Single molecule tracking of bacterial cell surface cytochromes reveals dynamics that impact long-distance electron transport

Chong, Grace W.; Pirbadian, Sahand; Zhao, Yunke; Zacharoff, Lori A.; Pinaud, Fabien; El-Naggar, Mohamed Y.

doi:10.1073/pnas.2119964119

Single molecule tracking of bacterial cell surface cytochromes reveals dynamics that impact long-distance electron transport

Journal Article · Tue May 03 00:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2119964119· OSTI ID:1979167

^[1]; ^[2]; ^[2]; ^[2]; ^[2]; El-Naggar, Mohamed Y. ^[2]

University of Southern California, Los Angeles, CA (United States); California Institute of Technology (CalTech), Pasadena, CA (United States)
University of Southern California, Los Angeles, CA (United States)

Using a series of multiheme cytochromes, the metal-reducing bacterium Shewanella oneidensis MR-1 can perform extracellular electron transfer (EET) to respire redox-active surfaces, including minerals and electrodes outside the cell. While the role of multiheme cytochromes in transporting electrons across the cell wall is well established, these cytochromes were also recently found to facilitate long-distance (micrometer-scale) redox conduction along outer membranes and across multiple cells bridging electrodes. Recent studies proposed that long-distance conduction arises from the interplay of electron hopping and cytochrome diffusion, which allows collisions and electron exchange between cytochromes along membranes. However, the diffusive dynamics of the multiheme cytochromes have never been observed or quantified in vivo, making it difficult to assess their hypothesized contribution to the collision-exchange mechanism. Here, we use quantum dot labeling, total internal reflection fluorescence microscopy, and single-particle tracking to quantify the lateral diffusive dynamics of the outer membrane-associated decaheme cytochromes MtrC and OmcA, two key components of EET in S. oneidensis. We observe confined diffusion behavior for both quantum dot-labeled MtrC and OmcA along cell surfaces (diffusion coefficients D_MtrC = 0.0192 ± 0.0018 µm²/s, D_OmcA = 0.0125 ± 0.0024 µm²/s) and the membrane extensions thought to function as bacterial nanowires. We find that these dynamics can trace a path for electron transport via overlap of cytochrome trajectories, consistent with the long-distance conduction mechanism. The measured dynamics inform kinetic Monte Carlo simulations that combine direct electron hopping and redox molecule diffusion, revealing significant electron transport rates along cells and membrane nanowires.

View Accepted Manuscript (DOE)

Research Organization:: University of Southern California, Los Angeles, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); National Science Foundation (NSF); National Institutes of Health (NIH); Air Force Office of Scientific Research (AFOSR); Office of Naval Research (ONR)

Grant/Contract Number:: SC0010609; SC0010609

OSTI ID:: 1979167

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 19 Vol. 119; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
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Single molecule tracking of bacterial cell surface cytochromes reveals dynamics that impact long-distance electron transport

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