Two-speed genome evolution drives pathogenicity in fungal pathogens of animals

Abstract

The origins and evolution 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. We discover that Bsal has the most repeat-rich genome of the Chytridiomycota, comprising 40.9% repetitive elements; this genome has expanded to more than 3× the length of its conspecific Bd , with autonomous and fully functional LTR/Gypsy elements contributing significantly to the expansion. The M36 metalloprotease virulence factors are highly expanded ( n = 177) in Bsal , most of which (53%) are flanked by transposable elements, suggesting they have a repeat-associated expansion. We find enrichment upstream of M36 metalloprotease genes of three novel repeat families belonging to the repeat superfamily of LINEs that are implicated with gene copy number variations. Additionally, Bsal has a highly compartmentalized genome architecture, with virulence factors enriched in gene-sparse/repeat-rich compartments, while core conserved genes are enriched in gene-rich/repeat-poor compartments. Genes upregulated during infection are primarily found in the gene-sparse/repeat-rich compartment in both Bd and Bsal . Furthermore, genes with signatures of positive selection in Bd are enriched in repeat-rich regions, suggesting these regions are a cradle for the evolution of chytrid pathogenicity. These are the hallmarks of two-speed genome evolution, and this study provides evidence of two-speed genomes in an animal pathogen, shedding light on the evolution of fungal pathogens of vertebrates driving global declines and extinctions.

Universal signatures of transposable element compartmentalization across eukaryotic genomes

“…Furthermore, TEs passively shape the distribution of genomic structural variants (including gene duplications and deletions) due to their tendency to facilitate nonallelic homologous recombination (NAHR) as well as their susceptibility to double stranded breaks during replication, with TE-rich genomic regions displaying a greater propensity for structural variation than TE-poor regions [9][10][11][12][13][14][15] (Figure 1A). TEs are non-randomly distributed across many genomes, and often show massive enrichment in specific compartments 5,[16][17][18][19] . Although TE-rich compartments are usually depleted in genes likely due to the deleterious effects of TE-associated variation, some genes show enrichment for these regions 16,[20][21][22] .…”

“…Gene ontology terms clearly related to host interactions and pathogenicity are poorly annotated for many species. Nonetheless, many pathogens show enrichment for extracellularly secreted gene products as well as various enzymes and biosynthesis processes, as revealed by manual inspection 5,19,[63][64][65][66] .…”

“…Theory 23 and empirical analysis 78,79 show that genomes can restructure themselves due to the beneficial effects of genomic structural plasticity, resulting in the colocalization between TEs and gene families for which copy number variation is beneficial. Fungal plant pathogens similarly illuminate extreme examples of TE compartmentalization wherein genomes show bimodal distributions of TE content and TE-rich compartments house genes involved in pathogenicity 5,19,71,80 . Here, we demonstrate remarkable patterns of convergence across eukaryotic lineages spanning 1.7 billion years of evolution, in which TE-compartmentalized genes primarily represent multigene families involved in the same functions and evolve under positive selection.…”

Segmental duplications drive the evolution of accessory regions in a major crop pathogen

“…Extensive duplications similarly occur in other plant pathogens (Dutheil et al ., 2016; Müller et al ., 2019; Wyka et al ., 2021; Wacker et al ., 2023) and are thought to be important drivers in co‐evolutionary arms races with their hosts. Understanding the evolution of ARs in Fusarium oxysporum can facilitate the discovery of new effector genes and provide insights into effector diversification.…”

Climate as a gatekeeper: Unexpected absence of Batrachochytrium salamandrivoran in an Asian Chytrid hotspot suggests a narrow climatic niche for Batrachochytrium salamandrivorans

“…Bsal has restricted distributional areas, co-occurring withBd in several microhabitats (Laking et al, 2017;Lötters et al, 2020). Bd -Bsal occurrences can potentially generate new genotypes with heightened pathogenicity (Farrer et al, 2011;Fisher & Garner, 2020;Wacker et al, 2023). Bsal has stronger pathogenicity compared to Bd within a shared host species, leading to more severe infection outcomes (Farrer et al, 2017).…”