Host-specific fungal plant pathogens exhibit distinct interactions with the leaf microbiota of wild grasses

The plants microbiome is influenced by the plant species and biotic factors such as the infection by pathogens. Pathogen-microbiome interactions are relevant for the progression of the disease since both can compete within the plant host. We hypothesize that pathogens specialized to different hosts have distinct, direct, and indirect influence on the host microbiome. We focused on the host-specific leaf pathogens Zymoseptoria tritici and Zymoseptoria passerinii. By using microbiome metabarcoding and coculture interactions, we evaluated the influence of virulent (wild host-infecting pathogen) and avirulent (domesticated host-infecting pathogen) Zymoseptoria lineages on the leaf microbiome of the wild grasses Aegilops cylindrica and Hordeum murinum which are hosts to virulent lineages of Z. tritici and Z. passerinii, respectively. Our microbiome analysis showed that the fungal communities were affected by virulent lineages, while the avirulent lineages had the most negative correlations with bacteria. Both virulent and avirulent pathogens had the same spectrum of interactions when experimentally cocultured with bacteria. The intensity of pathogen-induced growth enhancement differed between Zymoseptoria lineages. We demonstrated that sugar metabolism through the fungal secretion of invertase can be a determinant of bacterial growth enhancement. Our study highlights the role of microbial interactions on host-specificity and mechanisms underlying microbial interactions by Zymoseptoria spp.