Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
- University of California, Berkeley, United States
- The University of Chicago, United States
Abstract
Disparate redox activities that take place beyond the bounds of the prokaryotic cell cytosol must connect to membrane or cytosolic electron pools. Proteins post-translationally flavinylated by the enzyme ApbE mediate electron transfer in several characterized extracytosolic redox systems but the breadth of functions of this modification remains unknown. Here we present a comprehensive bioinformatic analysis of 31,910 prokaryotic genomes that provides evidence of extracytosolic ApbEs within ~50% of bacteria and the involvement of flavinylation in numerous uncharacterized biochemical processes. By mining flavinylation-associated gene clusters, we identify five protein classes responsible for transmembrane electron transfer and two domains of unknown function (DUF2271 and DUF3570) that are flavinylated by ApbE. We observe flavinylation/iron transporter gene colocalization patterns that implicate functions in iron reduction and assimilation. We find associations with characterized and uncharacterized respiratory oxidoreductases that highlight roles of flavinylation in respiratory electron transport chains. Finally, we identify interspecies gene cluster variability consistent with flavinylation/cytochrome functional redundancies and discover a class of 'multi-flavinylated proteins' that may resemble multiheme cytochromes in facilitating longer distance electron transfer. These findings provide key mechanistic insight into an important facet of bacterial physiology and establish flavinylation as a functionally diverse mediator of extracytosolic electron transfer.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
-
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life.https://doi.org/10.1038/nbt.4229.
Article and author information
Author details
Rafael Rivera-Lugo
Funding
National Institute of Allergy and Infectious Diseases (K22 AI144031)
- Samuel H Light
Ford Foundation
- Rafael Rivera-Lugo
Chan Zuckerberg Initiative
- Raphaël Méheust
- Jillian F Banfield
Innovative Genomics Institute
- Raphaël Méheust
- Jillian F Banfield
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Méheust et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,033
- views
-
- 295
- downloads
-
- 20
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Citations by DOI
-
- 20
- citations for umbrella DOI https://doi.org/10.7554/eLife.66878
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
eLife 10:e66878.
https://doi.org/10.7554/eLife.66878
