The fungal pathogen Batrachochytrium dendrobatidis drives the relationship between environmental and amphibian skin...

Microbial coalescence is a key process driving the assembly of communities when diverse compartments of ecosystems meet. Coalescence is likely involved in structuring amphibian skin microbiota, which play a crucial role in host immunity, but whose environmental microbial sources remain unknown. Here, we investigated the microbial sources (water and biofilm microbiota, i.e. adherent microbial community embedded collectively on submerged rocks) and coalescence processes of the skin microbiota of three amphibian species (Alytes obstetricans, Rana temporaria, and Bufo spinosus), in 20 mountain lakes of the French Pyrenees, infected or not with the fungal pathogen Batrachochytrium dendrobatidis (Bd). We used 16S ribosomal ribonucleic acid gene metabarcoding coupled with a Bayesian SourceTracker analysis and a phylogenetic null model. We found that the amphibian skin microbiome originated mainly from environmental water (9%-23%), less from biofilm (3%-6%), and not from horizontal transfer. Host exposure to Bd strongly influenced microbial engraftment. The presence of the pathogen probably did not affect the number of bacterial taxa shared between environmental and skin microbiotas, but enriched some of them, including protective ones, from the water only. Stochastic processes dominated the structuration of the resulting communities, but some deterministic selection probably occurred, maybe via microbiome dysbiosis that favor higher abundance of anti-Bd genera, which often are environmental opportunists. Our study provides first insights into the importance of microbial coalescence in shaping the amphibian skin microbiome, and the role of environmental microbial communities in mounting disease resistance.