Dysbiosis in leaf microbiome caused by Xanthomonas

Dysbiosis is characterized by a perturbed microbiota associated with host disease. In both plants and animals, the innate immune system contributes to maintain microbiota homeostasis in healthy organisms, with NADPH oxidases playing a crucial role. In Arabidopsis thaliana, the absence of NADPH oxidase RBOHD can lead to an altered leaf microbiota, including an enrichment of opportunistic Xanthomonas pathogens. It is currently unclear whether the microbiota change occurs independently of the opportunistic pathogens or is caused by the latter. Here, we tested the hypothesis that the opportunistic pathogen mediates the microbiota shift by secreting enzymes via the type-2 secretion system (T2SS). We found that the opportunistic Xanthomonas strains secrete a cocktail of cell wall degrading enzymes, which degrade leaf tissue and promote Xanthomonas growth during plant infection. Both disease severity and leaf degradation activity were increased in rbohD compared to Col-0 plants, attesting to the opportunistic behaviour of the Xanthomonas strains on immune compromised plants. The use of gnotobiotic plant experiments with a synthetic bacterial community of more than 100 commensal strains and drop-in of Xanthomonas wildtype or T2SSmutant strains revealed that T2SS-dependent virulence is required for plant disease and for the shift in microbiota composition. Overall, our data indicate that an immune compromised plant can enrich for an opportunistic pathogen that drives a community shift, here caused by tissue damage in leaves, creating an environment in which specific commensal bacteria can thrive.