Health or disease – a question of rhizomicrobial ecology? The case of Grapevine Trunk Disease

The incidence of the apoplectic breakdown associated with grapevine trunk diseases (GTDs) is promoted by climate change, which has become a challenge for viticulture worldwide. Outbreak of these conditional diseases is expected to depend on the rhizomicrobiome. However, the impact of the rhizomicrobiome on grapevine resilience has remained poorly understood, particularly with respect to its ecological aspects. This study explores the link between GTDs, the rhizomicrobiome, and soil chemistry in vineyards along the Upper Rhine. Using amplicon sequencing for both fungal and prokaryotic communities, we show that around half of the fungal rhizosphere community is endowed with pathotrophic potential, independently of the health status of the plant, including seventeen taxa known to be associated with GTD, predominantly Black Foot Disease. In contrast to fungi, bacterial diversity is shifted depending on the micronutrients Fe, Cu, Mn, and Zn. Moreover, taxa enriched in the rhizosphere of asymptomatic vines, such as Pseudophialocephala and Collarina for the mycobiome, and Caulobacter, Kitasatospora, and Entotheonellaceae for the bacteriome, may show correlations with soil properties. The most prominent feature associated with disease outbreaks was the drastic changes of microbial co-occurrence networks. These were significantly depleted for the prokaryotes, while they increased the fungal correlation networks, especially for GTDs taxa, such Fomitoporia, Stereum, Phaeomoniella, and Neofusicoccum. Thus, likely microbial interactions and not the mere presence of given taxa explains disease outbreak. This finding opens new strategies for sustainable management of GTDs.