from Shewanella putrefaciens and structural analysis of sequence-similar proteins: functional implications. Biochemistry 41, 5112-5119 (Pubitemid 34411665)
35. Worrall, J. A., Reinle, W., Bernhardt, R. and Ubbink, M. (2003) Transient protein interactions studied by NMR spectroscopy: the case of cytochrome c and adrenodoxin. Biochemistry 42, 7068-7076 (Pubitemid 36706490)
36. Scott, W. R. P., Hünenberger, P. H., Tironi, I. G., Mark, A. E., Billeter, S. R., Fennen, J., Torda, A. E., Huber, T., Krüger, P. and van Gunsteren, W. F. (1999) The GROMOS biomolecular simulation program package. J. Phys. Chem. A. 103, 3596-3607 (Pubitemid 129570863)
37. Bashford, D. and Karplus, M. (1990) pKa's of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry 29, 10219-10225 (Pubitemid 20384527)
38. Reference deleted
39. Gray, H. B. and Winkler, J. R. (2010) Electron flow through metalloproteins. Biochim. Biophys. Acta 1797, 1563-1572
40. 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
41. Bashir, Q., Scanu, S. and Ubbink, M. (2011) Dynamics in electron transfer protein complexes. FEBS J. 278, 1391-1400
42. Perkins, J. R., Diboun, I., Dessailly, B. H., Lees, J. G. and Orengo, C. (2010) Transient protein-protein interactions: structural, functional, and network properties. Structure 18, 1233-1243
43. Meschi, F., Wiertz, F., Klauss, L., Blok, A., Ludwig, B., Merli, A., Heering, H. A., Rossi, G. L. and Ubbink, M. (2011) Efficient electron transfer in a protein network lacking specific interactions. J. Am. Chem. Soc. 133, 16861-16867
44. 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
45. Gordon, E. H. J., Pike, A. D., Hill, A. E., Cuthbertson, P. M., Chapman, S. K. and Reid, G. A. (2000) Identification and characterization of a novel cytochrome c3 from Shewanella frigidimarina that is involved in Fe(III) respiration. Biochem. J. 349, 153-158 (Pubitemid 30440177)
46. Romine, M. F., Carlson, T. S., Norbeck, A. D., McCue, L. A. and Lipton, M. S. (2008) Identification of mobile elements and pseudogenes in the Shewanella oneidensis MR-1 genome. Appl. Environ. Microb. 74, 3257-3265 (Pubitemid 351747032)
47. 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
48. Paquete, C. M., Saraiva, I. H., Calcada, E. and Louro, R. O. (2010) Molecular basis for directional electron transfer. J. Biol. Chem. 285, 10370-10375
49. Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (Pubitemid 43205406)
50. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L. and Schwede, T. (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37, D387-D392