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Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development

Understanding interactions within the gut microbiome and its stability are of critical importance for deciphering ecological issues within the gut ecosystem. Recent studies indicate that long-term instability of gut microbiota is associated with human diseases, and recovery of stability is helpful i...

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Autores principales: Xiao, Fanshu, Zhu, Wengen, Yu, Yuhe, Huang, Jie, Li, Juan, He, Zhili, Wang, Jianjun, Yin, Huaqun, Yu, Huang, Liu, Shengwei, Chen, Pubo, Huang, Zhijian, He, Jianguo, Wang, Cheng, Shu, Longfei, Yan, Qingyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9045336/
https://www.ncbi.nlm.nih.gov/pubmed/35311546
http://dx.doi.org/10.1128/spectrum.01696-21
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author Xiao, Fanshu
Zhu, Wengen
Yu, Yuhe
Huang, Jie
Li, Juan
He, Zhili
Wang, Jianjun
Yin, Huaqun
Yu, Huang
Liu, Shengwei
Chen, Pubo
Huang, Zhijian
He, Jianguo
Wang, Cheng
Shu, Longfei
Yan, Qingyun
author_facet Xiao, Fanshu
Zhu, Wengen
Yu, Yuhe
Huang, Jie
Li, Juan
He, Zhili
Wang, Jianjun
Yin, Huaqun
Yu, Huang
Liu, Shengwei
Chen, Pubo
Huang, Zhijian
He, Jianguo
Wang, Cheng
Shu, Longfei
Yan, Qingyun
author_sort Xiao, Fanshu
collection PubMed
description Understanding interactions within the gut microbiome and its stability are of critical importance for deciphering ecological issues within the gut ecosystem. Recent studies indicate that long-term instability of gut microbiota is associated with human diseases, and recovery of stability is helpful in the return to health. However, much less is known about such topics in fish, which encompass nearly half of all vertebrate diversity. Here, we examined the assembly and succession of gut microbiota in more than 550 zebrafish, and evaluated the variations of microbial interactions and stability across fish development from larva to adult using molecular ecological network analysis. We found that microbial interactions and stability in the fish gut ecosystem generally increased with host development. This could be attributed to the development of the zebrafish immune system, the increasing amount of space available for microbial colonization within the gut, and the greater stability of nutrients available for the colonized microbiota in adult zebrafish. Moreover, the potential keystone taxa, even those with relatively low abundances, played important roles in affecting the microbial interactions and stability. These findings indicate that regulating rare keystone taxa in adult fish may have great potential in gut microbial management to maintain gut ecosystem stability, which could also provide references for managing gut microbiota in humans and other animals. IMPORTANCE Understanding gut microbial stability and the underlying mechanisms is an important but largely ignored ecological issue in vertebrate fish. Here, using a zebrafish model and network analysis of the gut microbiota we found that microbial interactions and stability in the gut ecosystem increase with fish development. This finding has important implications for microbial management to maintain gut homeostasis and provide better gut ecosystem services for the host. First, future studies should always consider using fish of different age groups to gain a full understanding of gut microbial networks. Second, management of the keystone taxa, even those that are only present at a low abundance, during the adult stage may be a viable pathway to maintain gut ecosystem stability. This study greatly expands our current knowledge regarding gut ecosystem stability in terms of ecological networks affected by fish development, and also highlights potential directions for gut microbial management in humans and other animals.
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spelling pubmed-90453362022-04-28 Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development Xiao, Fanshu Zhu, Wengen Yu, Yuhe Huang, Jie Li, Juan He, Zhili Wang, Jianjun Yin, Huaqun Yu, Huang Liu, Shengwei Chen, Pubo Huang, Zhijian He, Jianguo Wang, Cheng Shu, Longfei Yan, Qingyun Microbiol Spectr Research Article Understanding interactions within the gut microbiome and its stability are of critical importance for deciphering ecological issues within the gut ecosystem. Recent studies indicate that long-term instability of gut microbiota is associated with human diseases, and recovery of stability is helpful in the return to health. However, much less is known about such topics in fish, which encompass nearly half of all vertebrate diversity. Here, we examined the assembly and succession of gut microbiota in more than 550 zebrafish, and evaluated the variations of microbial interactions and stability across fish development from larva to adult using molecular ecological network analysis. We found that microbial interactions and stability in the fish gut ecosystem generally increased with host development. This could be attributed to the development of the zebrafish immune system, the increasing amount of space available for microbial colonization within the gut, and the greater stability of nutrients available for the colonized microbiota in adult zebrafish. Moreover, the potential keystone taxa, even those with relatively low abundances, played important roles in affecting the microbial interactions and stability. These findings indicate that regulating rare keystone taxa in adult fish may have great potential in gut microbial management to maintain gut ecosystem stability, which could also provide references for managing gut microbiota in humans and other animals. IMPORTANCE Understanding gut microbial stability and the underlying mechanisms is an important but largely ignored ecological issue in vertebrate fish. Here, using a zebrafish model and network analysis of the gut microbiota we found that microbial interactions and stability in the gut ecosystem increase with fish development. This finding has important implications for microbial management to maintain gut homeostasis and provide better gut ecosystem services for the host. First, future studies should always consider using fish of different age groups to gain a full understanding of gut microbial networks. Second, management of the keystone taxa, even those that are only present at a low abundance, during the adult stage may be a viable pathway to maintain gut ecosystem stability. This study greatly expands our current knowledge regarding gut ecosystem stability in terms of ecological networks affected by fish development, and also highlights potential directions for gut microbial management in humans and other animals. American Society for Microbiology 2022-03-21 /pmc/articles/PMC9045336/ /pubmed/35311546 http://dx.doi.org/10.1128/spectrum.01696-21 Text en Copyright © 2022 Xiao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Xiao, Fanshu
Zhu, Wengen
Yu, Yuhe
Huang, Jie
Li, Juan
He, Zhili
Wang, Jianjun
Yin, Huaqun
Yu, Huang
Liu, Shengwei
Chen, Pubo
Huang, Zhijian
He, Jianguo
Wang, Cheng
Shu, Longfei
Yan, Qingyun
Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development
title Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development
title_full Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development
title_fullStr Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development
title_full_unstemmed Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development
title_short Interactions and Stability of Gut Microbiota in Zebrafish Increase with Host Development
title_sort interactions and stability of gut microbiota in zebrafish increase with host development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9045336/
https://www.ncbi.nlm.nih.gov/pubmed/35311546
http://dx.doi.org/10.1128/spectrum.01696-21
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