Emergence and modular evolution of a novel motility machinery in bacteria.

Bacteria glide across solid surfaces by mechanisms that have remained largely mysterious despite decades of research. In the deltaproteobacterium Myxococcus xanthus, this locomotion allows the formation stress-resistant fruiting bodies where sporulation takes place. However, despite the large number...

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Main Authors: Jennifer Luciano, Rym Agrebi, Anne Valérie Le Gall, Morgane Wartel, Francesca Fiegna, Adrien Ducret, Céline Brochier-Armanet, Tâm Mignot
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-09-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3169522?pdf=render
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author Jennifer Luciano
Rym Agrebi
Anne Valérie Le Gall
Morgane Wartel
Francesca Fiegna
Adrien Ducret
Céline Brochier-Armanet
Tâm Mignot
author_facet Jennifer Luciano
Rym Agrebi
Anne Valérie Le Gall
Morgane Wartel
Francesca Fiegna
Adrien Ducret
Céline Brochier-Armanet
Tâm Mignot
author_sort Jennifer Luciano
collection DOAJ
description Bacteria glide across solid surfaces by mechanisms that have remained largely mysterious despite decades of research. In the deltaproteobacterium Myxococcus xanthus, this locomotion allows the formation stress-resistant fruiting bodies where sporulation takes place. However, despite the large number of genes identified as important for gliding, no specific machinery has been identified so far, hampering in-depth investigations. Based on the premise that components of the gliding machinery must have co-evolved and encode both envelope-spanning proteins and a molecular motor, we re-annotated known gliding motility genes and examined their taxonomic distribution, genomic localization, and phylogeny. We successfully delineated three functionally related genetic clusters, which we proved experimentally carry genes encoding the basal gliding machinery in M. xanthus, using genetic and localization techniques. For the first time, this study identifies structural gliding motility genes in the Myxobacteria and opens new perspectives to study the motility mechanism. Furthermore, phylogenomics provide insight into how this machinery emerged from an ancestral conserved core of genes of unknown function that evolved to gliding by the recruitment of functional modules in Myxococcales. Surprisingly, this motility machinery appears to be highly related to a sporulation system, underscoring unsuspected common mechanisms in these apparently distinct morphogenic phenomena.
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spelling doaj.art-0a5da69be5714924b2af2c620c21e8ba2022-12-22T00:04:09ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042011-09-0179e100226810.1371/journal.pgen.1002268Emergence and modular evolution of a novel motility machinery in bacteria.Jennifer LucianoRym AgrebiAnne Valérie Le GallMorgane WartelFrancesca FiegnaAdrien DucretCéline Brochier-ArmanetTâm MignotBacteria glide across solid surfaces by mechanisms that have remained largely mysterious despite decades of research. In the deltaproteobacterium Myxococcus xanthus, this locomotion allows the formation stress-resistant fruiting bodies where sporulation takes place. However, despite the large number of genes identified as important for gliding, no specific machinery has been identified so far, hampering in-depth investigations. Based on the premise that components of the gliding machinery must have co-evolved and encode both envelope-spanning proteins and a molecular motor, we re-annotated known gliding motility genes and examined their taxonomic distribution, genomic localization, and phylogeny. We successfully delineated three functionally related genetic clusters, which we proved experimentally carry genes encoding the basal gliding machinery in M. xanthus, using genetic and localization techniques. For the first time, this study identifies structural gliding motility genes in the Myxobacteria and opens new perspectives to study the motility mechanism. Furthermore, phylogenomics provide insight into how this machinery emerged from an ancestral conserved core of genes of unknown function that evolved to gliding by the recruitment of functional modules in Myxococcales. Surprisingly, this motility machinery appears to be highly related to a sporulation system, underscoring unsuspected common mechanisms in these apparently distinct morphogenic phenomena.http://europepmc.org/articles/PMC3169522?pdf=render
spellingShingle Jennifer Luciano
Rym Agrebi
Anne Valérie Le Gall
Morgane Wartel
Francesca Fiegna
Adrien Ducret
Céline Brochier-Armanet
Tâm Mignot
Emergence and modular evolution of a novel motility machinery in bacteria.
PLoS Genetics
title Emergence and modular evolution of a novel motility machinery in bacteria.
title_full Emergence and modular evolution of a novel motility machinery in bacteria.
title_fullStr Emergence and modular evolution of a novel motility machinery in bacteria.
title_full_unstemmed Emergence and modular evolution of a novel motility machinery in bacteria.
title_short Emergence and modular evolution of a novel motility machinery in bacteria.
title_sort emergence and modular evolution of a novel motility machinery in bacteria
url http://europepmc.org/articles/PMC3169522?pdf=render
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