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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 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.

SUBMITTER: Xiao F

PROVIDER: S-EPMC7815754 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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

Xiao Fanshu F Zhu Wengen W Yu Yuhe Y He Zhili Z Wu Bo B Wang Cheng C Shu Longfei L Li Xinghao X Yin Huaqun H Wang Jianjun J Juneau Philippe P Zheng Xiafei X Wu Yongjie Y Li Juan J Chen Xiaojuan X Hou Dongwei D Huang Zhijian Z He Jianguo J Xu Guohuan G Xie Liwei L Huang Jie J Yan Qingyun Q

NPJ biofilms and microbiomes 20210119 1

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 successi ...[more]

PMID: 33469034

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Project description:BACKGROUND: The integration of host genetics, environmental triggers and the microbiota is a recognised factor in the pathogenesis of barrier function diseases such as IBD. In order to determine how these factors interact to regulate the host immune response and ecological succession of the colon tissue-associated microbiota, we investigated the temporal interaction between the microbiota and the host following disruption of the colonic epithelial barrier. METHODOLOGY/PRINCIPAL FINDINGS: Oral administration of DSS was applied as a mechanistic model of environmental damage of the colon and the resulting inflammation characterized for various parameters over time in WT and Nod2 KO mice. RESULTS: In WT mice, DSS damage exposed the host to the commensal flora and led to a migration of the tissue-associated bacteria from the epithelium to mucosal and submucosal layers correlating with changes in proinflammatory cytokine profiles and a progressive transition from acute to chronic inflammation of the colon. Tissue-associated bacteria levels peaked at day 21 post-DSS and declined thereafter, correlating with recruitment of innate immune cells and development of the adaptive immune response. Histological parameters, immune cell infiltration and cytokine biomarkers of inflammation were indistinguishable between Nod2 and WT littermates following DSS, however, Nod2 KO mice demonstrated significantly higher tissue-associated bacterial levels in the colon. DSS damage and Nod2 genotype independently regulated the community structure of the colon microbiota. CONCLUSIONS/SIGNIFICANCE: The results of these experiments demonstrate the integration of environmental and genetic factors in the ecological succession of the commensal flora in mammalian tissue. The association of Nod2 genotype (and other host polymorphisms) and environmental factors likely combine to influence the ecological succession of the tissue-associated microflora accounting in part for their association with the pathogenesis of inflammatory bowel diseases.

Project description:A large number of descriptive surveys have shown that microbial communities experience successional changes over time and that ecological dominance is common in the microbial world. However, direct evidence for the ecological processes mediating succession or causing ecological dominance remains rare. Different dispersal abilities among species may be a key mechanism. We surveyed fungal diversity within a metacommunity of pitchers of the model carnivorous plant Sarracenia purpurea and discovered that the yeast Candida pseudoglaebosa was ecologically dominant. Its frequency in the metacommunity increased during the growing season, and it was not replaced by other taxa. We next measured its competitive ability in a manipulative laboratory experiment and tracked its dispersal over time in nature. Despite its dominance, C. pseudoglaebosa is not a superior competitor. Instead, it is a superior disperser: it arrives in pitchers earlier, and disperses into more pitchers, than other fungi. Differential dispersal across the spatially structured metacommunity of individual pitchers emerges as a key driver of the continuous dominance of C. pseudoglaebosa during succession.IMPORTANCE Microbial communities are ubiquitous and occupy nearly every imaginable habitat and resource, including human-influenced habitats (e.g., fermenting food and hospital surfaces) and habitats with little human influence (e.g., aquatic communities living in carnivorous plant pitchers). We studied yeast communities living in pitchers of the carnivorous purple pitcher plant to understand how and why microbial communities change over time. We found that dispersal ability is not only important for fungal communities early in their existence, it can also determine which species is dominant (here, the yeast Candida pseudoglaebosa) long after the species and its competitors have arrived. These results contrast with observations from many human-influenced habitats, in which a good competitor eventually outcompetes good dispersers, since humans often design these habitats to favor a specific competitor. This study will help microbiologists understand the qualities of microbial species that enable takeover of new habitats in both natural and human-influenced environments.

Dataset Information

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

Publications

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

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