A bundled anti-parallel cytochrome nanowire structure suggests roles in cell-cell electron transfer and biofilm formation
7 affiliations
- 1Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA
- 2Department of Plant and, Microbial Biology, BioTechnology Institute, University of Minnesota, Saint Paul, Minnesota, USA
- 3Materials Science and Engineering, University of California Irvine, Irvine, California, USA
- 4Department of Chemical and Biomolecular Engineering University of California Irvine, Irvine, California, USA
- 5Department of Chemistry, University of California Irvine, Irvine, California, USA
- 6Department of Molecular Biology and Biochemistry, University of California Irvine, Irvine, California, USA
- 7Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, Alabama, USA
Abstract
Long-range extracellular electron transfer enables respiring microbes to use minerals, organisms, or electrodes as electron acceptors by transporting electrons microns away from the cell surface. This process is primarily studied in Geobacter sulfurreducens, which produces at least three distinct, micrometer-long, multiheme cytochrome nanowires capable of electron transfer. However, the distribution and higher-order structure of such nanowires remains largely unknown. Here, we employed cryo-electron microscopy to determine the atomic structure of a unique cytochrome nanowire from Desulfuromonas soudanensis WTL, a halophilic, iron- and electrode-reducing bacterium from deep subsurface brine. These filaments are based on an OmcE tetraheme cytochrome homolog that assembles into highly ordered bundles of anti-parallel filaments. Electronic measurements of purified nanowire bundle films reveal that these bundles are conductive, with conductance increasing in a concentration-dependent manner. The apparent midpoint potential of these OmcE bundles was −145 mV vs SHE. They exhibit redox activity over a ~370 mV window attributable to five electrostatically coupled hemes, suggesting heme–heme interaction beyond the boundaries of individual OmcE repeat units. Observations of these bundles under diverse buffer conditions suggest that they represent stable supramolecular assemblies, although direct in vivo confirmation within intact biofilms remains a future goal. Furthermore, a similar cytochrome bundle structure was observed in Geobacter metallireducens, showing that this quaternary structure may be a common feature among nanowires secreted by electroactive microbes. Our findings demonstrate that cytochrome nanowires are widespread and can form specialized bundle interfaces. This novel state could facilitate conductive biofilm formation and form the basis for direct microbial electron exchange.
IMPORTANCE : All available structures of filaments containing a central core of closely spaced multiheme c-type cytochromes are derived from only a few organisms and are based on individual fibers easily imaged by cryo-electron microscopy. While imaging enriched preparations of extracellular appendages from a bacterium isolated from deep subsurface brine, we observed ordered bundles of anti-parallel cytochrome filaments. This quaternary arrangement contained specific contacts between adjacent nanowires, and a similar structure could be found in a relative from a related genus. This first report of bundling by nanowires suggests that such conductive structures may be missed in traditional surveys searching for novel filaments and provides an explanation for how nanowires could directly link adjacent cells in biofilms and granular communities.
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BibTeX
@article{petersen2026bundled,
title = {{A bundled anti-parallel cytochrome nanowire structure suggests roles in cell-cell electron transfer and biofilm formation}},
author = {Holly A. Petersen and Chi H. Chan and Gilbert O. Carpenter and Media Zakizadeh Tabari and Jessie Lynda Fields and Ayisha Zia and Shane T. Rich-New and Allon I. Hochbaum and Daniel R. Bond and Fengbin Wang},
journal = {mBio},
year = {2026},
month = aug,
doi = {10.1128/mbio.00906-26},
url = {https://doi.org/10.1128/mbio.00906-26},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - A bundled anti-parallel cytochrome nanowire structure suggests roles in cell-cell electron transfer and biofilm formation
AU - Holly A. Petersen
AU - Chi H. Chan
AU - Gilbert O. Carpenter
AU - Media Zakizadeh Tabari
AU - Jessie Lynda Fields
AU - Ayisha Zia
AU - Shane T. Rich-New
AU - Allon I. Hochbaum
AU - Daniel R. Bond
AU - Fengbin Wang
PY - 2026
DA - 2026/08/26
JO - mBio
DO - 10.1128/mbio.00906-26
UR - https://doi.org/10.1128/mbio.00906-26
AB - Long-range extracellular electron transfer enables respiring microbes to use minerals, organisms, or electrodes as electron acceptors by transporting electrons microns away from the cell surface. This process is primarily studied in Geobacter sulfurreducens, which produces at least three distinct, micrometer-long, multiheme cytochrome nanowires capable of electron transfer. However, the distribution and higher-order structure of such nanowires remains largely unknown. Here, we employed cryo-electron microscopy to determine the atomic structure of a unique cytochrome nanowire from Desulfuromonas soudanensis WTL, a halophilic, iron- and electrode-reducing bacterium from deep subsurface brine. These filaments are based on an OmcE tetraheme cytochrome homolog that assembles into highly ordered bundles of anti-parallel filaments. Electronic measurements of purified nanowire bundle films reveal that these bundles are conductive, with conductance increasing in a concentration-dependent manner. The apparent midpoint potential of these OmcE bundles was −145 mV vs SHE. They exhibit redox activity over a ~370 mV window attributable to five electrostatically coupled hemes, suggesting heme–heme interaction beyond the boundaries of individual OmcE repeat units. Observations of these bundles under diverse buffer conditions suggest that they represent stable supramolecular assemblies, although direct in vivo confirmation within intact biofilms remains a future goal. Furthermore, a similar cytochrome bundle structure was observed in Geobacter metallireducens, showing that this quaternary structure may be a common feature among nanowires secreted by electroactive microbes. Our findings demonstrate that cytochrome nanowires are widespread and can form specialized bundle interfaces. This novel state could facilitate conductive biofilm formation and form the basis for direct microbial electron exchange. IMPORTANCE : All available structures of filaments containing a central core of closely spaced multiheme c-type cytochromes are derived from only a few organisms and are based on individual fibers easily imaged by cryo-electron microscopy. While imaging enriched preparations of extracellular appendages from a bacterium isolated from deep subsurface brine, we observed ordered bundles of anti-parallel cytochrome filaments. This quaternary arrangement contained specific contacts between adjacent nanowires, and a similar structure could be found in a relative from a related genus. This first report of bundling by nanowires suggests that such conductive structures may be missed in traditional surveys searching for novel filaments and provides an explanation for how nanowires could directly link adjacent cells in biofilms and granular communities.
SN - 2150-7511
ER -