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

The plant’s 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 pathogensZymoseptoria triticiandZymoseptoria passerinii. By using microbiome metabarcoding and coculture interactions, we evaluated the influence of virulent (wild host-infecting pathogen) and avirulent (domesticated host-infecting pathogen)Zymoseptorialineages on the leaf microbiome of the wild grassesAegilops cylindricaandHordeum murinumwhich are hosts to virulent lineages ofZ. triticiandZ. 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 betweenZymoseptorialineages. 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 byZymoseptoriaspp.