Intraspecific variation at the free-living stage of a soil-borne pathogen is organized into an exploration syndrome associated with infectivity

Summary Many pathogens spend a substantial portion of their life cycle outside the host tissues. During its free-living stage, the root legume-plant pathogen Aphanomyces euteiches persists in soil either as non-motile resting oospores or actively explores the environment through mycelium and motile zoospores. These two latter stages are critical for survival, dispersal and host encounter. However, the extent of intraspecific variation during these phases remains poorly explored, and it is still unknown whether they are organized into phenotypic syndromes contributing to infection success. Here, we measured eight free-living phenotypic traits associated with mycelial and zoospore stages across 23 A. euteiches strains from distinct geographic regions (USA, Europe) whose genomes were sequenced. We tested whether traits are organized into a phenotypic syndrome linked to either geographic origin, genomic diversity or infectivity. The microbial strains exhibited substantial intraspecific phenotypic variation that we proposed as an ‘exploration syndrome’ linked to host search. Beyond this general syndrome, we detected sub-structure according to strains’ infectivity, geographic origin and genetic group. This suggests that the free-living stage of pathogens may contribute to disease potential. Our results highlight the importance of integrating functional trait approaches into plant pathology and suggest that the identified ‘exploration syndrome’ may serve as a predictor of infectivity in soilborne oomycete pathogens.