Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages
The type VI secretion system (T6SS) mediates protein translocation across the cell membrane of Gram-negative bacteria, including Vibrio cholerae – the causative agent of cholera. All V. cholerae strains examined to date harbor gene clusters encoding a T6SS. Structural similarity and sequence homolog...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Other Authors: | |
| Format: | Article |
| Language: | en_US |
| Published: |
Public Library of Science
2013
|
| Online Access: | http://hdl.handle.net/1721.1/76789 https://orcid.org/0000-0003-4235-9962 |
| _version_ | 1826201479241793536 |
|---|---|
| author | Unterweger, Daniel Kitaoka, Maya Miyata, Sarah T. Bachmann, Verena Brooks, Teresa M. Moloney, Jessica Sosa, Oscar Abraham Silva, David Duran-Gonzalez, Jorge Provenzano, Daniele Pukatzki, Stefan |
| author2 | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Unterweger, Daniel Kitaoka, Maya Miyata, Sarah T. Bachmann, Verena Brooks, Teresa M. Moloney, Jessica Sosa, Oscar Abraham Silva, David Duran-Gonzalez, Jorge Provenzano, Daniele Pukatzki, Stefan |
| author_sort | Unterweger, Daniel |
| collection | MIT |
| description | The type VI secretion system (T6SS) mediates protein translocation across the cell membrane of Gram-negative bacteria, including Vibrio cholerae – the causative agent of cholera. All V. cholerae strains examined to date harbor gene clusters encoding a T6SS. Structural similarity and sequence homology between components of the T6SS and the T4 bacteriophage cell-puncturing device suggest that the T6SS functions as a contractile molecular syringe to inject effector molecules into prokaryotic and eukaryotic target cells. Regulation of the T6SS is critical. A subset of V. cholerae strains, including the clinical O37 serogroup strain V52, express T6SS constitutively. In contrast, pandemic strains impose tight control that can be genetically disrupted: mutations in the quorum sensing gene luxO and the newly described regulator gene tsrA lead to constitutive T6SS expression in the El Tor strain C6706. In this report, we examined environmental V. cholerae isolates from the Rio Grande with regard to T6SS regulation. Rough V. cholerae lacking O-antigen carried a nonsense mutation in the gene encoding the global T6SS regulator VasH and did not display virulent behavior towards Escherichia coli and other environmental bacteria. In contrast, smooth V. cholerae strains engaged constitutively in type VI-mediated secretion and displayed virulence towards prokaryotes (E. coli and other environmental bacteria) and a eukaryote (the social amoeba Dictyostelium discoideum). Furthermore, smooth V. cholerae strains were able to outcompete each other in a T6SS-dependent manner. The work presented here suggests that constitutive T6SS expression provides V. cholerae with an advantage in intraspecific and interspecific competition. |
| first_indexed | 2024-09-23T11:52:09Z |
| format | Article |
| id | mit-1721.1/76789 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T11:52:09Z |
| publishDate | 2013 |
| publisher | Public Library of Science |
| record_format | dspace |
| spelling | mit-1721.1/767892022-10-01T06:35:36Z Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages Unterweger, Daniel Kitaoka, Maya Miyata, Sarah T. Bachmann, Verena Brooks, Teresa M. Moloney, Jessica Sosa, Oscar Abraham Silva, David Duran-Gonzalez, Jorge Provenzano, Daniele Pukatzki, Stefan Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Sosa, Oscar Abraham Sosa, Oscar Abraham The type VI secretion system (T6SS) mediates protein translocation across the cell membrane of Gram-negative bacteria, including Vibrio cholerae – the causative agent of cholera. All V. cholerae strains examined to date harbor gene clusters encoding a T6SS. Structural similarity and sequence homology between components of the T6SS and the T4 bacteriophage cell-puncturing device suggest that the T6SS functions as a contractile molecular syringe to inject effector molecules into prokaryotic and eukaryotic target cells. Regulation of the T6SS is critical. A subset of V. cholerae strains, including the clinical O37 serogroup strain V52, express T6SS constitutively. In contrast, pandemic strains impose tight control that can be genetically disrupted: mutations in the quorum sensing gene luxO and the newly described regulator gene tsrA lead to constitutive T6SS expression in the El Tor strain C6706. In this report, we examined environmental V. cholerae isolates from the Rio Grande with regard to T6SS regulation. Rough V. cholerae lacking O-antigen carried a nonsense mutation in the gene encoding the global T6SS regulator VasH and did not display virulent behavior towards Escherichia coli and other environmental bacteria. In contrast, smooth V. cholerae strains engaged constitutively in type VI-mediated secretion and displayed virulence towards prokaryotes (E. coli and other environmental bacteria) and a eukaryote (the social amoeba Dictyostelium discoideum). Furthermore, smooth V. cholerae strains were able to outcompete each other in a T6SS-dependent manner. The work presented here suggests that constitutive T6SS expression provides V. cholerae with an advantage in intraspecific and interspecific competition. Canadian Institutes of Health Research (Operating Grant MOP-84473) Alberta Heritage Foundation for Medical Research (Alberta Innovates-Health Solutions, Endowment Fund) National Institutes of Health (U.S.) (grant MD001091-01) National Institutes of Health (U.S.) (grant GM068855-02) Olegario V. Rana Fellowship Alberta Heritage Foundation for Medical Research (Alberta Innovates-Health Solutions Graduate Studentships) 2013-02-12T22:29:23Z 2013-02-12T22:29:23Z 2012-10 2012-07 Article http://purl.org/eprint/type/JournalArticle 1932-6203 http://hdl.handle.net/1721.1/76789 Unterweger, Daniel et al. “Constitutive Type VI Secretion System Expression Gives Vibrio Cholerae Intra- and Interspecific Competitive Advantages.” Ed. Thierry Soldati. PLoS ONE 7.10 (2012): e48320. Web. https://orcid.org/0000-0003-4235-9962 en_US http://dx.doi.org/10.1371/journal.pone.0048320 PLoS One Creative Commons Attribution http://creativecommons.org/licenses/by/2.5/ application/pdf Public Library of Science PLoS |
| spellingShingle | Unterweger, Daniel Kitaoka, Maya Miyata, Sarah T. Bachmann, Verena Brooks, Teresa M. Moloney, Jessica Sosa, Oscar Abraham Silva, David Duran-Gonzalez, Jorge Provenzano, Daniele Pukatzki, Stefan Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages |
| title | Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages |
| title_full | Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages |
| title_fullStr | Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages |
| title_full_unstemmed | Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages |
| title_short | Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages |
| title_sort | constitutive type vi secretion system expression gives vibrio cholerae intra and interspecific competitive advantages |
| url | http://hdl.handle.net/1721.1/76789 https://orcid.org/0000-0003-4235-9962 |
| work_keys_str_mv | AT unterwegerdaniel constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT kitaokamaya constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT miyatasaraht constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT bachmannverena constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT brooksteresam constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT moloneyjessica constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT sosaoscarabraham constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT silvadavid constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT durangonzalezjorge constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT provenzanodaniele constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages AT pukatzkistefan constitutivetypevisecretionsystemexpressiongivesvibriocholeraeintraandinterspecificcompetitiveadvantages |