Temporal Dynamics of the Sap Microbiome of Grapevine Under High Pierce’s Disease Pressure

Grapevine is a pillar of the California state economy and agricultural identity. This study provides a comprehensive culture-independent microbiome analysis from the sap of grapevine overtime and in a context of a vascular disease. The vascular system plays a key role by transporting nutrient, water and signals throughout the plant. The negative pressure in the xylem conduits, and low oxygen and nutrient content of its sap make it a unique and underexplored microbial environment. We hypothesized that grapevine hosts in its sap, microbes that have a beneficial impact on plant health by protecting against pathogen attack and supporting key biological processes. To address this hypothesis, we chose a vineyard under high Pierce’s disease (PD). PD is caused by the xylem-dwelling pathogenic bacterium Xylella fastidiosa. We selected ten grapevines within this vineyard with a range of disease phenotypes, and monitored them over 2 growing seasons. We sampled each vines at key phenological stages (bloom, veraison, and post-harvest) and used an amplicon metagenomics approach to profile the bacterial (16S -V4) and fungal (ITS) communities of the sap. We identified a core microbiome of the sap composed of seven bacterial (Streptococcus, Micrococcus, Pseudomonas, Bacteroides, Massilia, Acinetobacter and Bacillus) and five fungal (Cladosporium, Mycosphaerella, Alternaria, Aureobasidium, and Filobasidium) taxa that were present throughout the growing season. Overall, the sap microbial makeup collected from canes was more similar to the root microbial profile. Alpha diversity metrics indicated a microbial enrichment at bloom and in vines with moderate PD severity suggesting a host-driven microbial response to environmental cues. Beta diversity metrics demonstrated that disease condition and plant phenology impacted microbial community profiles. Our study identified several potential taxonomic targets with antimicrobial and plant growth promoting capabilities that inhabit the grapevine sap and that should be further tested as potential biological control or biofertilizer agents.