Spatial heterogeneity and microbial terroir: balancing dispersal limitation and cultivar as drivers of microbial diversity in viticulture

Abstract The microbial communities inhabiting grapevines and wines exhibit spatiotemporal patterns linked to region, climate, and cultivar. However, the degree of spatial heterogeneity within and between vineyards and its relationship to cultivar-associated biodiversity selection has not been studied previously. We combined high-density sampling of grapevine microbiota (N = 230) with spatial modeling and satellite imagery in two experiments: (i) two monoclonal Chardonnay vineyards to examine spatial heterogeneity in a genetically homogenous population; and (ii) three old-vine vineyards interplanted with mixed cultivars to investigate the relative effects of spatial distance and cultivar on the microbiota. Contrary to expectations based on monoclonal vineyards, cultivar effects were not apparent in mixed-cultivar vineyards. Instead, we demonstrate extensive spatial variation in the bacterial and fungal communities inhabiting individual grapevines and vineyards, and that community similarity is correlated with spatial distance within and between vineyards. This suggests that dispersal limitation may play an important role in shaping grapevine microbiota, as well as cumulative diversity within the vineyard ecosystem (gamma diversity), with implications for both plant health and wine quality. Spatial models may identify abnormalities in microbial communities, such as contaminant sources within vineyards, and future studies examining microbiota in agricultural settings should account for spatial variation within the study design, e.g., by sufficiently dense spatial sampling or collection of aggregate samples (e.g., grape musts) to avoid undersampling bias. Overall, this study adds to the complicated story of microbial biogeography associated with winegrowing and wine quality (microbial terroir), highlighting the roles of dispersal and potential microclimate effects in agricultural settings.