Phylogeny and ecological roles shaping yeast-hyphae morphogenesis in Ophiostomataceae

The Ophiostomataceae family encompasses numerous species that exhibit yeast-hyphae dimorphism, including well-known pathogens like the causal agents of Dutch elm disease, blue-staining fungi, and sporotrichosis. This dimorphism is not only observed in pathogenic interactions but also plays a crucial role in symbiotic relationships, such as ambrosia fungi. The ability to switch between these morphological forms may contribute to their adaptability and ecological functions within different environments and host interactions. This study seeks to elucidate the intricate interplay between dimorphism and fungal lifestyles across the species within the Ophiostomataceae family. We investigated six Ophiostomataceae genera: Raffaelea, Harringtonia, Leptographium, Ophiostoma, Heinzbutinia, and Esteya, representing four contrasting fungal lifestyles: ambrosia, non-ambrosia, pathogenic, and non-pathogenic. Under standardized growth conditions using a chemically defined medium with DL-proline as the sole nitrogen source, all strains, except one, exhibited increased yeast morphotype growth (≥50%). Our tested species exhibited varied responses to inoculum size, highlighting inter-species variation in response to inoculum size effects. Moreover, we traced the evolutionary history of dimorphism across the Ophiostomataceae family. Our results suggest that dimorphism was likely a trait of the common ancestor of Ophiostomataceae. Our analyses revealed that the dimorphic trait shows a strong phylogenetic signal, i.e., its presence or loss is conserved within specific phylogenetic lineages. Moreover, we found that dimorphism and ambrosia lifestyle are evolutionarily correlated across the Ophiostomataceae phylogeny. This study deepens our understanding of how the interplay between dimorphism and lifestyle has shaped the evolutionary trajectory of the Ophiostomataceae.