Panzootic chytrid fungus exploits diverse amphibian host environments through plastic infection strategies

Abstract

While some pathogens are limited to single species, others can colonize many hosts, likely contributing to the emergence of novel disease outbreaks. Despite this biodiversity threat, traits associated with host niche expansions are not well understood in multihost pathogens. Here, we aimed to uncover functional machinery driving multihost invasion by focusing on Batrachochytrium dendrobatidis (Bd), a pathogen that infects the skin of hundreds of amphibians worldwide. We performed a meta‐analysis of Bd gene expression using data from published infection experiments and newly generated profiles. We analysed Bd transcriptomic landscapes across the skin of 14 host species, reconstructed Bd isolates phylogenetic relationships, and inferred the origin and evolutionary history of differentially expressed genes under a phylogenetic framework comprising other 12 zoosporic fungi. Bd displayed plastic infection strategies when challenged by hosts with different disease susceptibility. Our analyses identified sets of differentially expressed genes under host environments with similar infection outcome. We stressed nutritional immunity and gene silencing as important processes required to overcome challenging skin environments in less susceptible hosts. Overall, Bd genes expressed during amphibian skin exploitation have arisen mainly via gene duplications with great family expansions, increasing the gene copy events previously described for this fungal species. Finally, we provide a comprehensive gene data set that can be used to further examine eco‐evolutionary hypotheses for this host‐pathogen system. Our study supports the idea that host environments exert contrasting selective pressures, such that gene expression plasticity could be one of the evolutionary keys leading to the success of multihost pathogens.

Evolutionary ecology of host competence after a chytrid outbreak in a naive amphibian community

“…During the epizootic, we observed a reduction in species contributions to community disease dynamics ( figure 4 ; electronic supplementary material, table S5), with more than half of the species exhibiting reductions in abundance, infection prevalence and infection intensity (electronic supplementary material, tables S1 and S5). This pattern could result from selection processes operating on hosts, on the pathogen or both [ 26 , 47 ].…”

Discovery of an endogenous DNA virus in the amphibian killing fungus and its association with pathogen genotype and virulence

“…It is conceivable that the expression of metalloproteases during infection triggers the frog immune system, with downregulation associated with immune evasion. Resolving this issue will require understanding the expression of the M36 metalloproteases and other virulence-associated genes, which are known to have upregulated expression on the frog host 32 .…”

Linking pathogen–microbiome–host interactions to explain amphibian population dynamics

“…Our nucleotide‐based metrics were computed from variants identified through a restriction enzyme sequencing method and included neutral markers, so even with an overall decrease of the genetic diversity, Bd ‐infected coquí frogs can still harbour variation in functional genomic locations for adaptation to Bd infection. Targeting defence (epi)genetic regions including the components of the MHC (Fu & Waldman, 2017; Richmond et al, 2009) and genes involved in mechanisms that impede pathogen growth, such as nutritional immune‐related genes (Torres‐Sánchez et al, 2022), could further improve our understanding of population dynamics, especially to generate better predictions of its evolutionary trajectory.…”