Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.

Bdellovibrio bacteriovorus invade Gram-negative bacteria in a predatory process requiring Type IV pili (T4P) at a single invasive pole, and also glide on surfaces to locate prey. Ras-like G-protein MglA, working with MglB and RomR in the deltaproteobacterium Myxococcus xanthus, regulates adventurous...

Full description

Bibliographic Details
Main Authors: David S Milner, Rob Till, Ian Cadby, Andrew L Lovering, Sarah M Basford, Emma B Saxon, Susan Liddell, Laura E Williams, R Elizabeth Sockett
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-04-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3983030?pdf=render
_version_ 1818544343334518784
author David S Milner
Rob Till
Ian Cadby
Andrew L Lovering
Sarah M Basford
Emma B Saxon
Susan Liddell
Laura E Williams
R Elizabeth Sockett
author_facet David S Milner
Rob Till
Ian Cadby
Andrew L Lovering
Sarah M Basford
Emma B Saxon
Susan Liddell
Laura E Williams
R Elizabeth Sockett
author_sort David S Milner
collection DOAJ
description Bdellovibrio bacteriovorus invade Gram-negative bacteria in a predatory process requiring Type IV pili (T4P) at a single invasive pole, and also glide on surfaces to locate prey. Ras-like G-protein MglA, working with MglB and RomR in the deltaproteobacterium Myxococcus xanthus, regulates adventurous gliding and T4P-mediated social motility at both M. xanthus cell poles. Our bioinformatic analyses suggested that the GTPase activating protein (GAP)-encoding gene mglB was lost in Bdellovibrio, but critical residues for MglA(Bd) GTP-binding are conserved. Deletion of mglA(Bd) abolished prey-invasion, but not gliding, and reduced T4P formation. MglA(Bd) interacted with a previously uncharacterised tetratricopeptide repeat (TPR) domain protein Bd2492, which we show localises at the single invasive pole and is required for predation. Bd2492 and RomR also interacted with cyclic-di-GMP-binding receptor CdgA, required for rapid prey-invasion. Bd2492, RomR(Bd) and CdgA localize to the invasive pole and may facilitate MglA-docking. Bd2492 was encoded from an operon encoding a TamAB-like secretion system. The TamA protein and RomR were found, by gene deletion tests, to be essential for viability in both predatory and non-predatory modes. Control proteins, which regulate bipolar T4P-mediated social motility in swarming groups of deltaproteobacteria, have adapted in evolution to regulate the anti-social process of unipolar prey-invasion in the "lone-hunter" Bdellovibrio. Thus GTP-binding proteins and cyclic-di-GMP inputs combine at a regulatory hub, turning on prey-invasion and allowing invasion and killing of bacterial pathogens and consequent predatory growth of Bdellovibrio.
first_indexed 2024-12-11T22:47:15Z
format Article
id doaj.art-32fb7509aa5e4aebba2482835e725a20
institution Directory Open Access Journal
issn 1553-7390
1553-7404
language English
last_indexed 2024-12-11T22:47:15Z
publishDate 2014-04-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Genetics
spelling doaj.art-32fb7509aa5e4aebba2482835e725a202022-12-22T00:47:34ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-04-01104e100425310.1371/journal.pgen.1004253Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.David S MilnerRob TillIan CadbyAndrew L LoveringSarah M BasfordEmma B SaxonSusan LiddellLaura E WilliamsR Elizabeth SockettBdellovibrio bacteriovorus invade Gram-negative bacteria in a predatory process requiring Type IV pili (T4P) at a single invasive pole, and also glide on surfaces to locate prey. Ras-like G-protein MglA, working with MglB and RomR in the deltaproteobacterium Myxococcus xanthus, regulates adventurous gliding and T4P-mediated social motility at both M. xanthus cell poles. Our bioinformatic analyses suggested that the GTPase activating protein (GAP)-encoding gene mglB was lost in Bdellovibrio, but critical residues for MglA(Bd) GTP-binding are conserved. Deletion of mglA(Bd) abolished prey-invasion, but not gliding, and reduced T4P formation. MglA(Bd) interacted with a previously uncharacterised tetratricopeptide repeat (TPR) domain protein Bd2492, which we show localises at the single invasive pole and is required for predation. Bd2492 and RomR also interacted with cyclic-di-GMP-binding receptor CdgA, required for rapid prey-invasion. Bd2492, RomR(Bd) and CdgA localize to the invasive pole and may facilitate MglA-docking. Bd2492 was encoded from an operon encoding a TamAB-like secretion system. The TamA protein and RomR were found, by gene deletion tests, to be essential for viability in both predatory and non-predatory modes. Control proteins, which regulate bipolar T4P-mediated social motility in swarming groups of deltaproteobacteria, have adapted in evolution to regulate the anti-social process of unipolar prey-invasion in the "lone-hunter" Bdellovibrio. Thus GTP-binding proteins and cyclic-di-GMP inputs combine at a regulatory hub, turning on prey-invasion and allowing invasion and killing of bacterial pathogens and consequent predatory growth of Bdellovibrio.http://europepmc.org/articles/PMC3983030?pdf=render
spellingShingle David S Milner
Rob Till
Ian Cadby
Andrew L Lovering
Sarah M Basford
Emma B Saxon
Susan Liddell
Laura E Williams
R Elizabeth Sockett
Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.
PLoS Genetics
title Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.
title_full Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.
title_fullStr Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.
title_full_unstemmed Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.
title_short Ras GTPase-like protein MglA, a controller of bacterial social-motility in Myxobacteria, has evolved to control bacterial predation by Bdellovibrio.
title_sort ras gtpase like protein mgla a controller of bacterial social motility in myxobacteria has evolved to control bacterial predation by bdellovibrio
url http://europepmc.org/articles/PMC3983030?pdf=render
work_keys_str_mv AT davidsmilner rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT robtill rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT iancadby rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT andrewllovering rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT sarahmbasford rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT emmabsaxon rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT susanliddell rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT lauraewilliams rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio
AT relizabethsockett rasgtpaselikeproteinmglaacontrollerofbacterialsocialmotilityinmyxobacteriahasevolvedtocontrolbacterialpredationbybdellovibrio