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The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses
The regulatory noncoding small RNAs (sRNAs) of bacteria are key elements influencing gene expression; however, there has been little evidence that beneficial bacteria use these molecules to communicate with their animal hosts. We report here that the bacterial sRNA SsrA plays an essential role in th...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7665748/ https://www.ncbi.nlm.nih.gov/pubmed/33141816 http://dx.doi.org/10.1371/journal.pbio.3000934 |
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author | Moriano-Gutierrez, Silvia Bongrand, Clotilde Essock-Burns, Tara Wu, Leo McFall-Ngai, Margaret J. Ruby, Edward G. |
author_facet | Moriano-Gutierrez, Silvia Bongrand, Clotilde Essock-Burns, Tara Wu, Leo McFall-Ngai, Margaret J. Ruby, Edward G. |
author_sort | Moriano-Gutierrez, Silvia |
collection | PubMed |
description | The regulatory noncoding small RNAs (sRNAs) of bacteria are key elements influencing gene expression; however, there has been little evidence that beneficial bacteria use these molecules to communicate with their animal hosts. We report here that the bacterial sRNA SsrA plays an essential role in the light-organ symbiosis between Vibrio fischeri and the squid Euprymna scolopes. The symbionts load SsrA into outer membrane vesicles, which are transported specifically into the epithelial cells surrounding the symbiont population in the light organ. Although an SsrA-deletion mutant (ΔssrA) colonized the host to a normal level after 24 h, it produced only 2/10 the luminescence per bacterium, and its persistence began to decline by 48 h. The host’s response to colonization by the ΔssrA strain was also abnormal: the epithelial cells underwent premature swelling, and host robustness was reduced. Most notably, when colonized by the ΔssrA strain, the light organ differentially up-regulated 10 genes, including several encoding heightened immune-function or antimicrobial activities. This study reveals the potential for a bacterial symbiont’s sRNAs not only to control its own activities but also to trigger critical responses promoting homeostasis in its host. In the absence of this communication, there are dramatic fitness consequences for both partners. |
format | Online Article Text |
id | pubmed-7665748 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-76657482020-11-18 The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses Moriano-Gutierrez, Silvia Bongrand, Clotilde Essock-Burns, Tara Wu, Leo McFall-Ngai, Margaret J. Ruby, Edward G. PLoS Biol Research Article The regulatory noncoding small RNAs (sRNAs) of bacteria are key elements influencing gene expression; however, there has been little evidence that beneficial bacteria use these molecules to communicate with their animal hosts. We report here that the bacterial sRNA SsrA plays an essential role in the light-organ symbiosis between Vibrio fischeri and the squid Euprymna scolopes. The symbionts load SsrA into outer membrane vesicles, which are transported specifically into the epithelial cells surrounding the symbiont population in the light organ. Although an SsrA-deletion mutant (ΔssrA) colonized the host to a normal level after 24 h, it produced only 2/10 the luminescence per bacterium, and its persistence began to decline by 48 h. The host’s response to colonization by the ΔssrA strain was also abnormal: the epithelial cells underwent premature swelling, and host robustness was reduced. Most notably, when colonized by the ΔssrA strain, the light organ differentially up-regulated 10 genes, including several encoding heightened immune-function or antimicrobial activities. This study reveals the potential for a bacterial symbiont’s sRNAs not only to control its own activities but also to trigger critical responses promoting homeostasis in its host. In the absence of this communication, there are dramatic fitness consequences for both partners. Public Library of Science 2020-11-03 /pmc/articles/PMC7665748/ /pubmed/33141816 http://dx.doi.org/10.1371/journal.pbio.3000934 Text en © 2020 Moriano-Gutierrez et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Moriano-Gutierrez, Silvia Bongrand, Clotilde Essock-Burns, Tara Wu, Leo McFall-Ngai, Margaret J. Ruby, Edward G. The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses |
title | The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses |
title_full | The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses |
title_fullStr | The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses |
title_full_unstemmed | The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses |
title_short | The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses |
title_sort | noncoding small rna ssra is released by vibrio fischeri and modulates critical host responses |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7665748/ https://www.ncbi.nlm.nih.gov/pubmed/33141816 http://dx.doi.org/10.1371/journal.pbio.3000934 |
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