Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota

Abstract Clarifying mechanisms underlying the ecological succession of gut microbiota is a central theme of gut ecology. Under experimental manipulations of zebrafish hatching and rearing environments, we test our core hypothesis that the host development will overwhelm environmental dispersal in go...

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Main Authors: Fanshu Xiao, Wengen Zhu, Yuhe Yu, Zhili He, Bo Wu, Cheng Wang, Longfei Shu, Xinghao Li, Huaqun Yin, Jianjun Wang, Philippe Juneau, Xiafei Zheng, Yongjie Wu, Juan Li, Xiaojuan Chen, Dongwei Hou, Zhijian Huang, Jianguo He, Guohuan Xu, Liwei Xie, Jie Huang, Qingyun Yan
Format: Article
Language:English
Published: Nature Publishing Group 2021-01-01
Series:npj Biofilms and Microbiomes
Online Access:https://doi.org/10.1038/s41522-020-00176-2
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author Fanshu Xiao
Wengen Zhu
Yuhe Yu
Zhili He
Bo Wu
Cheng Wang
Longfei Shu
Xinghao Li
Huaqun Yin
Jianjun Wang
Philippe Juneau
Xiafei Zheng
Yongjie Wu
Juan Li
Xiaojuan Chen
Dongwei Hou
Zhijian Huang
Jianguo He
Guohuan Xu
Liwei Xie
Jie Huang
Qingyun Yan
spellingShingle Fanshu Xiao
Wengen Zhu
Yuhe Yu
Zhili He
Bo Wu
Cheng Wang
Longfei Shu
Xinghao Li
Huaqun Yin
Jianjun Wang
Philippe Juneau
Xiafei Zheng
Yongjie Wu
Juan Li
Xiaojuan Chen
Dongwei Hou
Zhijian Huang
Jianguo He
Guohuan Xu
Liwei Xie
Jie Huang
Qingyun Yan
Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
npj Biofilms and Microbiomes
author_facet Fanshu Xiao
Wengen Zhu
Yuhe Yu
Zhili He
Bo Wu
Cheng Wang
Longfei Shu
Xinghao Li
Huaqun Yin
Jianjun Wang
Philippe Juneau
Xiafei Zheng
Yongjie Wu
Juan Li
Xiaojuan Chen
Dongwei Hou
Zhijian Huang
Jianguo He
Guohuan Xu
Liwei Xie
Jie Huang
Qingyun Yan
author_sort Fanshu Xiao
title Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
title_short Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
title_full Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
title_fullStr Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
title_full_unstemmed Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
title_sort host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota
publisher Nature Publishing Group
series npj Biofilms and Microbiomes
issn 2055-5008
publishDate 2021-01-01
description Abstract Clarifying mechanisms underlying the ecological succession of gut microbiota is a central theme of gut ecology. Under experimental manipulations of zebrafish hatching and rearing environments, we test our core hypothesis that the host development will overwhelm environmental dispersal in governing fish gut microbial community succession due to host genetics, immunology, and gut nutrient niches. We find that zebrafish developmental stage substantially explains the gut microbial community succession, whereas the environmental effects do not significantly affect the gut microbiota succession from larvae to adult fish. The gut microbiotas of zebrafish are clearly separated according to fish developmental stages, and the degree of homogeneous selection governing gut microbiota succession is increasing with host development. This study advances our mechanistic understanding of the gut microbiota assembly and succession by integrating the host and environmental effects, which also provides new insights into the gut ecology of other aquatic animals.
url https://doi.org/10.1038/s41522-020-00176-2
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spelling doaj-e313bd322c374893bf9df8e91a41da152021-01-24T12:44:31ZengNature Publishing Groupnpj Biofilms and Microbiomes2055-50082021-01-017111210.1038/s41522-020-00176-2Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiotaFanshu Xiao0Wengen Zhu1Yuhe Yu2Zhili He3Bo Wu4Cheng Wang5Longfei Shu6Xinghao Li7Huaqun Yin8Jianjun Wang9Philippe Juneau10Xiafei Zheng11Yongjie Wu12Juan Li13Xiaojuan Chen14Dongwei Hou15Zhijian Huang16Jianguo He17Guohuan Xu18Liwei Xie19Jie Huang20Qingyun Yan21Environmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityKey Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of SciencesKey Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of SciencesEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityKey Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of SciencesKey Laboratory of Biometallurgy of Ministry of Education, School of Minerals Processing and Bioengineering, Central South UniversityState Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of SciencesDepartment of Biological Science, GRIL, TOXEN, Ecotoxicology of Aquatic Microorganisms Laboratory, Université du Québec à Montréal, Succursale Centre-VilleEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityCollege of Agronomy, Hunan Agricultural UniversityKey Laboratory of Ecological Impacts of Hydraulic-Projects and Restoration of Aquatic Ecosystem of Ministry of Water Resources, Institute of Hydroecology, Ministry of Water Resources and Chinese Academy of SciencesEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityState Key Laboratory of Applied Microbiology Southern China, Guangdong Institute of Microbiology, Guangdong Academy of SciencesState Key Laboratory of Applied Microbiology Southern China, Guangdong Institute of Microbiology, Guangdong Academy of SciencesKey Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of SciencesEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityAbstract Clarifying mechanisms underlying the ecological succession of gut microbiota is a central theme of gut ecology. Under experimental manipulations of zebrafish hatching and rearing environments, we test our core hypothesis that the host development will overwhelm environmental dispersal in governing fish gut microbial community succession due to host genetics, immunology, and gut nutrient niches. We find that zebrafish developmental stage substantially explains the gut microbial community succession, whereas the environmental effects do not significantly affect the gut microbiota succession from larvae to adult fish. The gut microbiotas of zebrafish are clearly separated according to fish developmental stages, and the degree of homogeneous selection governing gut microbiota succession is increasing with host development. This study advances our mechanistic understanding of the gut microbiota assembly and succession by integrating the host and environmental effects, which also provides new insights into the gut ecology of other aquatic animals.https://doi.org/10.1038/s41522-020-00176-2