Grape expectations: disentangling environmental drivers of microbiome establishment in winegrowing ecosystems

Microbial communities play a central role in viticulture, influencing wine characteristics (a concept termed microbial terroir). Yet, the individual factors shaping these microbiomes remain poorly understood. We conducted a multi-year, large-scale survey of Swiss vineyards (95 sites, 680 samples), longitudinally sampling 12 sites (within 2.46 km and identical cultivar and rootstock) over three years. Using 16S rRNA gene and internal transcribed spacer (ITS) amplicon sequencing, untargeted metabolomics (GC-MS, LC-MS/MS), environmental monitoring, and sensory data, we disentangled environmental factors associated with community assembly and fermentation dynamics. Topography and climate collectively structured microbiomes but affected soil- and plant-associated communities differently. Berry-associated fungi showed the strongest site-specific signature, enabling machine-learning predictions of microclimatic variation. Climatic factors and berry chemistry selectively favor fermentative yeasts, which are each linked to distinct metabolite and aroma profiles. Plant stress metabolites were further associated with microbial and metabolite composition. Our integrative approach thereby fundamentally advances our understanding of microbial biogeography and terroir in viticulture.