Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria

Samuel H. Light, Raphaël Méheust, Jessica L. Ferrell, Jooyoung Cho, David Deng, Marco Agostoni, Anthony T. Iavarone, Jillian F. Banfield, Sarah E.F. D'Orazio, Daniel A. Portnoy

Research output: Contribution to journalArticlepeer-review

61 Scopus citations

Abstract

Mineral-respiring bacteria use a process called extracellular electron transfer to route their respiratory electron transport chain to insoluble electron acceptors on the exterior of the cell. We recently characterized a flavin-based extracellular electron transfer system that is present in the foodborne pathogen Listeria monocytogenes, as well as many other Gram-positive bacteria, and which highlights a more generalized role for extracellular electron transfer in microbial metabolism. Here we identify a family of putative extracellular reductases that possess a conserved posttranslational flavinylation modification. Phylogenetic analyses suggest that divergent flavinylated extracellular reductase subfamilies possess distinct and often unidentified substrate specificities. We show that flavinylation of a member of the fumarate reductase subfamily allows this enzyme to receive electrons from the extracellular electron transfer system and support L. monocytogenes growth. We demonstrate that this represents a generalizablemechanism by finding that a L. monocytogenes strain engineered to express a flavinylated extracellular urocanate reductase uses urocanate by a related mechanism and to a similar effect. These studies thus identify an enzyme family that exploits a modular flavin-based electron transfer strategy to reduce distinct extracellular substrates and support a multifunctional view of the role of extracellular electron transfer activities in microbial physiology.

Original languageEnglish
Pages (from-to)26892-26899
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number52
DOIs
StatePublished - Dec 26 2019

Bibliographical note

Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.

Keywords

  • Bacterial pathogenesis
  • Cellular respiration
  • Electromicrobiology
  • Exoelectrogen
  • Fumarate/urocanate

ASJC Scopus subject areas

  • General

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