ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage.
Listeria monocytogenes (Lm) is a ubiquitous bacterium able to survive and thrive within the environment and readily colonizes a wide range of substrates, often as a biofilm. It is also a facultative intracellular pathogen, which actively invades diverse hosts and induces listeriosis. So far, these t...
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2013
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oai:doaj.org-article:aa1a86c8e0a74af0a68e1874ffb914872021-11-18T06:06:06ZActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage.1553-73661553-737410.1371/journal.ppat.1003131https://doaj.org/article/aa1a86c8e0a74af0a68e1874ffb914872013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23382675/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Listeria monocytogenes (Lm) is a ubiquitous bacterium able to survive and thrive within the environment and readily colonizes a wide range of substrates, often as a biofilm. It is also a facultative intracellular pathogen, which actively invades diverse hosts and induces listeriosis. So far, these two complementary facets of Lm biology have been studied independently. Here we demonstrate that the major Lm virulence determinant ActA, a PrfA-regulated gene product enabling actin polymerization and thereby promoting its intracellular motility and cell-to-cell spread, is critical for bacterial aggregation and biofilm formation. We show that ActA mediates Lm aggregation via direct ActA-ActA interactions and that the ActA C-terminal region, which is not involved in actin polymerization, is essential for aggregation in vitro. In mice permissive to orally-acquired listeriosis, ActA-mediated Lm aggregation is not observed in infected tissues but occurs in the gut lumen. Strikingly, ActA-dependent aggregating bacteria exhibit an increased ability to persist within the cecum and colon lumen of mice, and are shed in the feces three order of magnitude more efficiently and for twice as long than bacteria unable to aggregate. In conclusion, this study identifies a novel function for ActA and illustrates that in addition to contributing to its dissemination within the host, ActA plays a key role in Lm persistence within the host and in transmission from the host back to the environment.Laetitia TravierStéphanie GuadagniniEdith GouinAlexandre DufourViviane Chenal-FrancisquePascale CossartJean-Christophe Olivo-MarinJean-Marc GhigoOlivier DissonMarc LecuitPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 1, p e1003131 (2013) |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Laetitia Travier Stéphanie Guadagnini Edith Gouin Alexandre Dufour Viviane Chenal-Francisque Pascale Cossart Jean-Christophe Olivo-Marin Jean-Marc Ghigo Olivier Disson Marc Lecuit ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. |
description |
Listeria monocytogenes (Lm) is a ubiquitous bacterium able to survive and thrive within the environment and readily colonizes a wide range of substrates, often as a biofilm. It is also a facultative intracellular pathogen, which actively invades diverse hosts and induces listeriosis. So far, these two complementary facets of Lm biology have been studied independently. Here we demonstrate that the major Lm virulence determinant ActA, a PrfA-regulated gene product enabling actin polymerization and thereby promoting its intracellular motility and cell-to-cell spread, is critical for bacterial aggregation and biofilm formation. We show that ActA mediates Lm aggregation via direct ActA-ActA interactions and that the ActA C-terminal region, which is not involved in actin polymerization, is essential for aggregation in vitro. In mice permissive to orally-acquired listeriosis, ActA-mediated Lm aggregation is not observed in infected tissues but occurs in the gut lumen. Strikingly, ActA-dependent aggregating bacteria exhibit an increased ability to persist within the cecum and colon lumen of mice, and are shed in the feces three order of magnitude more efficiently and for twice as long than bacteria unable to aggregate. In conclusion, this study identifies a novel function for ActA and illustrates that in addition to contributing to its dissemination within the host, ActA plays a key role in Lm persistence within the host and in transmission from the host back to the environment. |
format |
article |
author |
Laetitia Travier Stéphanie Guadagnini Edith Gouin Alexandre Dufour Viviane Chenal-Francisque Pascale Cossart Jean-Christophe Olivo-Marin Jean-Marc Ghigo Olivier Disson Marc Lecuit |
author_facet |
Laetitia Travier Stéphanie Guadagnini Edith Gouin Alexandre Dufour Viviane Chenal-Francisque Pascale Cossart Jean-Christophe Olivo-Marin Jean-Marc Ghigo Olivier Disson Marc Lecuit |
author_sort |
Laetitia Travier |
title |
ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. |
title_short |
ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. |
title_full |
ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. |
title_fullStr |
ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. |
title_full_unstemmed |
ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. |
title_sort |
acta promotes listeria monocytogenes aggregation, intestinal colonization and carriage. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2013 |
url |
https://doaj.org/article/aa1a86c8e0a74af0a68e1874ffb91487 |
work_keys_str_mv |
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