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The electrical conductivity of biofilms plays a critical role in advancing bioelectronics for energy and environmental appli-cations, yet the underlying mechanisms remain poorly under-stood. Previous studies proposed interheme electron transfer between hemes 5 and 10 in the outer-membrane deca-heme cytochrome (OMC) MtrC as the rate-limiting step in the bio-film electron conduction of Shewanella oneidensis MR-1. However, the strong interheme electron coupling in MtrC sug-gests that interprotein interactions may represent the primary barrier to biofilm electron conduction. Here, we investigated biofilm electron conduction mechanism with a focus on inter-protein electron transfer in S. oneidensis MR-1. Conductive currents and their temperature dependence were measured for estimating the thermal activation energy (Ea) using indium tin-doped oxide (ITO) interdigitated electrodes in wild-type and mutant biofilms. While deletion of periplasmic cytochromes had negligible impact on Ea, the deletion of OmcA or MtrC increased Ea threefold, revealing that interprotein interactions, particularly between OmcA and MtrC, dominate biofilm elec-tron transfer over clonal OMC interactions. Furthermore, sup-pressing outer-membrane fluidity dramatically increased Ea, while inter-heme exciton coupling negligibly changed in OMCs, confirming the critical role of protein diffusion and collision on the outer membrane. Flavin binding to OmcA or MtrC reduced conduction currents attributable to heme centers but enhanced those assignable to non-covalently bound fla-vins, suggesting that flavin occupancy blocks hemes 2 and 7, which serve as key interprotein electron transfer sites. These findings provide a mechanistic foundation for engineering highly conductive biofilms through targeted protein interface optimization, offering new avenues for the development of bioelectronic technologies.

Rights:

• Creative Commons BY Attribution 4.0 International
  

Keyword: biofilm, thermal activation energy, extracellular electron transport, deca-heme cytochrome, circular dichroism spectroscopy

Date published: 2025-12-24

Publisher: American Chemical Society (ACS)

Journal:

• Journal of the American Chemical Society (ISSN: 15205126) vol. 147 issue. 51 p. 46932-46940

Funding:

• Natural Science Foundation of Hunan Province 2024JJ4035
• Precursory Research for Embryonic Science and Technology JPMJPR19H1
• Japan Agency for Medical Research and Development 19gm6010002h0004
• Japan Society for the Promotion of Science 17H04969
• National Natural Science Foundation of China 42207073
• Huxiang Talent Foundation of Hunan Province 2024RC3210
• Hunan Natural Resources Research Post-Subsidy HBZ20240138

Manuscript type: Publisher's version (Version of record)

MDR DOI:

First published URL: https://doi.org/10.1021/jacs.5c10357

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Updated at: 2026-01-19 10:00:13 +0900

Published on MDR: 2026-01-19 12:21:41 +0900