The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes.
Bacterial pathogens typically infect only a limited range of hosts; however, the genetic mechanisms governing host-specificity are poorly understood. The alpha-proteobacterial genus Bartonella comprises 21 species that cause host-specific intraerythrocytic bacteremia as hallmark of infection in thei...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2010-06-01
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| Series: | PLoS Pathogens |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20548954/?tool=EBI |
| _version_ | 1830284996842094592 |
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| author | Muriel Vayssier-Taussat Danielle Le Rhun Hong Kuan Deng Francis Biville Sandra Cescau Antoine Danchin Geneviève Marignac Evelyne Lenaour Henri Jean Boulouis Maria Mavris Lionel Arnaud Huanming Yang Jing Wang Maxime Quebatte Philipp Engel Henri Saenz Christoph Dehio |
| author_facet | Muriel Vayssier-Taussat Danielle Le Rhun Hong Kuan Deng Francis Biville Sandra Cescau Antoine Danchin Geneviève Marignac Evelyne Lenaour Henri Jean Boulouis Maria Mavris Lionel Arnaud Huanming Yang Jing Wang Maxime Quebatte Philipp Engel Henri Saenz Christoph Dehio |
| author_sort | Muriel Vayssier-Taussat |
| collection | DOAJ |
| description | Bacterial pathogens typically infect only a limited range of hosts; however, the genetic mechanisms governing host-specificity are poorly understood. The alpha-proteobacterial genus Bartonella comprises 21 species that cause host-specific intraerythrocytic bacteremia as hallmark of infection in their respective mammalian reservoirs, including the human-specific pathogens Bartonella quintana and Bartonella bacilliformis that cause trench fever and Oroya fever, respectively. Here, we have identified bacterial factors that mediate host-specific erythrocyte colonization in the mammalian reservoirs. Using mouse-specific Bartonella birtlesii, human-specific Bartonella quintana, cat-specific Bartonella henselae and rat-specific Bartonella tribocorum, we established in vitro adhesion and invasion assays with isolated erythrocytes that fully reproduce the host-specificity of erythrocyte infection as observed in vivo. By signature-tagged mutagenesis of B. birtlesii and mutant selection in a mouse infection model we identified mutants impaired in establishing intraerythrocytic bacteremia. Among 45 abacteremic mutants, five failed to adhere to and invade mouse erythrocytes in vitro. The corresponding genes encode components of the type IV secretion system (T4SS) Trw, demonstrating that this virulence factor laterally acquired by the Bartonella lineage is directly involved in adherence to erythrocytes. Strikingly, ectopic expression of Trw of rat-specific B. tribocorum in cat-specific B. henselae or human-specific B. quintana expanded their host range for erythrocyte infection to rat, demonstrating that Trw mediates host-specific erythrocyte infection. A molecular evolutionary analysis of the trw locus further indicated that the variable, surface-located TrwL and TrwJ might represent the T4SS components that determine host-specificity of erythrocyte parasitism. In conclusion, we show that the laterally acquired Trw T4SS diversified in the Bartonella lineage to facilitate host-restricted adhesion to erythrocytes in a wide range of mammals. |
| first_indexed | 2024-12-19T03:31:09Z |
| format | Article |
| id | doaj.art-06e645ff011546a4992a24115a4f7c41 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-19T03:31:09Z |
| publishDate | 2010-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-06e645ff011546a4992a24115a4f7c412022-12-21T20:37:30ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742010-06-0166e100094610.1371/journal.ppat.1000946The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes.Muriel Vayssier-TaussatDanielle Le RhunHong Kuan DengFrancis BivilleSandra CescauAntoine DanchinGeneviève MarignacEvelyne LenaourHenri Jean BoulouisMaria MavrisLionel ArnaudHuanming YangJing WangMaxime QuebattePhilipp EngelHenri SaenzChristoph DehioBacterial pathogens typically infect only a limited range of hosts; however, the genetic mechanisms governing host-specificity are poorly understood. The alpha-proteobacterial genus Bartonella comprises 21 species that cause host-specific intraerythrocytic bacteremia as hallmark of infection in their respective mammalian reservoirs, including the human-specific pathogens Bartonella quintana and Bartonella bacilliformis that cause trench fever and Oroya fever, respectively. Here, we have identified bacterial factors that mediate host-specific erythrocyte colonization in the mammalian reservoirs. Using mouse-specific Bartonella birtlesii, human-specific Bartonella quintana, cat-specific Bartonella henselae and rat-specific Bartonella tribocorum, we established in vitro adhesion and invasion assays with isolated erythrocytes that fully reproduce the host-specificity of erythrocyte infection as observed in vivo. By signature-tagged mutagenesis of B. birtlesii and mutant selection in a mouse infection model we identified mutants impaired in establishing intraerythrocytic bacteremia. Among 45 abacteremic mutants, five failed to adhere to and invade mouse erythrocytes in vitro. The corresponding genes encode components of the type IV secretion system (T4SS) Trw, demonstrating that this virulence factor laterally acquired by the Bartonella lineage is directly involved in adherence to erythrocytes. Strikingly, ectopic expression of Trw of rat-specific B. tribocorum in cat-specific B. henselae or human-specific B. quintana expanded their host range for erythrocyte infection to rat, demonstrating that Trw mediates host-specific erythrocyte infection. A molecular evolutionary analysis of the trw locus further indicated that the variable, surface-located TrwL and TrwJ might represent the T4SS components that determine host-specificity of erythrocyte parasitism. In conclusion, we show that the laterally acquired Trw T4SS diversified in the Bartonella lineage to facilitate host-restricted adhesion to erythrocytes in a wide range of mammals.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20548954/?tool=EBI |
| spellingShingle | Muriel Vayssier-Taussat Danielle Le Rhun Hong Kuan Deng Francis Biville Sandra Cescau Antoine Danchin Geneviève Marignac Evelyne Lenaour Henri Jean Boulouis Maria Mavris Lionel Arnaud Huanming Yang Jing Wang Maxime Quebatte Philipp Engel Henri Saenz Christoph Dehio The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathogens |
| title | The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. |
| title_full | The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. |
| title_fullStr | The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. |
| title_full_unstemmed | The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. |
| title_short | The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. |
| title_sort | trw type iv secretion system of bartonella mediates host specific adhesion to erythrocytes |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20548954/?tool=EBI |
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