Drought and rewetting drive divergent microbial dynamics across soil compartments and reveal Trinickia as a key genus for soybean drought resilience

Abstract

Drought conditions are projected to intensify under climate change, and engineering more resilient plant microbiomes is a promising route to supporting crop productivity. However, effectively harnessing these microbiomes depends on identifying keystone taxa and functional traits that promote plant drought tolerance. Here, we combine deep shotgun metagenomics with absolute-abundance calibration to track genome-resolved microbial dynamics across a prolonged soybean drought and rewetting cycle. Leveraging 728 high-purity metagenome-assembled genomes that capture ~83% of prokaryotic reads on average, we show that drought drives significantly greater change in community structure in the rhizosphere than in bulk soil. This was accompanied by declining taxonomic, yet rising functional diversity. While rhizosphere communities rapidly recovered within 24 hours of rewetting, bulk soil communities instead underwent a progressive post-rewetting disturbance, consistent with a Birch-effect-driven successional shift. Rhizosphere drought enrichment was dominated by a single, taxonomically underexplored genus, Trinickia, whose genomes encode a coordinated suite of osmotic-stress-tolerance, bio-fertilisation, and phytohormone/polyamine biosynthesis traits consistent with plant growth promotion. Supporting this genomic inference, Trinickia abundance strongly correlated with increased root biomass during active drought, independent of plant developmental stage. Together, these findings identify the rhizosphere as a dynamically responsive compartment during drought and rewetting, and highlight Trinickia species as genomically and phenotypically supported candidates for microbiome-based strategies to improve soybean drought resilience.