Computational modeling of accessory chromosome transfers and pathogenicity in soil-borne fungi

Abstract

Soil-borne fungi fill in several different niches in soil ecology, from saprophytes through mutualistic endophytes to parasites. Interestingly, the ecological role of fungi in being either a pathogen or a commensal is not set in stone. Instead, several fungal species have now been reported to horizontally transfer pathogenicity genes. An intriguing mechanism of horizontal transfer that has been identified in several fungal species is the transfer of accessory chromosomes – chromosomes that are not essential and can therefore be lost and gained dynamically. Although horizontal chromosome transfer in fungi was reported as early as 1998, its evolutionary consequences, especially in relation to pathogenicity and disease in agriculture, are not well understood. To that end, we here present a spatial individual-based model of soil-borne fungi, with which we investigate the eco-evolutionary effects of horizontal chromosome transfer. We primarily focus on how horizontal transfer affects the prevalence of pathogenicity in a natural fungal/plant ecosystem, and how agricultural crop rotation shapes these complex dynamics. Our results suggest that the horizontal transfer of accessory chromosomes helps the survival of parasites by two distinct mechanisms. First, the ability to lose and regain accessory chromosomes increases evolvability, an effect that leads to a pronounced benefit of horizontal transfer during long-term crop rotation. Secondly, we also observe that horizontal transfer allows pathogenicity genes to escape the effects of weak selection or drift, an effect that is relevant even under monoculture conditions. Finally, the model naturally selects for accessory chromosomes enriched in pathogenicity genes, as observed in nature. These insights show us how horizontal transfer – a process that is known to massively impact prokaryotic evolution – has important consequences for fungal evolution and disease epidemiology, highlighting the need for more research into this field.