The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility
Abstract 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 imp...
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| Format: | Article |
| Language: | English |
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BMC
2021-01-01
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| Series: | BMC Microbiology |
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| Online Access: | https://doi.org/10.1186/s12866-020-02066-1 |
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| author | Nathaly Andrea Montenegro Benavides Alejandro Alvarez B. Mario L. Arrieta-Ortiz Luis Miguel Rodriguez-R David Botero Javier Felipe Tabima Luisa Castiblanco Cesar Trujillo Silvia Restrepo Adriana Bernal |
| author_facet | Nathaly Andrea Montenegro Benavides Alejandro Alvarez B. Mario L. Arrieta-Ortiz Luis Miguel Rodriguez-R David Botero Javier Felipe Tabima Luisa Castiblanco Cesar Trujillo Silvia Restrepo Adriana Bernal |
| author_sort | Nathaly Andrea Montenegro Benavides |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-14T01:05:57Z |
| format | Article |
| id | doaj.art-5c5c1cc619244dee8f6b8b0bd8378897 |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-12-14T01:05:57Z |
| publishDate | 2021-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-5c5c1cc619244dee8f6b8b0bd83788972022-12-21T23:22:59ZengBMCBMC Microbiology1471-21802021-01-0121111210.1186/s12866-020-02066-1The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motilityNathaly Andrea Montenegro Benavides0Alejandro Alvarez B.1Mario L. Arrieta-Ortiz2Luis Miguel Rodriguez-R3David Botero4Javier Felipe Tabima5Luisa Castiblanco6Cesar Trujillo7Silvia Restrepo8Adriana Bernal9Department of Biological Sciences, Universidad de los AndesDepartment of Biological Sciences, Universidad de los AndesInstitute for Systems BiologyDepartment of Microbiology and Digital Science Center (DiSC), University of InnsbruckDepartment of Biological Sciences, Universidad de los AndesBotany and Plant Pathology Department, Oregon State UniversityDepartment of Biological Sciences, Universidad de los AndesDepartment of Biological Sciences, Universidad de los AndesDepartment of Biological Sciences, Universidad de los AndesDepartment of Biological Sciences, Universidad de los AndesAbstract 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.https://doi.org/10.1186/s12866-020-02066-1Type VI secretionHcpVgrIcmFClpV, Xanthomonas, bacterial pathogenesis |
| spellingShingle | Nathaly Andrea Montenegro Benavides Alejandro Alvarez B. Mario L. Arrieta-Ortiz Luis Miguel Rodriguez-R David Botero Javier Felipe Tabima Luisa Castiblanco Cesar Trujillo Silvia Restrepo Adriana Bernal The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility BMC Microbiology Type VI secretion Hcp Vgr IcmF ClpV, Xanthomonas, bacterial pathogenesis |
| 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 | Type VI secretion Hcp Vgr IcmF ClpV, Xanthomonas, bacterial pathogenesis |
| url | https://doi.org/10.1186/s12866-020-02066-1 |
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