Amphibian skin bacteria contain a wide repertoire of genes linked to their antifungal capacities.

Abstract

Emerging diseases caused by fungi are a serious threat to wildlife biodiversity. The widespread fungal pathogen Batrachochytrium dendrobatidis (Bd) has caused dramatic amphibian population declines and species extinctions worldwide. While many amphibians have been negatively affected by Bd, some populations/species have persisted despite its presence. One factor contributing to amphibian protection against this fungus is the host-associated skin microbiome. In this study, we aimed to identify gene clusters associated with the antifungal activity of amphibian skin bacteria. Specifically, we explored skin bacteria isolated from species that have persisted in the wild despite the presence of Bd: the frogs Agalychnis callidryas, Craugastor fitzingeri, Dendropsophus ebraccatus, and the axolotl Ambystoma altamirani. Bacterial isolates were tested in vitro for their capacity to inhibit the growth of two fungal pathogens: Bd and the phytopathogen Botrytis cinerea (Bc). Genome mining of these bacterial isolates revealed a diverse repertoire of Biosynthetic Gene Clusters (BGCs) and chitin-degrading gene families (ChDGFs) whose composition and abundance differed among bacterial families. We found specific BGCs and ChDGFs that were associated with the capacity of bacteria to inhibit the growth of either Bd or Bc, suggesting that distinct fungi could be inhibited by different molecular mechanisms. By using similarity networks and machine learning, we identified BGCs encoding known antifungal compounds such as viscosin, fengycin, zwittermicin, as well as siderophores and a novel family of beta-lactones. Finally, we propose that the diversity of BGCs found in amphibian skin bacteria comprise a substantial genetic reservoir that could collectively explain the antifungal properties of the amphibian skin microbiome.