Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity

Ralstonia solanacearum is a bacterial plant pathogen causing important economic losses worldwide. In addition to the polar flagella responsible for swimming motility, this pathogen produces type IV pili (TFP) that govern twitching motility, a flagellum-independent movement on solid surfaces. The imp...

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Autores: Corral, Jordi, Sebastià, Pau, Coll, Núria S., Barbé, Jordi, Aranda, Jesús, Valls, Marc
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/220035
Acesso em linha:http://hdl.handle.net/10261/220035
Access Level:acceso abierto
Palavra-chave:Ralstonia solanacearum
pilI
chpA
pilA
fliC
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spelling Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicityCorral, JordiSebastià, PauColl, Núria S.Barbé, JordiAranda, JesúsValls, MarcRalstonia solanacearumpilIchpApilAfliCRalstonia solanacearum is a bacterial plant pathogen causing important economic losses worldwide. In addition to the polar flagella responsible for swimming motility, this pathogen produces type IV pili (TFP) that govern twitching motility, a flagellum-independent movement on solid surfaces. The implication of chemotaxis in plant colonization, through the control flagellar rotation by the proteins CheW and CheA, has been previously reported in R. solanacearum. In this work, we have identified in this bacterium homologues of the Pseudomonas aeruginosa pilI and chpA genes, suggested to play roles in TFP-associated motility analogous to those played by the cheW and cheA genes, respectively. We demonstrate that R. solanacearum strains with a deletion of the pilI or the chpA coding region show normal swimming and chemotaxis but altered biofilm formation and reduced twitching motility, transformation efficiency, and root attachment. Furthermore, these mutants displayed wild-type growth in planta and impaired virulence on tomato plants after soil-drench inoculations but not when directly applied to the xylem. Comparison with deletion mutants for pilA and fliC—encoding the major pilin and flagellin subunits, respectively—showed that both twitching and swimming are required for plant colonization and full virulence. This work proves for the first time the functionality of a pilus-mediated pathway encoded by pil-chp genes in R. solanacearum, demonstrating that pilI and chpA genes are bona fide motility regulators controlling twitching motility and its three related phenotypes: virulence, natural transformation, and biofilm formation.This study was funded by grants BIO2016-77011-R and AGL2016-78002-R (Spanish Ministry of Economy and Competitiveness). We acknowledge financial support from the Severo Ochoa Program for Centers of Excellence in R&D (SEV‐2015‐0533) and the CERCA Program from the Catalan Government (Generalitat de Catalunya). J.A. is a Serra Húnter Fellow (Generalitat de Catalunya). The project that gave rise to these results received the support of a fellowship (code is LCF/BQ/IN17/11620004) from la Caixa Foundation (identifier [ID] 100010434). This project has received funding from the European Union's Horizon 2020 research and innovation program under Marie Skłodowska-Curie grant agreement no. 713673.Peer reviewedAmerican Society for MicrobiologyMinisterio de Economía y Competitividad (España)Generalitat de CatalunyaFundación la CaixaEuropean CommissionConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202020202020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/220035reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2016-77011-Rinfo:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2016-78002-Rinfo:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SEV‐2015‐0533info:eu-repo/grantAgreement/EC/H2020/713673https://doi.org/10.1128/mSphere.00740-19Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2200352026-05-22T06:33:51Z
dc.title.none.fl_str_mv Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
title Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
spellingShingle Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
Corral, Jordi
Ralstonia solanacearum
pilI
chpA
pilA
fliC
title_short Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
title_full Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
title_fullStr Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
title_full_unstemmed Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
title_sort Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity
dc.creator.none.fl_str_mv Corral, Jordi
Sebastià, Pau
Coll, Núria S.
Barbé, Jordi
Aranda, Jesús
Valls, Marc
author Corral, Jordi
author_facet Corral, Jordi
Sebastià, Pau
Coll, Núria S.
Barbé, Jordi
Aranda, Jesús
Valls, Marc
author_role author
author2 Sebastià, Pau
Coll, Núria S.
Barbé, Jordi
Aranda, Jesús
Valls, Marc
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Generalitat de Catalunya
Fundación la Caixa
European Commission
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Ralstonia solanacearum
pilI
chpA
pilA
fliC
topic Ralstonia solanacearum
pilI
chpA
pilA
fliC
description Ralstonia solanacearum is a bacterial plant pathogen causing important economic losses worldwide. In addition to the polar flagella responsible for swimming motility, this pathogen produces type IV pili (TFP) that govern twitching motility, a flagellum-independent movement on solid surfaces. The implication of chemotaxis in plant colonization, through the control flagellar rotation by the proteins CheW and CheA, has been previously reported in R. solanacearum. In this work, we have identified in this bacterium homologues of the Pseudomonas aeruginosa pilI and chpA genes, suggested to play roles in TFP-associated motility analogous to those played by the cheW and cheA genes, respectively. We demonstrate that R. solanacearum strains with a deletion of the pilI or the chpA coding region show normal swimming and chemotaxis but altered biofilm formation and reduced twitching motility, transformation efficiency, and root attachment. Furthermore, these mutants displayed wild-type growth in planta and impaired virulence on tomato plants after soil-drench inoculations but not when directly applied to the xylem. Comparison with deletion mutants for pilA and fliC—encoding the major pilin and flagellin subunits, respectively—showed that both twitching and swimming are required for plant colonization and full virulence. This work proves for the first time the functionality of a pilus-mediated pathway encoded by pil-chp genes in R. solanacearum, demonstrating that pilI and chpA genes are bona fide motility regulators controlling twitching motility and its three related phenotypes: virulence, natural transformation, and biofilm formation.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/220035
url http://hdl.handle.net/10261/220035
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2016-77011-R
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2016-78002-R
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SEV‐2015‐0533
info:eu-repo/grantAgreement/EC/H2020/713673
https://doi.org/10.1128/mSphere.00740-19
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
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repository.mail.fl_str_mv
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