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Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro

BACKGROUND: A foodborne pathogen, Vibrio vulnificus, encounters normal microflora inhabiting the gut environments prior to causing fatal septicemia or gastroenteritis and should overcome the barriers derived from the gut commensals for successful infection. Its interactions with gut commensals durin...

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Autores principales: Kim, Jeong-A, Jang, Bo-Ram, Kim, Yu-Ra, Jung, You-Chul, Kim, Kun-Soo, Lee, Kyu-Ho
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8293591/
https://www.ncbi.nlm.nih.gov/pubmed/34284824
http://dx.doi.org/10.1186/s40168-021-01095-w
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author Kim, Jeong-A
Jang, Bo-Ram
Kim, Yu-Ra
Jung, You-Chul
Kim, Kun-Soo
Lee, Kyu-Ho
author_facet Kim, Jeong-A
Jang, Bo-Ram
Kim, Yu-Ra
Jung, You-Chul
Kim, Kun-Soo
Lee, Kyu-Ho
author_sort Kim, Jeong-A
collection PubMed
description BACKGROUND: A foodborne pathogen, Vibrio vulnificus, encounters normal microflora inhabiting the gut environments prior to causing fatal septicemia or gastroenteritis and should overcome the barriers derived from the gut commensals for successful infection. Its interactions with gut commensals during the infection process, however, have not yet been understood. In the present study, the effect of V. vulnificus on the community structures of gut microbiota in mice was examined. RESULTS: Analyses of microbiota in the fecal samples of mice that died due to V. vulnificus infection revealed the decreased abundance of bacteria belonged to Bacteroidetes, notably, the species Bacteroides vulgatus. In vitro coculturing of the two bacterial species resulted in the decreased survival of B. vulgatus. The antagonistic effect of V. vulnificus against B. vulgatus was found to be mediated by cyclo-Phe-Pro (cFP), one of the major compounds secreted by V. vulnificus. cFP-treated B. vulgatus showed collapsed cellular morphology with an undulated cell surface, enlarged periplasmic space, and lysed membranes, suggesting the occurrence of membrane disruption. The degree of membrane disruption caused by cFP was dependent upon the cellular levels of ObgE in B. vulgatus. Recombinant ObgE exhibited a high affinity to cFP at a 1:1 ratio. When mice were orally injected with cFP, their feces contained significantly reduced B. vulgatus levels, and their susceptibility to V. vulnificus infection was considerably increased. CONCLUSIONS: This study demonstrates that V. vulnificus-derived cFP modulates the abundance of the predominant species among gut commensals, which made V. vulnificus increase its pathogenicity in the hosts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01095-w.
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spelling pubmed-82935912021-07-21 Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro Kim, Jeong-A Jang, Bo-Ram Kim, Yu-Ra Jung, You-Chul Kim, Kun-Soo Lee, Kyu-Ho Microbiome Research BACKGROUND: A foodborne pathogen, Vibrio vulnificus, encounters normal microflora inhabiting the gut environments prior to causing fatal septicemia or gastroenteritis and should overcome the barriers derived from the gut commensals for successful infection. Its interactions with gut commensals during the infection process, however, have not yet been understood. In the present study, the effect of V. vulnificus on the community structures of gut microbiota in mice was examined. RESULTS: Analyses of microbiota in the fecal samples of mice that died due to V. vulnificus infection revealed the decreased abundance of bacteria belonged to Bacteroidetes, notably, the species Bacteroides vulgatus. In vitro coculturing of the two bacterial species resulted in the decreased survival of B. vulgatus. The antagonistic effect of V. vulnificus against B. vulgatus was found to be mediated by cyclo-Phe-Pro (cFP), one of the major compounds secreted by V. vulnificus. cFP-treated B. vulgatus showed collapsed cellular morphology with an undulated cell surface, enlarged periplasmic space, and lysed membranes, suggesting the occurrence of membrane disruption. The degree of membrane disruption caused by cFP was dependent upon the cellular levels of ObgE in B. vulgatus. Recombinant ObgE exhibited a high affinity to cFP at a 1:1 ratio. When mice were orally injected with cFP, their feces contained significantly reduced B. vulgatus levels, and their susceptibility to V. vulnificus infection was considerably increased. CONCLUSIONS: This study demonstrates that V. vulnificus-derived cFP modulates the abundance of the predominant species among gut commensals, which made V. vulnificus increase its pathogenicity in the hosts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01095-w. BioMed Central 2021-07-20 /pmc/articles/PMC8293591/ /pubmed/34284824 http://dx.doi.org/10.1186/s40168-021-01095-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Kim, Jeong-A
Jang, Bo-Ram
Kim, Yu-Ra
Jung, You-Chul
Kim, Kun-Soo
Lee, Kyu-Ho
Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro
title Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro
title_full Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro
title_fullStr Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro
title_full_unstemmed Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro
title_short Vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-Phe-Pro
title_sort vibrio vulnificus induces the death of a major bacterial species in the mouse gut via cyclo-phe-pro
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8293591/
https://www.ncbi.nlm.nih.gov/pubmed/34284824
http://dx.doi.org/10.1186/s40168-021-01095-w
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