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Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus

INTRODUCTION: The intestinal microbiota participates in host physiology and pathology through metabolites, in which short-chain fatty acids (SCFAs) are considered principal products and have extensive influence on intestine homeostasis. It has been reported that skin ulceration syndrome (SUS), the d...

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Autores principales: Song, Mingshan, Zhang, Zhen, Li, Yanan, Xiang, Yangxi, Li, Chenghua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10616862/
https://www.ncbi.nlm.nih.gov/pubmed/37915855
http://dx.doi.org/10.3389/fmicb.2023.1263731
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author Song, Mingshan
Zhang, Zhen
Li, Yanan
Xiang, Yangxi
Li, Chenghua
author_facet Song, Mingshan
Zhang, Zhen
Li, Yanan
Xiang, Yangxi
Li, Chenghua
author_sort Song, Mingshan
collection PubMed
description INTRODUCTION: The intestinal microbiota participates in host physiology and pathology through metabolites, in which short-chain fatty acids (SCFAs) are considered principal products and have extensive influence on intestine homeostasis. It has been reported that skin ulceration syndrome (SUS), the disease of Apostichopus japonicus caused by Vibrio splendidus, is associated with the alteration of the intestinal microbiota composition. METHOD: To investigate whether the intestinal microbiota affects A. japonicus health via SCFAs, in this study, we focus on the SCFA profiling and intestinal barrier function in A. japonicus treated with V. splendidus. RESULTS AND DISCUSSION: We found that V. splendidus could destroy the mid-intestine integrity and downregulate the expression of tight junction proteins ZO-1 and occludin in A. japonicus, which further dramatically decreased microorganism abundance and altered SCFAs contents. Specifically, acetic acid is associated with the largest number of microorganisms and has a significant correlation with occludin and ZO-1 among the seven SCFAs. Furthermore, our findings showed that acetic acid could maintain the intestinal barrier function by increasing the expression of tight junction proteins and rearranging the tight junction structure by regulating F-actin in mid-intestine epithelial cells. Thus, our results provide insights into the effects of the gut microbiome and SCFAs on intestine barrier homeostasis and provide essential knowledge for intervening in SUS by targeting metabolites or the gut microbiota.
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spelling pubmed-106168622023-11-01 Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus Song, Mingshan Zhang, Zhen Li, Yanan Xiang, Yangxi Li, Chenghua Front Microbiol Microbiology INTRODUCTION: The intestinal microbiota participates in host physiology and pathology through metabolites, in which short-chain fatty acids (SCFAs) are considered principal products and have extensive influence on intestine homeostasis. It has been reported that skin ulceration syndrome (SUS), the disease of Apostichopus japonicus caused by Vibrio splendidus, is associated with the alteration of the intestinal microbiota composition. METHOD: To investigate whether the intestinal microbiota affects A. japonicus health via SCFAs, in this study, we focus on the SCFA profiling and intestinal barrier function in A. japonicus treated with V. splendidus. RESULTS AND DISCUSSION: We found that V. splendidus could destroy the mid-intestine integrity and downregulate the expression of tight junction proteins ZO-1 and occludin in A. japonicus, which further dramatically decreased microorganism abundance and altered SCFAs contents. Specifically, acetic acid is associated with the largest number of microorganisms and has a significant correlation with occludin and ZO-1 among the seven SCFAs. Furthermore, our findings showed that acetic acid could maintain the intestinal barrier function by increasing the expression of tight junction proteins and rearranging the tight junction structure by regulating F-actin in mid-intestine epithelial cells. Thus, our results provide insights into the effects of the gut microbiome and SCFAs on intestine barrier homeostasis and provide essential knowledge for intervening in SUS by targeting metabolites or the gut microbiota. Frontiers Media S.A. 2023-10-17 /pmc/articles/PMC10616862/ /pubmed/37915855 http://dx.doi.org/10.3389/fmicb.2023.1263731 Text en Copyright © 2023 Song, Zhang, Li, Xiang and Li. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Song, Mingshan
Zhang, Zhen
Li, Yanan
Xiang, Yangxi
Li, Chenghua
Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus
title Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus
title_full Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus
title_fullStr Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus
title_full_unstemmed Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus
title_short Midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in Apostichopus japonicus
title_sort midgut microbiota affects the intestinal barrier by producing short-chain fatty acids in apostichopus japonicus
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10616862/
https://www.ncbi.nlm.nih.gov/pubmed/37915855
http://dx.doi.org/10.3389/fmicb.2023.1263731
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