Divergent Nrf family proteins and MtrCAB homologs facilitate extracellular electron transfer in Aeromonas hydrophila

Bridget E. Conley, Peter J. Intile, Daniel R. Bond, Jeffrey A. Gralnick

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

Extracellular electron transfer (EET) is a strategy for respiration in which electrons generated from metabolism are moved outside the cell to a terminal electron acceptor, such as iron or manganese oxide. EET has primarily been studied in two model systems, Shewanella oneidensis and Geobacter sulfurreducens. Metal reduction has also been reported in numerous microorganisms, including Aeromonas spp., which are ubiquitous Gammaproteobacteria found in aquatic ecosystems, with some species capable of pathogenesis in humans and fish. Genomic comparisons of Aeromonas spp. revealed a potential outer membrane conduit homologous to S. oneidensis MtrCAB. While the ability to respire metals and mineral oxides is not widespread in the genus Aeromonas, 90% of the sequenced Aeromonas hydrophila isolates contain MtrCAB homologs. A. hydrophila ATCC 7966 mutants lacking mtrA are unable to reduce metals. Expression of A. hydrophila mtrCAB in an S. oneidensis mutant lacking homologous components restored metal reduction. Although the outer membrane conduits for metal reduction were similar, homologs of the S. oneidensis inner membrane and periplasmic EET components CymA, FccA, and CctA were not found in A. hydrophila. We characterized a cluster of genes predicted to encode components related to a formate-dependent nitrite reductase (NrfBCD), here named NetBCD (for Nrf-like electron transfer), and a predicted diheme periplasmic cytochrome, PdsA (periplasmic diheme shuttle). We present genetic evidence that proteins encoded by this cluster facilitate electron transfer from the cytoplasmic membrane across the periplasm to the MtrCAB conduit and function independently from an authentic NrfABCD system. A. hydrophila mutants lacking pdsA and netBCD were unable to reduce metals, while heterologous expression of these genes could restore metal reduction in an S. oneidensis mutant background. EET may therefore allow A. hydrophila and other species of Aeromonas to persist and thrive in iron- or manganese-rich oxygenlimited environments.

Original languageEnglish (US)
Article numbere02134-18
JournalApplied and environmental microbiology
Volume84
Issue number23
DOIs
StatePublished - Dec 1 2018

Bibliographical note

Funding Information:
We thank Tim Yahr (University of Iowa) for sharing the pEXG2 vector. This work was supported by a grant from the National Science Foundation (DEB-1542513) to J.A.G. and D.R.B. B.E.C. was partly supported by the Stanwood Johnston Fellowship from the University of Minnesota.

Publisher Copyright:
© 2018 American Society for Microbiology.

Keywords

  • Extracellular electron transfer
  • Metal reduction
  • Mtr
  • Nrf

Fingerprint

Dive into the research topics of 'Divergent Nrf family proteins and MtrCAB homologs facilitate extracellular electron transfer in Aeromonas hydrophila'. Together they form a unique fingerprint.

Cite this