Environmental Water and Sediment Microbial Communities Shape Intestine Microbiota for Host Health: The Central Dogma in an Anthropogenic Aquaculture Ecosystem.

Zhijian Huang,Daliang Ning,Shaoping Weng,Zhixuan Deng,Jianguo He,Chengguang Xing,Zhili He,Hao Wang,Chuanle Xiao,Renjun Zhou,Shenzheng Zeng,Xisha Deng,Lingfei Yu,Jizhong Zhou,Dongdong Wei,Qingyun Yan,Dongwei Hou

doi:10.3389/fmicb.2021.772149

Abstract

From increasing evidence has emerged a tight link among the environment, intestine microbiota, and host health status; moreover, the microbial interaction in different habitats is crucial for ecosystems. However, how the environmental microbial community assembly governs the intestinal microbiota and microbial communities of multiple habitats contribute to the metacommunity remain elusive. Here, we designed two delicate experiments from temporal and spatial scales in a shrimp culture pond ecosystem (SCPE). Of the SCPE metacommunity, the microbial diversity was mainly contributed to by the diversity of–βIntraHabitats and βInterHabitats, and water and sediment communities had a large contribution to the shrimp intestine community as shown by SourceTracker and Sloan neutral community model analyses. Also, phylogenetic bin-based null model results show that microbial assembly of three habitats in the SCPE appeared to be largely driven by stochastic processes. These results enrich our understanding of the environment–intestinal microbiota–host health closely linked relationship, making it possible to be the central dogma for an anthropogenic aquaculture ecosystem. Our findings enhance the mechanistic understanding of microbial assembly in the SCPE for further analyzing metacommunities, which has important implications for microbial ecology and animal health.

Highlights

The intestinal microbiome is increasingly recognized as having a fundamental role in regulating the physiology and health of animals and humans (Clemente et al, 2012; Le Chatelier et al, 2013; Jie et al, 2017)
We aimed to understand microbial assembly mechanisms for a metacommunity of three habitats in shrimp culture pond ecosystem (SCPE) with three ecological questions: (i) What ecological processes shape the microbial community structures in the three habitats? (ii) What is the contribution of communities from each habitat to the SCPE metacommunity? (iii) Is the shrimp intestinal microbiota shaped by environmental microbial communities? To address these questions, we hypothesized that (H1) the communities of three habitats have important contributions to the SCPE microbial metacommunity and (H2) environmental microbial communities have a decisive role in shaping the shrimp intestinal microbiota
Combined with the results of SourceTracker, structure equation model (SEM), and Sloan neutral community model analyses, these results indicate that environmental microbial communities had a large contribution to the succession of shrimp intestinal microbiota in the SCPE metacommunity, which may be due to the relatively highly stochastic processes involved in the microbial assembly of the shrimp intestine

Summary

Introduction

The intestinal microbiome is increasingly recognized as having a fundamental role in regulating the physiology and health of animals and humans (Clemente et al, 2012; Le Chatelier et al, 2013; Jie et al, 2017). Both host genetics and the environment can shape the composition of the human intestinal microbiota (Benson et al, 2010; Spor et al, 2011; Turpin et al, 2016), and a recent study demonstrates that the effect of environmental factors appears to outweigh host genetics in shaping the microbiota (Rothschild et al, 2018). Microbial communities from multiple habitats in aquaculture systems (e.g., surrounding water, animal intestine, and sediment) are all closely related to the occurrence of aquatic animal diseases (Zhu et al, 2016; Hou et al, 2017, 2018; Xiong et al, 2017), challenging us to fully understand the structure, function, and interaction in such complex aquaculture ecosystems

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