Evidence for Quinol Oxidation Activity of ImoA, a Novel NapC/ NirT Family Protein from the Neutrophilic Fe(II)-Oxidizing Bacterium Sideroxydans lithotrophicus ES-1

Abhiney Jain, Anaísa Coelho, Joana Madjarov, Catarina M. Paquete, Jeffrey A. Gralnick

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5 Scopus citations

Abstract

Sideroxydans species are important chemolithoautotrophic Fe(II)-oxidizing bacteria in freshwater environments and play a role in biogeochemical cycling of multiple elements. Due to difficulties in laboratory cultivation and genetic intractability, the electron transport proteins required for the growth and survival of this organism remain understudied. In Sideroxydans lithotrophicus ES-1, it is proposed that the Mto pathway transfers electrons from extracellular Fe(II) oxidation across the periplasm to an inner membrane NapC/NirT family protein encoded by Slit_2495 to reduce the quinone pool. Based on sequence similarity, Slit_2495 has been putatively called CymA, a NapC/NirT family protein which in Shewanella oneidensis MR-1 oxidizes the quinol pool during anaerobic respiration of a wide range of substrates. However, our phylogenetic analysis using the alignment of different NapC/NirT family proteins shows that Slit_2495 clusters closer to NirT sequences than to CymA. We propose the name ImoA (inner membrane oxidoreductase) for Slit_2495. Our data demonstrate that ImoA can oxidize quinol pools in the inner membrane and is able to functionally replace CymA in S. oneidensis. The ability of ImoA to oxidize quinol in vivo as opposed to its proposed function of reducing quinone raises questions about the directionality and/or reversibility of electron flow through the Mto pathway in S. lithotrophicus.

Original languageEnglish (US)
JournalmBio
Volume13
Issue number5
DOIs
StatePublished - Sep 2022

Bibliographical note

Funding Information:
This work was funded by national funds through FCT–Fundação para a Ciência e a Tecnologia, I.P. (FCT), Project MOSTMICRO-ITQB with refs UIDB/04612/2020 and UIDP/ 04612/2020, and projects PTDC/BIA-BQM/4143/2021 and PD/BD/135153/2017 integrated in the PhD Program in NMR applied to chemistry, materials, and biosciences (PD/00065/2013). This project also received funding from the European Union’s Horizon 2020 Research and Innovation Program under the grant agreement number BioCat 867360.

Funding Information:
This work was also supported by the Office of Naval Research (N0014-21-1-2166) and the National Science Foundation (MCB-1815584). We declare that there are no conflicts of interest.

Publisher Copyright:
© 2022 Jain et al.

Keywords

  • Fe(II)-oxidizing bacteria
  • Mto
  • extracellular electron transfer
  • extracellular matrix electron transfer
  • iron oxidizing bacteria
  • quinol oxidoreductase

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