Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

Fengbin Wang; Yangqi Gu; J Patrick O'Brien; Sophia M Yi; Sibel Ebru Yalcin; Vishok Srikanth; Cong Shen; Dennis Vu; Nicole L Ing; Allon I Hochbaum; Edward H Egelman; Nikhil S Malvankar

doi:10.1016/j.cell.2019.03.029

Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

Cell. 2019 Apr 4;177(2):361-369.e10. doi: 10.1016/j.cell.2019.03.029.

Authors

Affiliations

¹ Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA 22908, USA.
² Microbial Sciences Institute, Yale University, New Haven, CT 06516, USA; Department of Molecular, Cellular & Developmental Biology, Yale University, New Haven, CT 06511, USA.
³ Microbial Sciences Institute, Yale University, New Haven, CT 06516, USA; Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06511, USA.
⁴ Microbial Sciences Institute, Yale University, New Haven, CT 06516, USA; Department of Microbial Pathogenesis, Yale University, New Haven, CT 06511, USA.
⁵ Department of Materials Science & Engineering, University of California, Irvine, Irvine, CA 92697, USA.
⁶ Department of Materials Science & Engineering, University of California, Irvine, Irvine, CA 92697, USA; Department of Chemistry, University of California, Irvine, Irvine, CA 92697, USA. Electronic address: hochbaum@uci.edu.
⁷ Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA 22908, USA. Electronic address: egelman@virginia.edu.
⁸ Microbial Sciences Institute, Yale University, New Haven, CT 06516, USA; Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06511, USA. Electronic address: nikhil.malvankar@yale.edu.

Abstract

Long-range (>10 μm) transport of electrons along networks of Geobacter sulfurreducens protein filaments, known as microbial nanowires, has been invoked to explain a wide range of globally important redox phenomena. These nanowires were previously thought to be type IV pili composed of PilA protein. Here, we report a 3.7 Å resolution cryoelectron microscopy structure, which surprisingly reveals that, rather than PilA, G. sulfurreducens nanowires are assembled by micrometer-long polymerization of the hexaheme cytochrome OmcS, with hemes packed within ∼3.5-6 Å of each other. The inter-subunit interfaces show unique structural elements such as inter-subunit parallel-stacked hemes and axial coordination of heme by histidines from neighboring subunits. Wild-type OmcS filaments show 100-fold greater conductivity than other filaments from a ΔomcS strain, highlighting the importance of OmcS to conductivity in these nanowires. This structure explains the remarkable capacity of soil bacteria to transport electrons to remote electron acceptors for respiration and energy sharing.

Keywords: Geobacter; atomic force microscopy; bioelectronics; biomaterials; cryoelectron microscopy; cytochromes; electron conductivity; extracellular electron transport; microbial nanowires; protein structure.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Biofilms
Electric Conductivity
Electron Transport / physiology*
Electrons
Fimbriae Proteins / chemistry
Fimbriae, Bacterial / chemistry
Geobacter / metabolism*
Heme / metabolism*
Nanowires
Oxidation-Reduction

Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

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