Disruption without diversity loss: how spreading thermotolerant Pilidium lythri infection perturbs plant-soil microbiome stability

Abstract

While global warming accelerates phytopathogen spread, still little is known on how fungal pathogens disrupt fragile balance in plant-microbe interactions. Here, we demonstrate that the thermotolerant fungus Pilidium lythri combines broad chemical resistance with a remarkable ability to destabilize microbial communities in strawberry soil-plant systems. Using high-throughput sequencing (16S rRNA and ITS markers) across 72 samples, combined with mixed-effects modelling, source-tracking, microbiota assembly mechanisms investigation and network analysis we demonstrate that P. lythri disrupted bacterial community assembly processes, transitioning from deterministic to stochastic dynamics in the bulk soil, aligning with the Anna Karenina Principle. Despite stable dominance index (ENS) under infection bacterial and fungal communities, rhizosphere fungal diversity increased under infection. Network analysis of this niche revealed decreased fungal connectivity, with enhanced antagonistic interactions between taxa. We also noted that microbial migration patterns between niches under pathogen inoculation highlighted shifts in community interactions. Our work uncovers how emerging thermotolerant fungal phytopathogens destabilize plant holobiont without reducing diversity, important for managing emerging agricultural threats in a warming climate.