Gut microbial ecology of Xenopus tadpoles across life stages

Thibault Scalvenzi,Mickaël Bourge,Nicolas Pollet,Isabelle Clavereau

doi:10.24072/pcjournal.53

Abstract

Background: The microorganism world living in amphibians is still largely under-represented and under-studied in the literature. Among anuran amphibians, African clawed frogs of the Xenopus genus stand as well-characterized models with an in-depth knowledge of their developmental biological processes including their metamorphosis. In this study, we analyzed the succession of microbial communities and their activities across diverse body habitats of Xenopus tropicalis using different approaches including flow cytometry and 16s rDNA gene metabarcoding. We also evaluated the metabolic capacity of the premetamorphic tadpoles gut microbiome using metagenomic and metatranscriptomic sequencing. Results: We analyzed the bacterial components of the Xenopus gut microbiota, the adult gut biogeography, the succession of communities during ontogeny, the impact of the alimentation in shaping the tadpoles gut bacterial communities and the transmission of skin and fecal bacteria to the eggs. We also identified the most active gut bacteria and their metabolic contribution to tadpole physiology including carbohydrate breakdown, nitrogen recycling, essential amino-acids and vitamin biosynthesis. Conclusions: We present a comprehensive new microbiome dataset of a laboratory amphibian model. Our data provide evidences that studies on the Xenopus tadpole model can shed light on the interactions between a vertebrate host and its microbiome. We interpret our findings in light of bile acids being key molecular components regulating the gut microbiome composition during amphibian development and metamorphosis. Further studies into the metabolic interactions between amphibian tadpoles and their microbiota during early development and metamorphosis should provide useful information on the evolution of host-microbiota interactions in vertebrates.

Highlights

Metazoans are vehicles for microbial communities, named microbiota
We identified two important and significant changes: the first was an increase of bacterial species number and diversity that occurred during tadpole growth between pre and prometamorphosis (p=0.000 using betta and the breakaway estimation of richness); and the second was the opposite, namely a significant drop in species richness and diversity that occurred at the climax of metamorphosis (Figure S3 and Supplementary_table_2, (p=0.000 using betta and the breakaway estimation of richness)
We provide evidence that the diet of Xenopus tadpoles affected the diversity of their gut microbiome and that the mucosal immunity of tadpoles can interact with a variety of bacterial communities (Figure 5)

Summary

Introduction

Metazoans are vehicles for microbial communities, named microbiota. The microbiota and its metazoan host have mutualistic interactions and are thought to adapt and evolve as an holobiont (Wilson, Sober 1989; Gill et al 2006; Zilber-Rosenberg, Rosenberg 2008; Bordenstein, Theis 2015). A few years later, these results were challenged by Eugène and Elisabeth Wollmann, who observed that Rana temporaria tadpoles could complete their metamorphosis in sterile conditions (Wollman 1913). They reported that tadpoles could be fed solely with bacteria, pinpointing their nutritive roles (Wollman, Wollman 1915). Our data provide evidences that studies on the Xenopus tadpole model can shed light on the interactions between a vertebrate host and its microbiome. Further studies into the metabolic interactions between amphibian tadpoles and their microbiota during early development and metamorphosis should provide useful information on the evolution of host-microbiota interactions in vertebrates

Methods

Findings

Discussion

Conclusion