Response of gut microbiota to feed-borne bacteria depends on fish growth rate: a snapshot survey of farmed juvenile Takifugu obscurus

Abstract

Understanding the ecological processes in controlling the assemblage of gut microbiota becomes an essential prerequisite for a more sustainable aquaculture. Here we used 16S rRNA amplicon sequencing to characterize the hindgut microbiota from cultured obscure puffer Takifugu obscurus. The gut microbiota is featured with lower alpha-diversity, greater beta-dispersion and higher average 16S rRNA copy numbers comparing to water and sediment, but far less so to feed. SourceTracker predicted a notable source signature from feed in gut microbiota. Furthermore, effect of varying degrees of feed-associated bacteria on compositional, functional and phylogenetic diversity of gut microbiota were revealed. Coincidently, considerable increase of species richness and feed source proportions both were observed in slow growth fugu, implying a reduced stability in gut microbiota upon bacterial disturbance from feed. Moreover, quantitative ecological analytic framework was applied and the ecological processes underlying such community shift were determined. In the context of lower degree of feed disturbance, homogeneous selection and dispersal limitation largely contribute to the community stability and partial variations among hosts. Whilst with the degree of feed disturbance increased, variable selection leads to an augmented interaction within gut microbiota, entailing community unstability and shift. Altogether, our findings illustrated a clear diversity-function relationships in fugu gut microbiota, and it has implicated in a strong correlation between feed-borne bacteria and host growth rate. These results provide a new insight into aquaculture of fugu and other economically important fishes, as well as a better understanding of host-microbe interactions in the vertebrate gastrointestinal tract. IMPORTANCEEnvironmental bacteria has a great impact on fish gut microbiota, yet little is known as to where fish acquire their gut symbionts, and how gut microbiota response to environmental bacteria. Through the integrative analysis by community profiling and source tracking, we show that feed-associated bacteria can impose a strong disturbance upon fugu gut microbiota. As a result, marked alterations in the composition and function of gut microbiota in slow growth fugu were observed, which is potentially correlated with the host physiological condition such as gastric evacuation rate. Our findings emphasized the intricate linkage between feed and gut microbiota, and highlighted the importance of resolving the feed source signal before the conclusion of comparative analysis of microbiota can be drawn. Our results provide a deeper insight into aquaculture of fugu and other economically important fishes, and have further implications for an improved understanding of host-microbe interactions in the vertebrate gastrointestinal tract.