Secreted flavin cofactors for anaerobic respiration of fumarate and urocanate by Shewanella oneidensis: Cost and role

Eric D. Kees, Augustus R. Pendleton, Catarina M. Paquete, Matthew B. Arriola, Aunica L. Kane, Nicholas J. Kotloski, Peter J. Intile, Jeffrey A. Gralnick

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Shewanella oneidensis strain MR-1, a facultative anaerobe and model organism for dissimilatory metal reduction, uses a periplasmic flavocytochrome, FccA, both as a terminal fumarate reductase and as a periplasmic electron transfer hub for extracellular respiration of a variety of substrates. It is currently unclear how maturation of FccA and other periplasmic flavoproteins is achieved, specifically in the context of flavin cofactor loading, and the fitness cost of flavin secretion has not been quantified. We demonstrate that deletion of the inner membrane flavin adenine dinucleotide (FAD) exporter Bfe results in a 23% slower growth rate than that of the wild type during fumarate respiration and an 80 to 90% loss in fumarate reductase activity. Exogenous flavin supplementation does not restore FccA activity in a Δbfe mutant unless the gene encoding the periplasmic FAD hydrolase UshA is also deleted. We demonstrate that the small Bfe-independent pool of FccA is sufficient for anaerobic growth with fumarate. Strains lacking Bfe were unable to grow using urocanate as the sole electron acceptor, which relies on the periplasmic flavoprotein UrdA. We show that periplasmic flavoprotein maturation occurs in careful balance with periplasmic FAD hydrolysis, and that the current model for periplasmic flavin cofactor loading must account for a Bfe-independent mechanism for flavin transport. Finally, we determine that the metabolic burden of flavin secretion is not significant during growth with flavin-independent anaerobic electron acceptors. Our work helps frame the physiological motivations that drove evolution of flavin secretion by Shewanella.

Original languageEnglish (US)
Article numbere00852-19
JournalApplied and environmental microbiology
Issue number16
StatePublished - Aug 15 2019

Bibliographical note

Funding Information:
This work was supported by an Office of Naval Research award (no. N00014-13-10552) to J.A.G. E.D.K. was partially supported by the University of Minnesota Informatics Institute and MnDRIVE. C.M.P. was supported by Project LISBOA-01-0145-FEDER-007660 (Microbiologia Molecular, Estrutural e Celular), funded by FEDER funds through COMPETE2020-Programa Operacional Competitividade e Internacionaliza??o (POCI). The NMR spectrometers at CERMAX are part of the National NMR Network (PTNMR) and are partially supported by Infrastructure Project no. 022161 (cofinanced by FEDER through COMPETE 2020-POCI, PORL, and FCT through PIDDAC).

Publisher Copyright:
© 2019 American Society for Microbiology.

Copyright 2019 Elsevier B.V., All rights reserved.


  • Anaerobic respiration
  • Fitness
  • Flavin
  • Shewanella

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