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The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility

BACKGROUND: The type VI protein secretion system (T6SS) is important in diverse cellular processes in Gram-negative bacteria, including interactions with other bacteria and with eukaryotic hosts. In this study we analyze the evolution of the T6SS in the genus Xanthomonas and evaluate its importance...

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Autores principales: Montenegro Benavides, Nathaly Andrea, Alvarez B., Alejandro, Arrieta-Ortiz, Mario L., Rodriguez-R, Luis Miguel, Botero, David, Tabima, Javier Felipe, Castiblanco, Luisa, Trujillo, Cesar, Restrepo, Silvia, Bernal, Adriana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7788950/
https://www.ncbi.nlm.nih.gov/pubmed/33407123
http://dx.doi.org/10.1186/s12866-020-02066-1
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author Montenegro Benavides, Nathaly Andrea
Alvarez B., Alejandro
Arrieta-Ortiz, Mario L.
Rodriguez-R, Luis Miguel
Botero, David
Tabima, Javier Felipe
Castiblanco, Luisa
Trujillo, Cesar
Restrepo, Silvia
Bernal, Adriana
author_facet Montenegro Benavides, Nathaly Andrea
Alvarez B., Alejandro
Arrieta-Ortiz, Mario L.
Rodriguez-R, Luis Miguel
Botero, David
Tabima, Javier Felipe
Castiblanco, Luisa
Trujillo, Cesar
Restrepo, Silvia
Bernal, Adriana
author_sort Montenegro Benavides, Nathaly Andrea
collection PubMed
description BACKGROUND: The type VI protein secretion system (T6SS) is important in diverse cellular processes in Gram-negative bacteria, including interactions with other bacteria and with eukaryotic hosts. In this study we analyze the evolution of the T6SS in the genus Xanthomonas and evaluate its importance of the T6SS for virulence and in vitro motility in Xanthomonas phaseoli pv. manihotis (Xpm), the causal agent of bacterial blight in cassava (Manihot esculenta). We delineate the organization of the T6SS gene clusters in Xanthomonas and then characterize proteins of this secretion system in Xpm strain CIO151. RESULTS: We describe the presence of three different clusters in the genus Xanthomonas that vary in their organization and degree of synteny between species. Using a gene knockout strategy, we also found that vgrG and hcp are required for maximal aggressiveness of Xpm on cassava plants while clpV is important for both motility and maximal aggressiveness. CONCLUSION: We characterized the T6SS in 15 different strains in Xanthomonas and our phylogenetic analyses suggest that the T6SS might have been acquired by a very ancient event of horizontal gene transfer and maintained through evolution, hinting at their importance for the adaptation of Xanthomonas to their hosts. Finally, we demonstrated that the T6SS of Xpm is functional, and significantly contributes to virulence and motility. This is the first experimental study that demonstrates the role of the T6SS in the Xpm-cassava interaction and the T6SS organization in the genus Xanthomonas. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-020-02066-1.
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spelling pubmed-77889502021-01-07 The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility Montenegro Benavides, Nathaly Andrea Alvarez B., Alejandro Arrieta-Ortiz, Mario L. Rodriguez-R, Luis Miguel Botero, David Tabima, Javier Felipe Castiblanco, Luisa Trujillo, Cesar Restrepo, Silvia Bernal, Adriana BMC Microbiol Research Article BACKGROUND: The type VI protein secretion system (T6SS) is important in diverse cellular processes in Gram-negative bacteria, including interactions with other bacteria and with eukaryotic hosts. In this study we analyze the evolution of the T6SS in the genus Xanthomonas and evaluate its importance of the T6SS for virulence and in vitro motility in Xanthomonas phaseoli pv. manihotis (Xpm), the causal agent of bacterial blight in cassava (Manihot esculenta). We delineate the organization of the T6SS gene clusters in Xanthomonas and then characterize proteins of this secretion system in Xpm strain CIO151. RESULTS: We describe the presence of three different clusters in the genus Xanthomonas that vary in their organization and degree of synteny between species. Using a gene knockout strategy, we also found that vgrG and hcp are required for maximal aggressiveness of Xpm on cassava plants while clpV is important for both motility and maximal aggressiveness. CONCLUSION: We characterized the T6SS in 15 different strains in Xanthomonas and our phylogenetic analyses suggest that the T6SS might have been acquired by a very ancient event of horizontal gene transfer and maintained through evolution, hinting at their importance for the adaptation of Xanthomonas to their hosts. Finally, we demonstrated that the T6SS of Xpm is functional, and significantly contributes to virulence and motility. This is the first experimental study that demonstrates the role of the T6SS in the Xpm-cassava interaction and the T6SS organization in the genus Xanthomonas. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-020-02066-1. BioMed Central 2021-01-06 /pmc/articles/PMC7788950/ /pubmed/33407123 http://dx.doi.org/10.1186/s12866-020-02066-1 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Montenegro Benavides, Nathaly Andrea
Alvarez B., Alejandro
Arrieta-Ortiz, Mario L.
Rodriguez-R, Luis Miguel
Botero, David
Tabima, Javier Felipe
Castiblanco, Luisa
Trujillo, Cesar
Restrepo, Silvia
Bernal, Adriana
The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
title The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
title_full The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
title_fullStr The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
title_full_unstemmed The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
title_short The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
title_sort type vi secretion system of xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7788950/
https://www.ncbi.nlm.nih.gov/pubmed/33407123
http://dx.doi.org/10.1186/s12866-020-02066-1
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