Highlighting the complexity of pathogenesis: the host microbiota impacts disease development on apple fruit and is a cornerstone for its biocontrol

Apple fruit is the most produced temperate fruit with a trade value estimated at 7.5 billion $ and is usually stored up to one year after harvest. Postharvest pathogens often compromise storage, responsible for up to 55% of fruit losses, depending on the country and fruit. They are also a source of mycotoxin contamination. A sustainable way to control that pathogen is using beneficial microorganisms called biocontrol agents (BCA). Despite promising efficacy in laboratory conditions, BCAs efficacy is variable and often reduced once applied at a large scale through either orchard or postharvest treatment. We hypothesized that the epiphytic microbiota plays a role in the variability of BCA efficiency (Pichia anomala, strain K) and postharvest disease development due to Botrytis cinerea on apples. A diverse set of 18 epiphytic microbial communities were harvested from apple carposphere and bio-banked. The analysis of their bacterial and fungal taxonomic composition and carbon metabolic footprint confirmed that contrasted microbiotas were harvested. Their impact on B. cinerea disease development was evaluated through a standardized in vivo bioassay. The reduction of B. cinerea rot development ranged from 20% to 80% when the microbiotas were applied alone. In addition, three microbiotas enhanced the biological control efficiency of strain K (up to +100%, whatever the tested microbiota concentrations) while others limited its action (down to -27%). A co-clustering analysis of biocontrol efficacy with carbon profiles or taxonomic composition was carried out. It identified promising molecules whose high metabolization was associated with high biocontrol by the microbiota and taxa with higher abundance in microbiota limiting B. cinerea rot development. Putative beneficial taxa were isolated from the most efficient microbiota. In vivo bioassays confirmed the efficacy of two molecules and two strains belonging to species never mentioned for their biocontrol properties against plant disease. This study demonstrated that natural epiphytic microbiota significantly influences postharvest disease development in apples and cause a variability in biocontrol efficacy. By mining the generated data, our approach identified promising molecules and taxa that enhance biocontrol, offering new insights for sustainable postharvest pathogen management.