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.

Key Drivers of Ecological Assembly in the Hindgut of Atlantic Cod (Gadus morhua) when Fed with a Macroalgal Supplemented diet – How Robust Is the Gut to Taxonomic Perturbation?

“…This is consistent with Hayes et al (2020) 41 , where the authors showed neutral processes dominated the gut microbiome in farmed Atlantic salmon ( Salmo salar ). In contrast, however, other authors have found a decreasing influence of neutral processes over time in zebrafish ( Danio rerio ) gut microbial communities 42,43 . However, environmental conditions (e.g.…”

“…This may point to host-associated factors, however, it is difficult to say with certainty in our study design if patterns are due to host-associated pressures. Host development was found to be a significant influence on driving deterministic microbial community assembly in the zebrafish gut 42 . However, host pressures in the juvenile or adult cod gut are not widely described, a study design similar to the zebrafish study but with Atlantic cod could help elucidate these factors.…”

Probiotics in Fish Nutrition—Long-Standing Household Remedy or Native Nutraceuticals?

“…However, to maintain its basic intestinal functionality, the host also actively selects for symbiotic and commensal microorganisms. Therefore, the gut microbiota is influenced by both external factors and the selective pressure exerted by the host [23][24][25][26]. Compared to the surrounding environment, the microbial communities associated with an organism are regarded as relatively stable, particularly those in the GIT [27,28], which assures metabolic, nutritional, and immunologic functionality.…”

Quantifying the Importance of Abiotic and Biotic Factors Governing the Succession of Gut Microbiota Over Shrimp Ontogeny

“…However, it seems that the gut microbiota of larval shrimp is more similar with the rearing bacterioplankton community, compared with the adults (Burns et al, 2016;Xiong et al, 2018). A possible explanation is that the selection on external taxa is increased as host matured (Xiong et al, 2019a;Xiao et al, 2021). However, the deteriorated water quality imposes stress on shrimp, which in turn depresses their capability of filtering on external taxa (Xiong et al, 2017).…”

“…Accordingly, there is non-linear trend in the relative importance of deterministicity in governing the gut microbiota over shrimp development (Xiong et al, 2019b). It is now recognized that the gut microbiota is conjointly affected by rearing geochemical variables, bacterioplankton, and host development (Xiong et al, 2019b;Xiao et al, 2021), while little is known on the interplay among these variables. Theoretical evidence has proposed that the successional pattern of host-associated (e.g., gut microbiota) communities is distinct from that of free-living bacteria (e.g., bacterioplankton) (Baselga, 2010;Xiong et al, 2019b), whereas experimental evidence is lacking.…”