The soil-borne fungus Verticillium dahliae differentially employs molecular tools to establish interactions with phylogenetically distant terrestrial microalgae

The ubiquitous soil-borne fungus Verticillium dahliae is a notorious pathogen of hundreds of vascular plant species. In absence of a suitable plant host, V. dahliae resides in the soil where it encounters, and interacts with, a rich soil microbial community. In addition to bacteria and other fungi, this soil microbial community contains significant numbers of unicellular microalgae. Considering the capacity of V. dahliae to interact with plant hosts, we set out to test if this fungus evolved strategies to interact with microalgae. To this end, we co-cultured V. dahliae with phylogenetically diverse terrestrial microalgal species, showing that it engages in stable interactions with microalgae, ranging from beneficial to detrimental depending on the algal lineage. These differential interactions are characterized by close physical associations, often resulting in the formation of interspecies biofilms. Transcriptomic analyses showed that V. dahliae mounts fundamentally different transcriptional programs, which depend on the microalgal partner. These findings show that the plant pathogenic fungus V. dahliae has the capability to establish symbiotic interactions with extremely divergent plant lineages through different lifestyles, ranging from mutualistic to pathogenic, and readily adapts to these different host niches by utilizing host-specific molecular toolkits.