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The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter

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posted on 2023-03-29, 22:19 authored by Y Tan, RY Adhikari, NS Malvankar, JE Ward, KP Nevin, TL Woodard, JA Smith, OL Snoeyenbos-West, Ashley FranksAshley Franks, MT Tuominen, DR Lovley
Studies on the mechanisms for extracellular electron transfer in Geobacter species have primarily focused on Geobacter sulfurreducens, but the poor conservation of genes for some electron transfer components within the Geobacter genus suggests that there may be a diversity of extracellular electron transport strategies among Geobacter species. Examination of the gene sequences for PilA, the type IV pilus monomer, in Geobacter species revealed that the PilA sequence of Geobacter uraniireducens was much longer than that of G. sulfurreducens. This is of interest because it has been proposed that the relatively short PilA sequence of G. sulfurreducens is an important feature conferring conductivity to G. sulfurreducens pili. In order to investigate the properties of the G. uraniireducens pili in more detail, a strain of G. sulfurreducens that expressed pili comprised the PilA of G. uraniireducens was constructed. This strain, designated strain GUP, produced abundant pili, but generated low current densities and reduced Fe(III) very poorly. At pH 7, the conductivity of the G. uraniireducens pili was 3 × 10-4 S/cm, much lower than the previously reported 5 × 10-2 S/cm conductivity of G. sulfurreducens pili at the same pH. Consideration of the likely voltage difference across pili during Fe(III) oxide reduction suggested that G. sulfurreducens pili can readily accommodate maximum reported rates of respiration, but that G. uraniireducens pili are not sufficiently conductive to be an effective mediator of long-range electron transfer. In contrast to G. sulfurreducens and G. metallireducens, which require direct contact with Fe(III) oxides in order to reduce them, G. uraniireducens reduced Fe(III) oxides occluded within microporous beads, demonstrating that G. uraniireducens produces a soluble electron shuttle to facilitate Fe(III) oxide reduction. The results demonstrate that Geobacter species may differ substantially in their mechanisms for long-range electron transport and that it is important to have information beyond a phylogenetic affiliation in order to make conclusions about the mechanisms by which Geobacter species are transferring electrons to extracellular electron acceptors.

Funding

This research was supported by the Office of Naval Research (grant nos. N00014-12-1-0229 and N00014-13-1- 0550) and National Science Foundation (NSF) Nanoscale Science and Engineering Center (NSEC) Center for Hierarchical Manufacturing (CHM; grant no. CMMI-1025020). NM holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund.

History

Publication Date

2016-06-28

Journal

Frontiers in Microbiology

Volume

7

Issue

June

Article Number

980

Pagination

10p.

Publisher

Frontiers Media

ISSN

1664-302X

Rights Statement

© 2016 Tan, Adhikari, Malvankar, Ward, Nevin, Woodard, Smith, Snoeyenbos-West, Franks, Tuominen and Lovley. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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