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Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life

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 bre...

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Autores principales: Méheust, Raphaël, Huang, Shuo, Rivera-Lugo, Rafael, Banfield, Jillian F, Light, Samuel H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8238504/
https://www.ncbi.nlm.nih.gov/pubmed/34032212
http://dx.doi.org/10.7554/eLife.66878
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author Méheust, Raphaël
Huang, Shuo
Rivera-Lugo, Rafael
Banfield, Jillian F
Light, Samuel H
author_facet Méheust, Raphaël
Huang, Shuo
Rivera-Lugo, Rafael
Banfield, Jillian F
Light, Samuel H
author_sort Méheust, Raphaël
collection PubMed
description 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 multi-heme cytochromes in facilitating longer distance electron transfer. These findings provide mechanistic insight into an important facet of bacterial physiology and establish flavinylation as a functionally diverse mediator of extracytosolic electron transfer.
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spelling pubmed-82385042021-06-30 Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life Méheust, Raphaël Huang, Shuo Rivera-Lugo, Rafael Banfield, Jillian F Light, Samuel H eLife Biochemistry and Chemical Biology 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 multi-heme cytochromes in facilitating longer distance electron transfer. These findings provide mechanistic insight into an important facet of bacterial physiology and establish flavinylation as a functionally diverse mediator of extracytosolic electron transfer. eLife Sciences Publications, Ltd 2021-05-25 /pmc/articles/PMC8238504/ /pubmed/34032212 http://dx.doi.org/10.7554/eLife.66878 Text en © 2021, Méheust et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Biochemistry and Chemical Biology
Méheust, Raphaël
Huang, Shuo
Rivera-Lugo, Rafael
Banfield, Jillian F
Light, Samuel H
Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
title Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
title_full Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
title_fullStr Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
title_full_unstemmed Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
title_short Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
title_sort post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life
topic Biochemistry and Chemical Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8238504/
https://www.ncbi.nlm.nih.gov/pubmed/34032212
http://dx.doi.org/10.7554/eLife.66878
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