Abstract
While emerging fungi threaten global biodiversity, the paucity of fungal genome assemblies impedes thoroughly characterizing epidemics and developing effective mitigation strategies. Here, we generate de novo genomic assemblies for six outbreaks of the emerging pathogen Batrachochytrium salamandrivorans (Bsal). We reveal the European epidemic currently damaging amphibian populations to comprise multiple, highly divergent lineages demonstrating isolate-specific adaptations and metabolic capacities. In particular, we show extensive gene family expansions and acquisitions, through a variety of evolutionary mechanisms, and an isolate-specific saprotrophic lifecycle. This finding both explains the chytrid’s ability to divorce transmission from host density, producing Bsal’s enigmatic host population declines, and is a key consideration in developing successful mitigation measures.
Highlights
While emerging fungi threaten global biodiversity, the paucity of fungal genome assemblies impedes thoroughly characterizing epidemics and developing effective mitigation strategies
We sequenced nine Batrachochytrium salamandrivorans (Bsal) isolates collected from six outbreak sites, all associated with fire salamander (Salamandra salamandra) dieoffs and together spanning much of the geographical and temporal range of the European outbreak, using both Pacific Biosciences (PacBio) and Illumina sequencing technologies
Principal component analysis (PCA), variant, and gene presence–absence analyses of the Illumina data indicated that isolates within “time-series pairs” appear to cluster together, displaying apparently lower variation compared to that observed between outbreak sites, and this supported considering one assembly per outbreak site as representative
Summary
While emerging fungi threaten global biodiversity, the paucity of fungal genome assemblies impedes thoroughly characterizing epidemics and developing effective mitigation strategies. We sought to describe the variation present within the European outbreak, using Pacific Biosciences (PacBio) Sequel and Illumina data to assemble highly contiguous de novo assemblies for isolates from six outbreaks, generate a dated phylogeny, and investigate evolutionary rates and mechanisms These per-outbreak assemblies exposed the scope of intraspecific variation in both genome size and composition, as well as isolatespecific protein acquisitions, losses, and expansions, and facilitated the investigation of Bsal evolution including horizontal gene transfer (HGT) events occurring after lineage divergence. These analyses guided the discovery of an isolate-specific saprotrophic lifecycle, a finding that both helps to explain Bsal’s devastating host population declines and necessitates a substantial redirection of current mitigation efforts, which largely focus on amphibian hosts
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