Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option

Walker, David J.  F.; Nevin, Kelly P.; Holmes, Dawn E.; Rotaru, Amelia-Elena; Ward, Joy E.; Woodard, Trevor L.; Zhu, Jiaxin; Ueki, Toshiyuki; Nonnenmann, Stephen S.; McInerney, Michael J.; Lovley, Derek R.

doi:10.1038/s41396-019-0575-9

Title: Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option

Journal Article · 02 January 2020 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-019-0575-9 · OSTI ID:1604770

Walker, David J. F. ^[1]; Nevin, Kelly P. ^[2]; Holmes, Dawn E. ^[3]; Rotaru, Amelia-Elena ^[4]; Ward, Joy E. ^[2]; Woodard, Trevor L. ^[2]; Zhu, Jiaxin ^[2]; Ueki, Toshiyuki ^[2]; Nonnenmann, Stephen S. ^[2];

^[5]; Lovley, Derek R. ^[2]

Univ. of Massachusetts, Amherst, MA (United States); University of Oklahoma
Univ. of Massachusetts, Amherst, MA (United States)
Univ. of Massachusetts, Amherst, MA (United States); Western New England University, Springfield, MA (United States)
Univ. of Massachusetts, Amherst, MA (United States); Univ. of Southern Denmark, Odense (Denmark)
Univ. of Oklahoma, Norman, OK (United States)

Syntrophic interspecies electron exchange is necessary for the stable functioning of diverse anaerobic microbial communities. Hydrogen/formate interspecies electron transfer (HFIT), in which H₂ and/or formate function as diffusible electron carriers, has been considered to be the primary mechanism for electron transfer because most common syntrophs were thought to lack biochemical components, such as electrically conductive pili (e-pili), necessary for direct interspecies electron transfer (DIET). Herein we report that Syntrophus aciditrophicus, one of the most intensively studied microbial models for HFIT, produces e-pili and can grow via DIET. Heterologous expression of the putative S. aciditrophicus type IV pilin gene in Geobacter sulfurreducens yielded conductive pili of the same diameter (4 nm) and conductance of the native S. aciditrophicus pili and enabled long-range electron transport in G. sulfurreducens. S. aciditrophicus lacked abundant c-type cytochromes often associated with DIET. Pilin genes likely to yield e-pili were found in other genera of hydrogen/formate-producing syntrophs. The discovery that DIET is a likely option for diverse syntrophs that are abundant in many anaerobic environments necessitates a reexamination of the paradigm that HFIT is the predominant mechanism for syntrophic electron exchange within anaerobic microbial communities of biogeochemical and practical significance.

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Research Organization:: Univ. of Oklahoma, Norman, OK (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-96ER20214

OSTI ID:: 1604770

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 3 Vol. 14; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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An Escherichia coli Chassis for Production of Electrically Conductive Protein Nanowires Ueki, Toshiyuki; Walker, David J. F.; Woodard, Trevor L. ACS Synthetic Biology, Vol. 9, Issue 3 https://doi.org/10.1021/acssynbio.9b00506	journal	March 2020
Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire Filman, David J.; Marino, Stephen F.; Ward, Joy E. Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0448-9	journal	June 2019
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The Archaellum of Methanospirillum hungatei Is Electrically Conductive Walker, David J. F.; Martz, Eric; Holmes, Dawn E. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.00579-19	journal	April 2019
Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics Ziels, Ryan M.; Nobu, Masaru K.; Sousa, Diana Z. mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00159-19	journal	August 2019
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Title: Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option

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