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

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-ß IntraHabitats and ß InterHabitats , 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.

Stochastic processes shape the bacterial community assembly in shrimp cultural pond sediments.

Sediment environments harbor a repertoire of microorganisms that contribute to animal health and the microecosystem in aquaculture ecosystems, but their community diversity and the potential factors that control it remain unclear. Here, we applied 16S rRNA gene amplicon sequencing to investigate bacterial diversity and assembly mechanisms in the sediments of shrimp cultural ponds at the mesoscale. Our results showed that sediment bacterial communities contained 10,333 operational taxonomic units (OTUs) but had only 34 core OTUs and that the relative abundances of these core OTUs were significantly correlated with the physicochemical properties of the sediments. Proteobacteria, Bacteroidetes, Chloroflexi, Cyanobacteria, Acidobacteria, Firmicutes, Actinobacteria, Ignavibacteriae, Spirochaetae and Planctomycetes were the ten most abundant bacterial phyla. Notably, some opportunistic pathogens (e.g. Vibrio and Photobacterium) and potential functional microbes (e.g. Nitrospira, Nitrosomonas, Desulfobulbus and Desulfuromusa) were widely distributed in shrimp cultural pond sediments. More importantly, we found that there was a significant negative but weak distance-decay relationship among bacterial communities in shrimp culture pond sediments at the mesoscale, and that the spatial turnover of these bacterial communities appeared to be largely driven by stochastic processes. Additionally, environmental factors, such as pH and total nitrogen, also played important roles in influencing the sediment bacterial structure. Our findings enhance our understanding of microbial ecology in aquatic ecosystems and facilitate sediment microbiota management in aquaculture. KEY POINTS: • Core bacterial taxa in cultural pond sediments contributed to the shrimp health and element cycling. • There was a significant negative distance-decay relationship among bacterial communities in shrimp culture pond sediments at the mesoscale, and its spatial turnover appeared to be largely driven by stochastic processes. • Environmental factors (e.g. pH and total nitrogen) played important roles in influencing bacterial structure in shrimp cultural pond sediments.

Intestine Bacterial Community Composition of Shrimp Varies Under Low- and High-Salinity Culture Conditions.

Intestine microbiota is tightly associated with host health status. Increasing studies have focused on assessing how host intestine microbiota is affected by biotic factors but ignored abiotic factors. Here, we aimed to understand the effects of salinity on shrimp intestine microbiota, by comparing the differences of intestine bacterial signatures of shrimp under low-salinity (LS) and high-salinity (HS) culture conditions. Our results found that intestine core bacterial taxa of shrimp under LS and HS culture conditions were different and that under HS contained more opportunistic pathogen species. Notably, compared with LS culture conditions, opportunistic pathogens (e.g., Vibrio species) were enriched in shrimp intestine under HS. Network analysis revealed that shrimp under HS culture conditions exhibited less connected and lower competitive intestine bacterial interspecies interactions compared with LS. In addition, under HS culture conditions, several opportunistic pathogens were identified as keystone species of intestine bacterial network in shrimp. Furthermore, the ecological drift process played a more important role in the intestine bacterial assembly of shrimp under HS culture conditions than that under LS. These above traits regarding the intestine microbiota of shrimp under HS culture conditions might lead to host at a higher risk of disease. Collectively, this work aids our understanding of the effects of salinity on shrimp intestine microbiota and helps for shrimp culture.

Microecological Koch's postulates reveal that intestinal microbiota dysbiosis contributes to shrimp white feces syndrome.

