Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners

Edwards, Marcus J.; White, Gaye F.; Lockwood, Colin W.; Lawes, Matthew C.; Martel, Anne; Harris, Gemma; Scott, David J.; Richardson, David J.; Butt, Julea N.; Clarke, Thomas A.

Abstract

Many subsurface microorganisms couple their metabolism to the reduction or oxidation of extracellular substrates. For example, anaerobic mineral-respiring bacteria can use external metal oxides as terminal electron acceptors during respiration. Porin–cytochrome complexes facilitate the movement of electrons generated through intracellular catabolic processes across the bacterial outer membrane to these terminal electron acceptors. In the mineral-reducing model bacterium Shewanella oneidensis MR-1, this complex is composed of two decaheme cytochromes (MtrA and MtrC) and an outer-membrane β-barrel (MtrB). However, the structures and mechanisms by which porin–cytochrome complexes transfers electrons are unknown. Here, we used small-angle neutron scattering (SANS) to study the molecular structure of the transmembrane complexes MtrAB and MtrCAB. Ab initio modeling of the scattering data yielded a molecular envelope with dimensions of ~105×60×35ÅforMtrABand~170×60×45Å for MtrCAB. The shapes of these molecular envelopes suggested that MtrC interacts with the surface of MtrAB, extending ~70 Å from the membrane surface and allowing the terminal hemes to interact with both MtrAB and an extracellular acceptor. The data also reveal that MtrA fully extends through the length of MtrB, with ~30 Å being exposed into the periplasm. Proteoliposome models containing membrane associated MtrCAB and internalized small tetraheme cytochrome (STC) indicate that MtrCAB could reduce Fe(III) citrate with STC as an electron donor, disclosing a direct interaction between MtrCAB and STC. Taken together, both structural and proteoliposome experiments support porin-cytochrome–mediated electron transfer via periplasmic cytochromes such as STC.

Citation

Edwards, M. J., White, G. F., Lockwood, C. W., Lawes, M. C., Martel, A., Harris, G., Scott, D. J., Richardson, D. J., Butt, J. N., & Clarke, T. A. (2018). Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners. Journal of Biological Chemistry, 293(21), 8103-8112. https://doi.org/10.1074/jbc.RA118.001850

• Journal Article Type: Article
• Acceptance Date: Apr 10, 2018
• Online Publication Date: Apr 10, 2018
• Publication Date: May 25, 2018
• Deposit Date: Apr 16, 2018
• Publicly Available Date: Apr 16, 2018
• Journal: Journal of Biological Chemistry
• Print ISSN: 0021-9258
• Electronic ISSN: 1083-351X
• Publisher: American Society for Biochemistry and Molecular Biology
• Peer Reviewed: Peer Reviewed
• Volume: 293
• Issue: 21
• Pages: 8103-8112
• DOI: https://doi.org/10.1074/jbc.RA118.001850
• Keywords: Shewanella, cytochrome, outer membrane, electron transfer, ; small angle neutron scattering, MtrCAB
• Public URL: https://nottingham-repository.worktribe.com/output/934050
• Publisher URL: http://www.jbc.org/content/early/2018/04/10/jbc.RA118.001850
• Contract Date: Apr 16, 2018