Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity

ABSTRACT 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...

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Autores principales:	Jordi Corral, Pau Sebastià, Núria S. Coll, Jordi Barbé, Jesús Aranda, Marc Valls
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Ralstonia solanacearum pilI chpA pilA fliC Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/03cb128a14af45f49cee680b5613f167
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spelling	oai:doaj.org-article:03cb128a14af45f49cee680b5613f1672021-11-15T15:29:16ZTwitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity10.1128/mSphere.00740-192379-5042https://doaj.org/article/03cb128a14af45f49cee680b5613f1672020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00740-19https://doaj.org/toc/2379-5042ABSTRACT 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. IMPORTANCE Twitching and swimming are two bacterial movements governed by pili and flagella. The present work identifies for the first time in the Gram-negative plant pathogen Ralstonia solanacearum a pilus-mediated chemotaxis pathway analogous to that governing flagellum-mediated chemotaxis. We show that regulatory genes in this pathway control all of the phenotypes related to pili, including twitching motility, natural transformation, and biofilm formation, and are also directly implicated in virulence, mainly during the first steps of the plant infection. Our results show that pili have a higher impact than flagella on the interaction of R. solanacearum with tomato plants and reveal new types of cross-talk between the swimming and twitching motility phenotypes: enhanced swimming in bacteria lacking pili and a role for the flagellum in root attachment.Jordi CorralPau SebastiàNúria S. CollJordi BarbéJesús ArandaMarc VallsAmerican Society for MicrobiologyarticleRalstonia solanacearumpilIchpApilAfliCMicrobiologyQR1-502ENmSphere, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Ralstonia solanacearum pilI chpA pilA fliC Microbiology QR1-502
spellingShingle	Ralstonia solanacearum pilI chpA pilA fliC Microbiology QR1-502 Jordi Corral Pau Sebastià Núria S. Coll Jordi Barbé Jesús Aranda Marc Valls Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity
description	ABSTRACT 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. IMPORTANCE Twitching and swimming are two bacterial movements governed by pili and flagella. The present work identifies for the first time in the Gram-negative plant pathogen Ralstonia solanacearum a pilus-mediated chemotaxis pathway analogous to that governing flagellum-mediated chemotaxis. We show that regulatory genes in this pathway control all of the phenotypes related to pili, including twitching motility, natural transformation, and biofilm formation, and are also directly implicated in virulence, mainly during the first steps of the plant infection. Our results show that pili have a higher impact than flagella on the interaction of R. solanacearum with tomato plants and reveal new types of cross-talk between the swimming and twitching motility phenotypes: enhanced swimming in bacteria lacking pili and a role for the flagellum in root attachment.
format	article
author	Jordi Corral Pau Sebastià Núria S. Coll Jordi Barbé Jesús Aranda Marc Valls
author_facet	Jordi Corral Pau Sebastià Núria S. Coll Jordi Barbé Jesús Aranda Marc Valls
author_sort	Jordi Corral
title	Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity
title_short	Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity
title_full	Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity
title_fullStr	Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity
title_full_unstemmed	Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity
title_sort	twitching and swimming motility play a role in <named-content content-type="genus-species">ralstonia solanacearum</named-content> pathogenicity
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/03cb128a14af45f49cee680b5613f167
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Twitching and Swimming Motility Play a Role in <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Pathogenicity

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