Microbial community succession and dynamics during the season-long development of apple fruit (Malus × domestica)

Microorganisms colonize every external and internal surface of plants, including fruits. Relatively little is known about the fruit microbiome and its role in disease resistance and fruit quality during fruit development and storage. The fruit tissue, the carposphere, is a carbohydrate-rich habitat. Amplicon sequencing of fungal and bacterial communities identified distinct microbial community composition and diversity across tissue types such as the exocarp and mesocarp. We determined microbial richness was highest during bloom and in mature fruits. Endophytic microbes were shared across many fruit development stages, while epiphytic microbes were transient. However, we identified a pattern of succession with increasing diversity of the epiphytic microbiota across the growing season. Notably, we also show that fungal and bacterial taxa with carbohydrate-degrading potential have different abundance patterns across apple developmental stages, which could indicate that host plants have distinct regulation for microbial subgroups or that microbes interact with different elements of host regulatory mechanisms. The identification of a stable microbiota associated with tree fruit, and understanding how those microbes establish and function, will provide fundamental insights regarding the engineering of a consortium of microbes that could thrive under storage and possibly reduce food waste.IMPORTANCEPlant-associated microbes are not well-characterized in specialty crop systems. We describe the fungal and bacterial microbial communities colonizing the surface and interior of apple flowers and fruits over the course of one growing season. This work provides a foundational understanding of microbes present, how the populations change over time, and provides insight into the origins of endophytic microbes. These findings will be used in future apple disease-related research, particularly on the development of organic or biologically based pesticides.