Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.

Axenically cultured Liberibacter crescens (Lcr) is a closely related surrogate for uncultured plant pathogenic species of the genus Liberibacter, including 'Candidatus L. asiaticus' (CLas) and 'Ca. L. solanacearum' (CLso). All Liberibacters encode a completely conserved gene repe...

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Autores principales: Lulu Cai, Mukesh Jain, Marta Sena-Vélez, Kathryn M Jones, Laura A Fleites, Michelle Heck, Dean W Gabriel
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Publicado: Public Library of Science (PLoS) 2021
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spelling oai:doaj.org-article:6535f79a11bb4d6c8b086c609f5501942021-12-02T20:19:16ZTad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.1932-620310.1371/journal.pone.0258583https://doaj.org/article/6535f79a11bb4d6c8b086c609f5501942021-01-01T00:00:00Zhttps://doi.org/10.1371/journal.pone.0258583https://doaj.org/toc/1932-6203Axenically cultured Liberibacter crescens (Lcr) is a closely related surrogate for uncultured plant pathogenic species of the genus Liberibacter, including 'Candidatus L. asiaticus' (CLas) and 'Ca. L. solanacearum' (CLso). All Liberibacters encode a completely conserved gene repertoire for both flagella and Tad (Tight Adherence) pili and all are missing genes critical for nucleotide biosynthesis. Both flagellar swimming and Tad pilus-mediated twitching motility in Lcr were demonstrated for the first time. A role for Tad pili in the uptake of extracellular dsDNA for food in Liberibacters was suspected because both twitching and DNA uptake are impossible without repetitive pilus extension and retraction, and no genes encoding other pilus assemblages or mechanisms for DNA uptake were predicted to be even partially present in any of the 35 fully sequenced Liberibacter genomes. Insertional mutations of the Lcr Tad pilus genes cpaA, cpaB, cpaE, cpaF and tadC all displayed such severely reduced growth and viability that none could be complemented. A mutation affecting cpaF (motor ATPase) was further characterized and the strain displayed concomitant loss of twitching, viability and reduced periplasmic uptake of extracellular dsDNA. Mutations of comEC, encoding the inner membrane competence channel, had no effect on either motility or growth but completely abolished natural transformation in Lcr. The comEC mutation was restored by complementation using comEC from Lcr but not from CLas strain psy62 or CLso strain RS100, indicating that unlike Lcr, these pathogens were not naturally competent for transformation. This report provides the first evidence that the Liberibacter Tad pili are dynamic and essential for both motility and DNA uptake, thus extending their role beyond surface adherence.Lulu CaiMukesh JainMarta Sena-VélezKathryn M JonesLaura A FleitesMichelle HeckDean W GabrielPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 16, Iss 10, p e0258583 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Lulu Cai
Mukesh Jain
Marta Sena-Vélez
Kathryn M Jones
Laura A Fleites
Michelle Heck
Dean W Gabriel
Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.
description Axenically cultured Liberibacter crescens (Lcr) is a closely related surrogate for uncultured plant pathogenic species of the genus Liberibacter, including 'Candidatus L. asiaticus' (CLas) and 'Ca. L. solanacearum' (CLso). All Liberibacters encode a completely conserved gene repertoire for both flagella and Tad (Tight Adherence) pili and all are missing genes critical for nucleotide biosynthesis. Both flagellar swimming and Tad pilus-mediated twitching motility in Lcr were demonstrated for the first time. A role for Tad pili in the uptake of extracellular dsDNA for food in Liberibacters was suspected because both twitching and DNA uptake are impossible without repetitive pilus extension and retraction, and no genes encoding other pilus assemblages or mechanisms for DNA uptake were predicted to be even partially present in any of the 35 fully sequenced Liberibacter genomes. Insertional mutations of the Lcr Tad pilus genes cpaA, cpaB, cpaE, cpaF and tadC all displayed such severely reduced growth and viability that none could be complemented. A mutation affecting cpaF (motor ATPase) was further characterized and the strain displayed concomitant loss of twitching, viability and reduced periplasmic uptake of extracellular dsDNA. Mutations of comEC, encoding the inner membrane competence channel, had no effect on either motility or growth but completely abolished natural transformation in Lcr. The comEC mutation was restored by complementation using comEC from Lcr but not from CLas strain psy62 or CLso strain RS100, indicating that unlike Lcr, these pathogens were not naturally competent for transformation. This report provides the first evidence that the Liberibacter Tad pili are dynamic and essential for both motility and DNA uptake, thus extending their role beyond surface adherence.
format article
author Lulu Cai
Mukesh Jain
Marta Sena-Vélez
Kathryn M Jones
Laura A Fleites
Michelle Heck
Dean W Gabriel
author_facet Lulu Cai
Mukesh Jain
Marta Sena-Vélez
Kathryn M Jones
Laura A Fleites
Michelle Heck
Dean W Gabriel
author_sort Lulu Cai
title Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.
title_short Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.
title_full Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.
title_fullStr Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.
title_full_unstemmed Tad pilus-mediated twitching motility is essential for DNA uptake and survival of Liberibacters.
title_sort tad pilus-mediated twitching motility is essential for dna uptake and survival of liberibacters.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/6535f79a11bb4d6c8b086c609f550194
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AT mukeshjain tadpilusmediatedtwitchingmotilityisessentialfordnauptakeandsurvivalofliberibacters
AT martasenavelez tadpilusmediatedtwitchingmotilityisessentialfordnauptakeandsurvivalofliberibacters
AT kathrynmjones tadpilusmediatedtwitchingmotilityisessentialfordnauptakeandsurvivalofliberibacters
AT lauraafleites tadpilusmediatedtwitchingmotilityisessentialfordnauptakeandsurvivalofliberibacters
AT michelleheck tadpilusmediatedtwitchingmotilityisessentialfordnauptakeandsurvivalofliberibacters
AT deanwgabriel tadpilusmediatedtwitchingmotilityisessentialfordnauptakeandsurvivalofliberibacters
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