Repeat-driven genome expansion and two-speed genome architecture of amphibian-infecting chytrids

Over the past half century, the chytridiomycosis panzootic has led to the decline of over 500 amphibian species with 90 attributed extinctions. Chytridiomycosis of amphibians is caused by two fungal species Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). The genetic mechanisms underlying host-specificity and pathology in the Batrachochytrium genus remain elusive and their evolution and origins of virulence are largely unknown. Using deep nanopore sequencing, we found that Bsal is extremely repeat-rich with high numbers of long terminal repeats, long interspersed nuclear elements and transposable elements. This repeat-driven genome expansion in Bsal has resulted in a tripling of its length compared with Bd. Key pathogenicity genes including M36 metalloproteases have expanded compared with Bd, and are enriched for flanking transposable elements, suggesting its genome expansion is connected to selective evolutionary processes. Both batrachochytrids have evidence of a two speed genome architecture, including an enrichment of functional categories in compartments of repeat richness or sparsity. Furthermore, among Bd lineages, M36 metalloproteases with signatures of positive selection and, both in Bsal and Bd, genes upregulated during infection in vivo are enriched in repeat-rich and gene-sparse compartment of the genome. This is the first evidence for a two-speed genome in an animal pathogen, shedding new light on the role of repetitive sequences on the evolution of fungal pathogens driving global declines and extinctions of amphibians.