Abstract
Pathogenic fungi constitute a growing threat to both plant and animal species on a global scale. Despite a clonal mode of reproduction dominating the population genetic structure of many fungi, putatively asexual species are known to adapt rapidly when confronted by efforts to control their growth and transmission. However, the mechanisms by which adaptive diversity is generated across a clonal background are often poorly understood. We sequenced a global panel of the emergent amphibian pathogen, Batrachochytrium dendrobatidis (Bd), to high depth and characterized rapidly changing features of its genome that we believe hold the key to the worldwide success of this organism. Our analyses show three processes that contribute to the generation of de novo diversity. Firstly, we show that the majority of wild isolates manifest chromosomal copy number variation that changes over short timescales. Secondly, we show that cryptic recombination occurs within all lineages of Bd, leading to large regions of the genome being in linkage equilibrium, and is preferentially associated with classes of genes of known importance for virulence in other pathosystems. Finally, we show that these classes of genes are under directional selection, and that this has predominantly targeted the Global Panzootic Lineage (BdGPL). Our analyses show that Bd manifests an unusually dynamic genome that may have been shaped by its association with the amphibian host. The rates of variation that we document likely explain the high levels of phenotypic variability that have been reported for Bd, and suggests that the dynamic genome of this pathogen has contributed to its success across multiple biomes and host-species.
Highlights
A diverse cadre of fungi and fungal-like oomycetes have recently taken centre stage as emerging infectious diseases (EIDs) owing to their increasing impact on animals, plants and wider ecosystem health [1]
We report three novel features of genome diversity linked to pathogenicity in the emerging amphibian pathogen, Batrachochytrium dendrobatidis (Bd)
We identified widespread chromosome copy number variation (CCNV) across our lineages, with individual isolates harboring between 2 to 5 copies of each chromosome and rapid rates of chromosomal copy-number variation (CCNV) occurring in culture
Summary
A diverse cadre of fungi and fungal-like oomycetes have recently taken centre stage as emerging infectious diseases (EIDs) owing to their increasing impact on animals, plants and wider ecosystem health [1]. Maintaining the pool of genetic diversity necessary to respond to selection is facilitated by the ability of fungi to utilise multiple reproductive modes, including cryptic recombination that enables inbreeding, outcrossing, hybridization, and the generation of diversity via parasexual mechanisms [5] These features are suspected to have contributed to the rise of contemporary fungal EIDs, which play a major role in host population declines across a broad swathe of plant and animal species [1,6,7]. It is increasingly apparent that pathogenic fungi manifest highly plastic genome architecture in the form of variable numbers of individual chromosomes, known as chromosomal copy-number variation (CCNV) or aneuploidy This feature has been identified across the fungal phylum Ascomycota, ranging from Botrytis cinerea [8], Histoplasma capsulatum [9], Saccharomyces cerevisiae [10], Candida albicans [11] and the Basidiomycota Cryptococcus neoformans [12,13,14]. Stress occurring as a consequence of either host response or exposure to antifungal
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