How agricultural legacy shapes the drought response of the wheat rhizobiome

Background Drought is an increasing threat to soil microbiomes, which underpin critical soil functions and crop production. While drought-induced shifts in soil microbial diversity are well documented, the impact on the functional potential of microbiomes remains poorly understood. It is particularly unclear whether alternative cropping systems, such as organic farming, enhance the microbial ability to cope with drought compared to conventional systems. To fill this gap, we imposed a field-scale drought in a long-term trial comparing organic and conventional systems since 1978. We assessed the functional potential of the wheat rhizosphere microbiome using shotgun metagenomics. Results The legacy of cropping systems was the primary driver of the rhizosphere's functional potential, which persisted under drought. While the extent of the functional shift in response to drought was similar across all systems, the drought-affected communities remained functionally unique. All systems were enriched with gene functions common for drought adaptation, such as cell membrane modification, sporulation, osmolyte accumulation, antioxidant production, and DNA repair. However, we observed a decrease in gene functions associated with ribosomal hibernation (dormancy) and exopolysaccharide production under drought, suggesting a plant-mediated response where microbes benefit from root exudates for protection and to remain active. Metabolically, communities shifted towards increased efficiency and an enrichment of gene functions involved in scavenging phosphorus and iron, whereas the potential for complex organic matter degradation was reduced. Although they share a common set of survival gene functions, the cropping systems exhibited nuanced strategies, highlighted by an increase in sporulation-related gene functions in conventional systems receiving synthetic fertilizers and pesticides, and programmed-cell-death-associated gene functions in manure-fertilized systems. Conclusion Our findings reveal that agricultural management plays a dual role, profoundly shaping the functional potential of the soil microbiome while having a limited influence on the genetic tools for drought adaptation. We conclude that the plant is a critical actor in orchestrating the rhizosphere's drought response, leading to unique adaptations compared to bulk soil. Ultimately, no system conferred superior functional resistance to drought. The intrinsic resistance of the microbial gene pool appears to be more strongly affected by the plant-microbe interactions than the legacy effects of agricultural management.