A tale from 30 French vineyards: how shifts in bacterial and fungal species shape microbial communities from vine to wine and impact fresh mushroom aroma off-odors

Abstract

Grape berry quality is highly influenced by the pedoclimatic conditions in vineyards and specific microbial communities colonizing the berry surface during ripening. Yet, microbial community shifts from vine to wine have not been fully explored, especially mycobiota. Fungi are well-known producers of volatile organic compounds (VOCs) that may impact wine quality. Some fungi as well as their interactions may contribute to wine defects such as fresh mushroom aroma (FMA). To decipher the microbial succession from vine to wine, we monitored bacterial and fungal communities in 30 vineyards at five different stages from vine to wine during three successive years (2021-2023). Climatic conditions, vine data and growing practices were recorded. The cultural and metabarcoding data generated were compared with sensorial analyses of still wines resulting from 30 grape must micro-vinifications to determine to what extent fungal composition and microbial interactions led to the FMA defect in wines. We observed distinct shifts in microbial communities, mainly influenced by climatic data and berry ripening stage. In the early stages, yeasts dominated followed by a progressive increase in mold diversity. Climatic conditions not only shaped mycobiota but also played a crucial role in FMA detection in wines. Wines exhibiting FMA off odors were linked to vineyards with higher precipitation and lower temperatures during the 2021 and 2023 growing seasons. FMA was primarily linked to higher fungal counts and Penicillium species, especially Penicillium crocicola among the fifteen Penicillium species identified. On Meunier or Pinot noir grapes, Botrytis cinerea co-inoculated with Penicillium bialowiezense or Penicillium citreonigrum also led to detectable FMA off-odors and an increase in known FMA markers. Untargeted head space GC-MS identified known FMA-associated VOCs (8 carbon VOCs) but also unidentified VOCs suggesting the FMA defect is most likely linked to combinations of multiple fungal derived compounds. Overall, our results advance the understanding of how microbial communities evolve from vine to wine. We showed how specific individual and co-cultured grape-associated fungi thrived on berries and induced FMA off odors. This research provides the groundwork to put in place better vineyard and wine management practices including the possible use of the identified repressive species to control fungal populations on berries.