Abstract

BackgroundGut microbiota plays important roles in host animal metabolism, homeostasis and environmental adaptation. However, the interplay between the gut microbiome and urochordate ascidian, the most closet relative of vertebrate, remains less explored. In this study, we characterized the gut microbial communities of urochordate ascidian (Halocynthia roretzi) across the changes of season and starvation stress using a comprehensive set of omic approaches including 16S rRNA gene amplicon sequencing, shotgun metagenomics, metabolomic profiling, and transcriptome sequencing.ResultsThe 16S rRNA gene amplicon profiling revealed that ascidians harbor indigenous gut microbiota distinctly different to the marine microbial community and significant variations in composition and abundance of gut bacteria, with predominant bacterial orders representing each season. Depressed alpha-diversities of gut microbiota were observed across starvation stress when compared to the communities in aquafarm condition. Synechococcales involving photosynthesis and its related biosynthesis was reduced in abundance while the enrichments of Xanthomonadales and Legionellales may facilitate bile acid biosynthesis during starvation. Metabolomics analysis found that long chain fatty acids, linolenic acid, cyanoamino acid, and pigments derived from gut bacteria were upregulated, suggesting a beneficial contribution of the gut microbiome to the ascidian under starvation stress.ConclusionsOur findings revealed seasonal variation of ascidian gut microbiota. Defense and energy-associated metabolites derived from gut microbiome may provide an adaptive interplay between gut microbiome and ascidian host that maintains a beneficial metabolic system across season and starvation stress. The diversity-generating metabolisms from both microbiota and host might lead to the co-evolution and environmental adaptation.Graphical

Highlights

  • Gut microbiota plays important roles in host animal metabolism, homeostasis and environmental adaptation

  • Increasing evidences indicate a defensive role of metabolic products from the symbiotic bacteria in ascidians [17], where the tunic of ascidians have been characterized as one of habitats colonized with high abundance of bacteria

  • The peritrophic membranes of ascidians formed long stringy shape twist filled with dark fecal materials

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Summary

Introduction

Gut microbiota plays important roles in host animal metabolism, homeostasis and environmental adaptation. We characterized the gut microbial communities of urochordate ascidian (Halocynthia roretzi) across the changes of season and starvation stress using a comprehensive set of omic approaches including 16S rRNA gene amplicon sequencing, shotgun metagenomics, metabolomic profiling, and transcriptome sequencing. Ascidians are known as invasive organism forming biofouling in marine aquaculture that cases economic (2020) 2:30 adaptation [8,9,10]. These bioactive compounds could be synthesized by ascidians or their bacterial symbionts [11, 12]. The seasonal and spatial dynamics of the microbial communities in the inner-tunic of two invasive ascidians, S. plicata and Herdmania momus were examined [22]

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