Dysbiosis of a leaf microbiome is caused by enzyme secretion of opportunisticXanthomonasstrains

Abstract

AbstractDysbiosis 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. InArabidopsis thaliana, the absence of NADPH oxidase RBOHD can lead to an altered leaf microbiota, including an enrichment of opportunisticXanthomonaspathogens. It is currently unclear whether the microbiota change occurs independently of the opportunistic pathogens or is caused by the latter, and which virulence factors ofXanthomonasare essential for its opportunistic lifestyle. Here, we found that the opportunisticXanthomonasstrains secrete a cocktail of cell wall degrading enzymes via the type-2 secretion system (T2SS) that degrade leaf tissue and promoteXanthomonasgrowth during plant infection. Both disease severity and leaf degradation activity were increased inrbohDcompared to Col-0 plants, attesting to the opportunistic behaviour of theXanthomonasstrains on immune compromised plants. Using gnotobiotic plant experiments with a synthetic bacterial community of more than 100 commensal strains and drop-in ofXanthomonaswildtype or mutant strains revealed that T2SS-dependent virulence is required for plant disease and for the shift in microbiota composition. Overall, our data indicate that a single opportunistic pathogen can drive community shifts, here caused by tissue damage in leaves, creating an environment in which specific commensal bacteria can thrive.