BACKGROUND: Recently, increasing evidence supports that some complex diseases are not attributed to a given pathogen, but dysbiosis in the host intestinal microbiota (IM). The full intestinal ecosystem alterations, rather than a single pathogen, are associated with white feces syndrome (WFS), a globally severe non-infectious shrimp disease, while no experimental evidence to explore the causality. Herein, we conducted comprehensive metagenomic and metabolomic analysis, and intestinal microbiota transplantation (IMT) to investigate the causal relationship between IM dysbiosis and WFS. RESULTS: Compared to the Control shrimp, we found dramatically decreased microbial richness and diversity in WFS shrimp. Ten genera, such as Vibrio, Candidatus Bacilloplasma, Photobacterium, and Aeromonas, were overrepresented in WFS, whereas 11 genera, including Shewanella, Chitinibacter, and Rhodobacter were enriched in control. The divergent changes in these populations might contribute the observation that a decline of pathways conferring lipoic acid metabolism and mineral absorption in WFS. Meanwhile, some sorts of metabolites, especially lipids and organic acids, were found to be related to the IM alteration in WFS. Integrated with multiomics and IMT, we demonstrated that significant alterations in the community composition, functional potentials, and metabolites of IM were closely linked to shrimp WFS. The distinguished metabolites which were attributed to the IM dysbiosis were validated by feed-supplementary challenge. Both homogenous selection and heterogeneous selection process were less pronounced in WFS microbial community assembly. Notably, IMT shrimp from WFS donors eventually developed WFS clinical signs, while the dysbiotic IM can be recharacterized in recipient shrimp. CONCLUSIONS: Collectively, our findings offer solid evidence of the causality between IM dysbiosis and shrimp WFS, which exemplify the 'microecological Koch's postulates' (an intestinal microbiota dysbiosis, a disease) in disease etiology, and inspire our cogitation on etiology from an ecological perspective. Video abstract.

Intestinal bacterial signatures of white feces syndrome in shrimp.

Increasing evidence suggests that the intestinal microbiota is closely correlated with the host's health status. Thus, a serious disturbance that disrupts the stability of the intestinal microecosystem could cause host disease. Shrimps are one of the most important products among fishery trading commodities. However, digestive system diseases, such as white feces syndrome (WFS), frequently occur in shrimp culture and have led to enormous economic losses across the world. The WFS occurrences are unclear. Here, we compared intestinal bacterial communities of WFS shrimp and healthy shrimp. Intestinal bacterial communities of WFS shrimp exhibited less diversity but were more heterogeneous than those of healthy shrimp. The intestinal bacterial communities were significantly different between WFS shrimp and healthy shrimp; compared with healthy shrimp, in WFS shrimp, Candidatus Bacilloplasma and Phascolarctobacterium were overrepresented, whereas Paracoccus and Lactococcus were underrepresented. PICRUSt functional predictions indicated that the relative abundances of genes involved in energy metabolism and genetic information processing were significantly greater in WFS shrimp. Collectively, we found that the composition and predicted functions of the intestinal bacterial community were markedly shifted by WFS. Significant increases in Candidatus Bacilloplasma and Phascolarctobacterium and decreases in Paracoccus and Lactococcus may contribute to WFS in shrimp.

Environmental Factors Shape Water Microbial Community Structure and Function in Shrimp Cultural Enclosure Ecosystems.

The effects of environmental factors on water microbial communities have been extensively studied, but little is known about the effects in shrimp cultural enclosure ecosystems. We analyzed 16S rRNA gene amplicons to determine the principal environmental factors that shape the structure and function of microbial communities in shrimp cultural enclosure ecosystems from Guangdong and Hainan provinces, in China. High quality sequences were clustered into operational taxonomic units (OTUs) at the 97% similarity level, generating 659-1,835 OTUs per sample. The 10 most abundant phyla were Proteobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Actinobacteria, Verrucomicrobia, Firmicutes, Chlorobi, Chloroflexi, and Chlamydiae. The results of canonical correspondence analyses (CCA) indicated that salinity, total phosphate (TP), total nitrogen (TN), temperature, and pH were the most important factors shaping microbial community structure. Differences in microbial community structure between high and low salinity samples were explained by changes in the relative abundances of some OTUs (e.g., OTU5, OTU19, OTU21, OTU39, and OTU71). Moreover, the contribution of spatial distribution to the microbial community assembly was investigated via aggregated boosted tree (ABT) analyses, and the results indicated spatial isolation was not a major factor affecting the phylogenetic diversity and phylotypes of water microbial communities. Furthermore, we predicted water microbial community functional profiling using the PICRUSt program and principal component analyses (PCA) suggested that salinity was a major contributor to the structure and function of the microbial communities. Collectively, these results showed that environmental factors influenced the structure and function of water microbial communities, while salinity was the principal environmental factor instead of temperature, TP, TN, and pH in shrimp cultural enclosure ecosystems.