How agricultural legacy shapes the drought response of the wheat rhizobiome

Abstract 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 ability of microbes to maintain their functionality under drought compared to conventional systems. To fill this gap, we imposed a field-scale drought in a 44-year long-term trial comparing organic and conventional systems, and assessed the functional potential of the wheat rhizosphere microbiome using shotgun metagenomics. Results Agricultural management legacy was the primary driver of the rhizosphere functional gene composition, accounting for 24–32% of total variation across ontologies and persisting under drought (which explained 3–6% of variation). While the magnitude of the drought-induced shift in the functional potential was similar across all systems, drought-stressed communities remained distinct. All systems enriched metagenomic toolkits for core drought endurance, including cell membrane modification, endospore formation, osmolyte accumulation, antioxidant production, and DNA repair. Conversely, we observed a relative depletion of genes associated with ribosomal hibernation (dormancy) and exopolysaccharide synthesis under drought, suggesting a reliance on plant root exudates over endogenous genomic investment. In terms of the metabolic potential, communities exhibited an enriched capacity for inorganic phosphorus and iron scavenging alongside a relative depletion of genes involved in complex organic matter degradation. Although communities across all systems shared a common set of functional genes associated with stress survival and metabolic adaptation, they exhibited nuanced system-specific metagenomic strategies, marked by an enrichment of sporulation-related genes in conventional systems receiving synthetic inputs and programmed-cell-death pathways 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 exerting limited influence on the core metagenomic toolkit for drought adaptation, with only subtle nuances between systems. Rather than driving broad system-specific shifts, drought stress consistently enriched metagenomic toolkits associated with osmotic stress tolerance, cellular maintenance, and nutrient scavenging across all management regimes. Ultimately, no cropping system conferred superior metagenomic resistance to drought, yet each system preserved its distinct metagenomic identity under severe water deficit, highlighting the enduring legacy of agricultural management.