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SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner

Both the bacterial flagellum and the evolutionary related injectisome encoded on the Salmonella pathogenicity island 1 (SPI-1) play crucial roles during the infection cycle of Salmonella species. The interplay of both is highlighted by the complex cross-regulation that includes transcriptional contr...

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Autores principales: Saleh, Doaa Osama, Horstmann, Julia A., Giralt-Zúñiga, María, Weber, Willi, Kaganovitch, Eugen, Durairaj, Abilash Chakravarthy, Klotzsch, Enrico, Strowig, Till, Erhardt, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10298799/
https://www.ncbi.nlm.nih.gov/pubmed/37315106
http://dx.doi.org/10.1371/journal.ppat.1011451
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author Saleh, Doaa Osama
Horstmann, Julia A.
Giralt-Zúñiga, María
Weber, Willi
Kaganovitch, Eugen
Durairaj, Abilash Chakravarthy
Klotzsch, Enrico
Strowig, Till
Erhardt, Marc
author_facet Saleh, Doaa Osama
Horstmann, Julia A.
Giralt-Zúñiga, María
Weber, Willi
Kaganovitch, Eugen
Durairaj, Abilash Chakravarthy
Klotzsch, Enrico
Strowig, Till
Erhardt, Marc
author_sort Saleh, Doaa Osama
collection PubMed
description Both the bacterial flagellum and the evolutionary related injectisome encoded on the Salmonella pathogenicity island 1 (SPI-1) play crucial roles during the infection cycle of Salmonella species. The interplay of both is highlighted by the complex cross-regulation that includes transcriptional control of the flagellar master regulatory operon flhDC by HilD, the master regulator of SPI-1 gene expression. Contrary to the HilD-dependent activation of flagellar gene expression, we report here that activation of HilD resulted in a dramatic loss of motility, which was dependent on the presence of SPI-1. Single cell analyses revealed that HilD-activation triggers a SPI-1-dependent induction of the stringent response and a substantial decrease in proton motive force (PMF), while flagellation remains unaffected. We further found that HilD activation enhances the adhesion of Salmonella to epithelial cells. A transcriptome analysis revealed a simultaneous upregulation of several adhesin systems, which, when overproduced, phenocopied the HilD-induced motility defect. We propose a model where the SPI-1-dependent depletion of the PMF and the upregulation of adhesins upon HilD-activation enable flagellated Salmonella to rapidly modulate their motility during infection, thereby enabling efficient adhesion to host cells and delivery of effector proteins.
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spelling pubmed-102987992023-06-28 SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner Saleh, Doaa Osama Horstmann, Julia A. Giralt-Zúñiga, María Weber, Willi Kaganovitch, Eugen Durairaj, Abilash Chakravarthy Klotzsch, Enrico Strowig, Till Erhardt, Marc PLoS Pathog Research Article Both the bacterial flagellum and the evolutionary related injectisome encoded on the Salmonella pathogenicity island 1 (SPI-1) play crucial roles during the infection cycle of Salmonella species. The interplay of both is highlighted by the complex cross-regulation that includes transcriptional control of the flagellar master regulatory operon flhDC by HilD, the master regulator of SPI-1 gene expression. Contrary to the HilD-dependent activation of flagellar gene expression, we report here that activation of HilD resulted in a dramatic loss of motility, which was dependent on the presence of SPI-1. Single cell analyses revealed that HilD-activation triggers a SPI-1-dependent induction of the stringent response and a substantial decrease in proton motive force (PMF), while flagellation remains unaffected. We further found that HilD activation enhances the adhesion of Salmonella to epithelial cells. A transcriptome analysis revealed a simultaneous upregulation of several adhesin systems, which, when overproduced, phenocopied the HilD-induced motility defect. We propose a model where the SPI-1-dependent depletion of the PMF and the upregulation of adhesins upon HilD-activation enable flagellated Salmonella to rapidly modulate their motility during infection, thereby enabling efficient adhesion to host cells and delivery of effector proteins. Public Library of Science 2023-06-14 /pmc/articles/PMC10298799/ /pubmed/37315106 http://dx.doi.org/10.1371/journal.ppat.1011451 Text en © 2023 Saleh et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Saleh, Doaa Osama
Horstmann, Julia A.
Giralt-Zúñiga, María
Weber, Willi
Kaganovitch, Eugen
Durairaj, Abilash Chakravarthy
Klotzsch, Enrico
Strowig, Till
Erhardt, Marc
SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner
title SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner
title_full SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner
title_fullStr SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner
title_full_unstemmed SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner
title_short SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner
title_sort spi-1 virulence gene expression modulates motility of salmonella typhimurium in a proton motive force- and adhesins-dependent manner
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10298799/
https://www.ncbi.nlm.nih.gov/pubmed/37315106
http://dx.doi.org/10.1371/journal.ppat.1011451
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