Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.

In some species of myxobacteria, adjacent cells sufficiently similar at the adhesin protein TraA can exchange components of their outer membranes. The primary benefits of such outer membrane exchange (OME) in natural populations are unclear, but in some OME interactions, transferred OM content can i...

Full description

Bibliographic Details
Main Authors: Sarah M Cossey, Yuen-Tsu Nicco Yu, Laura Cossu, Gregory J Velicer
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0224817
_version_ 1818403328112984064
author Sarah M Cossey
Yuen-Tsu Nicco Yu
Laura Cossu
Gregory J Velicer
author_facet Sarah M Cossey
Yuen-Tsu Nicco Yu
Laura Cossu
Gregory J Velicer
author_sort Sarah M Cossey
collection DOAJ
description In some species of myxobacteria, adjacent cells sufficiently similar at the adhesin protein TraA can exchange components of their outer membranes. The primary benefits of such outer membrane exchange (OME) in natural populations are unclear, but in some OME interactions, transferred OM content can include SitA toxins that kill OME participants lacking an appropriate immunity gene. Such OME-dependent toxin transfer across Myxococcus xanthus strains that differ only in their sitBAI toxin/antitoxin cassette can mediate inter-strain killing and generate colony-merger incompatibilities (CMIs)-inter-colony border phenotypes between distinct genotypes that differ from respective self-self colony interfaces. Here we ask whether OME-dependent toxin transfer is a common cause of prevalent CMIs and antagonisms between M. xanthus natural isolates identical at TraA. We disrupted traA in eleven isolates from a cm-scale soil population and assayed whether traA disruption eliminated or reduced CMIs between swarming colonies or antagonisms between strains in mixed cultures. Among 33 isolate pairs identical at traA that form clear CMIs, in no case did functional disruption of traA in one partner detectably alter CMI phenotypes. Further, traA disruption did not alleviate strong antagonisms observed during starvation-induced fruiting-body development in seven pairs of strains identical at traA. Collectively, our results suggest that most mechanisms of interference competition and inter-colony kin discrimination in natural populations of myxobacteria do not require OME. Finally, our experiments also indicate that several closely related laboratory reference strains kill some natural isolates by toxins delivered by a shared, OME-independent type VI secretion system (T6SS), suggesting that some antagonisms between sympatric natural isolates may also involve T6SS toxins.
first_indexed 2024-12-14T08:22:30Z
format Article
id doaj.art-3e5c2518bf1f453ba55302f00abf7c05
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-14T08:22:30Z
publishDate 2019-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-3e5c2518bf1f453ba55302f00abf7c052022-12-21T23:09:44ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-011411e022481710.1371/journal.pone.0224817Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.Sarah M CosseyYuen-Tsu Nicco YuLaura CossuGregory J VelicerIn some species of myxobacteria, adjacent cells sufficiently similar at the adhesin protein TraA can exchange components of their outer membranes. The primary benefits of such outer membrane exchange (OME) in natural populations are unclear, but in some OME interactions, transferred OM content can include SitA toxins that kill OME participants lacking an appropriate immunity gene. Such OME-dependent toxin transfer across Myxococcus xanthus strains that differ only in their sitBAI toxin/antitoxin cassette can mediate inter-strain killing and generate colony-merger incompatibilities (CMIs)-inter-colony border phenotypes between distinct genotypes that differ from respective self-self colony interfaces. Here we ask whether OME-dependent toxin transfer is a common cause of prevalent CMIs and antagonisms between M. xanthus natural isolates identical at TraA. We disrupted traA in eleven isolates from a cm-scale soil population and assayed whether traA disruption eliminated or reduced CMIs between swarming colonies or antagonisms between strains in mixed cultures. Among 33 isolate pairs identical at traA that form clear CMIs, in no case did functional disruption of traA in one partner detectably alter CMI phenotypes. Further, traA disruption did not alleviate strong antagonisms observed during starvation-induced fruiting-body development in seven pairs of strains identical at traA. Collectively, our results suggest that most mechanisms of interference competition and inter-colony kin discrimination in natural populations of myxobacteria do not require OME. Finally, our experiments also indicate that several closely related laboratory reference strains kill some natural isolates by toxins delivered by a shared, OME-independent type VI secretion system (T6SS), suggesting that some antagonisms between sympatric natural isolates may also involve T6SS toxins.https://doi.org/10.1371/journal.pone.0224817
spellingShingle Sarah M Cossey
Yuen-Tsu Nicco Yu
Laura Cossu
Gregory J Velicer
Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.
PLoS ONE
title Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.
title_full Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.
title_fullStr Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.
title_full_unstemmed Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.
title_short Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population.
title_sort kin discrimination and outer membrane exchange in myxococcus xanthus experimental analysis of a natural population
url https://doi.org/10.1371/journal.pone.0224817
work_keys_str_mv AT sarahmcossey kindiscriminationandoutermembraneexchangeinmyxococcusxanthusexperimentalanalysisofanaturalpopulation
AT yuentsuniccoyu kindiscriminationandoutermembraneexchangeinmyxococcusxanthusexperimentalanalysisofanaturalpopulation
AT lauracossu kindiscriminationandoutermembraneexchangeinmyxococcusxanthusexperimentalanalysisofanaturalpopulation
AT gregoryjvelicer kindiscriminationandoutermembraneexchangeinmyxococcusxanthusexperimentalanalysisofanaturalpopulation