Two-speed genome expansion drives the evolution of pathogenicity in animal fungal pathogens

Abstract

The origins of virulence in amphibian-infecting chytrids Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) are largely unknown. Here, we use deep nanopore sequencing of Bsal and comparative genomics against 21 high-quality genome assemblies that span the fungal Chytridiomycota. Bsal has the most repeat-rich genome, comprising 40.9% repetitive elements, which has expanded to more than 3X the length of its conspecific Bd. M36 metalloprotease virulence factors are highly expanded in Bsal and 53% of the 177 unique genes are flanked by transposable elements, suggesting repeat-driven expansion. The largest M36 sub-family are mostly (84%) flanked upstream by a novel LINE element, a repeat superfamily implicated with gene copy number variations. We find that Bsal has a highly compartmentalized genome architecture, with virulence factors enriched in gene-sparse/repeat-rich compartments, while core conserved genes occur in gene-rich/repeat-poor compartments. This is a hallmark of two-speed genome evolution. Furthermore, genes with signatures of positive selection in Bd are enriched in repeat-rich regions, suggesting they are a cradle for chytrid pathogenicity evolution, and Bd also has a two-speed genome. This is the first evidence of two-speed genomes in any animal pathogen, and sheds new light on the evolution of fungal pathogens of vertebrates driving global declines and extinctions.

Lifestyles shape genome size and gene content in fungal pathogens

“…Some other genetic mechanisms that contribute to genome expansion have been attributed to rapid adaptation of pathogens to hosts and these include accessory chromosomes (Croll & McDonald, 2012) or TE activity (Mat Razali et al, 2019), often linking the emergence of pathogenicity to genome size expansion (Raffaele & Kamoun, 2012). For instance, TE expansions are known to play a role in the emergence of new virulence genes in emerging pathogens (Bao et al, 2017; Wacker et al, 2021).…”