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

Fengbin Wang, Chi Ho Chan, Victor Suciu, Khawla Mustafa, Madeline Ammend, Dong Si, Allon I. Hochbaum, Edward H. Egelman, Daniel R. Bond

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

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-electron microscopy (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.

Original languageEnglish (US)
Article numbere81551
JournaleLife
Volume11
DOIs
StatePublished - Sep 2022

Bibliographical note

Funding Information:
The cryo-EM imaging was done at the Molecular Electron Microscopy Core Facility at the University of Virginia, which is supported by the School of Medicine and built with NIH grant G20-RR31199. This work was supported by NIH Grant GM122510 (E.H.E.), K99GM138756 (F.W.), DOE grant DE-SC0020322 (A.I.H., D.R.B., E.H.E., and M A.), AFOSR grant FA9550-19-1-0380 (A.I.H), NSF grant 2030381 (D.S.), Office of Naval research grant N00014-18-1-2632 (C.H.C), and the SRCP Seed Grant at the University of Washington Bothell (D.S).

Publisher Copyright:
© Wang et al.

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