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...
Main Authors: | , , , , , , , , |
---|---|
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 |