Structure of Geobacter OmcZ filaments suggests extracellular cytochrome polymers evolved independently multiple times

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Abstract

While early genetic and low-resolution structural observations suggested that extracellular conductive filaments on metal reducing organisms such as Geobacter were composed of Type IV pili, it has now been established that bacterial c-type cytochromes can polymerize to form extracellular filaments capable of long-range electron transport. Atomic structures exist for two such cytochrome filaments, formed from the hexaheme cytochrome OmcS and the tetraheme cytochrome OmcE. Due to the highly conserved heme packing within the central OmcS and OmcE cores, and shared pattern of heme coordination between subunits, it has been suggested that these polymers have a common origin. We have now used cryo-EM to determine the structure of a third extracellular filament, formed from the Geobacter sulfurreducens octaheme cytochrome, OmcZ. In contrast to the linear heme chains in OmcS and OmcE from the same organism, the packing of hemes, heme:heme angles, and between-subunit heme coordination is quite different in OmcZ. A branched heme arrangement within OmcZ leads to a highly surface exposed heme in every subunit, which may account for the formation of conductive biofilm networks, and explain the higher measured conductivity of OmcZ filaments. This new structural evidence suggests that conductive cytochrome polymers arose independently on more than one occasion from different ancestral multiheme proteins.

Data availability

PDB (model)deposited with accession code 8D9MEMDB (map)deposited with accession code EMD-27266

The following data sets were generated

1. Wang F
2. Chan CH
3. Mustafa K
4. Hochbaum AI
5. Bond DR
6. Egelman EH
(2022) Cryo-EM of the OmcZ nanowires from Geobacter sulfurreducens
PDB, 8D9M.

https://www.rcsb.org/structure/unreleased/8D9M

Article and author information

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Fengbin Wang

Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States

Competing interests
No competing interests declared.
Chi Ho Chan

Department of Plant and MIcrobial Biology, University of Minnesota, St. Paul, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-6596-3436
Victor Suciu

Division of Computing and Software Systems, University of Washington Bothell, Bothell, United States

Competing interests
No competing interests declared.
Khawla Mustafa

Department of Chemistry, University of California, Irvine, Irvine, United States

Competing interests
No competing interests declared.
Madeline Ammend

Department of Plant and Microbial Biology, University of Minnesota, Saint Paul, United States

Competing interests
No competing interests declared.
Dong Si

Division of Computing and Software Systems, University of Washington Bothell, Bothell, United States

Competing interests
No competing interests declared.
Allon I Hochbaum

Department of Chemistry, University of California, Irvine, Irvine, United States

For correspondence
hochbaum@uci.edu

Competing interests
No competing interests declared.
Edward H Egelman

Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States

For correspondence
egelman@virginia.edu

Competing interests
Edward H Egelman, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0003-4844-5212
Daniel R Bond

Department of Plant and Microbial Biology, University of Minnesota, Saint Paul, United States

For correspondence
dbond@umn.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-8083-7107

Funding

National Institutes of Health (GM122510)

Edward H Egelman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.