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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...

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Autores principales: Moriano-Gutierrez, Silvia, Bongrand, Clotilde, Essock-Burns, Tara, Wu, Leo, McFall-Ngai, Margaret J., Ruby, Edward G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
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.
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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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