Provenance legacies override species effects in shaping oak rhizosphere microbiomes and metabolomes

As climate change drives more frequent drought-heat extremes, selecting drought-tolerant trees is crucial for future forest resilience. However, the role of tree-microbial associations remains largely unclear. We investigated how geographic origin, species identity, and intrinsic water use efficiency (iWUE) shape the rhizosphere microbiome and root-rhizosphere metabolome of Quercus robur L. and Q. petraea (Matt.) Liebl. In a 6-yr common garden experiment, we analyzed trees from two distinct geographic origins (upper Rhine basin and north German lowland) using 16S/ITS metabarcoding and untargeted metabolomics. We found a consistent legacy effect of seed origin on the prokaryotic rhizosphere microbiome and metabolome, whereas tree species had no significant impact. The bacterial family Pseudonocardiaceae was enriched for trees from the drier origin (NGL), while Blastocatellaceae and Micromonosporaceae were associated with iWUE. Higher iWUE also correlated with lower prokaryotic diversity. Ellagic acid, a polyphenol associated with drought tolerance, was enriched in the drier origin. The rhizosphere fungal community, however, was largely unaffected by origin or species. Our findings suggest that ecotypic adaptation linked to origin can outweigh species-level traits in shaping the oak rhizosphere. These findings emphasize that provenance-driven adaptation influences plant-microbe interactions and underscore the need for provenance-aware selection to strengthen forest drought resilience.