Linking Tree Health, Rhizosphere Physicochemical Properties, and Microbiome in Acute Oak Decline

Forest decline diseases are complex processes driven by biotic and abiotic factors. Although information about host–microbiome–environment interactions in agricultural systems is emerging rapidly, similar studies on tree health are still in their infancy. We used acute oak decline (AOD) as a model system to understand whether the rhizosphere physicochemical properties and microbiome are linked to tree health by studying these two factors in healthy and diseased trees located in three sites in different AOD stages—low, mid and severe. We found significant changes in the rhizosphere properties and microbiome composition across the different AOD sites and between the tree health conditions. Rhizosphere pH correlated with microbiome composition, with the microbial assemblages changing in more acidic soils. At the severe AOD site, the oak trees exhibited the lowest rhizosphere pH and distinct microbiome, regardless of their health condition, whereas, at the low and mid-stage AOD sites, only diseased trees showed lower pH and the microbial composition differed significantly from healthy trees. On these two sites, less extreme soil conditions and a high presence of host-beneficial microbiota were observed in the healthy oak trees. For the first time, this study gathers evidence of associations among tree health conditions, rhizosphere properties and microbiome as well as links aboveground tree decline symptoms to the belowground environment. This provides a baseline of rhizosphere community profiling of UK oak trees and paves the way for these associations to be investigated in other tree species suffering decline disease events.