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. ORCID:, Butt, Julea N. ORCID: and Clarke, Thomas A. ORCID: (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). pp. 8103-8112. ISSN 0021-9258

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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 transfer 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 × 35 Å for MtrAB and ∼170 × 60 × 45 Å 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.

Item Type: Article
Uncontrolled Keywords: shewanella,protein complex,electron transfer complex,liposome,membrane protein,cytochrome
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science > School of Environmental Sciences
Faculty of Science
Faculty of Medicine and Health Sciences > Norwich Medical School

Faculty of Science > School of Chemistry
Faculty of Science > School of Natural Sciences
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Depositing User: Pure Connector
Date Deposited: 19 Apr 2018 11:32
Last Modified: 12 May 2023 12:31
DOI: 10.1074/jbc.RA118.001850

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