Persistent legacy effects on soil metagenomes facilitate plant adaptive responses to drought

Both chronic and acute drought alter the composition and physiology of soil microbiomes, with implications for globally important processes including carbon cycling and plant productivity. When water is scarce, selection favors microbes with thicker peptidoglycan cell walls, sporulation ability, and constitutive osmolyte production (Schimel, Balser, and Wallenstein 2007)—but also the ability to degrade complex plant-derived polysaccharides, suggesting that the success of plants and microbes during drought are inextricably linked. However, communities vary enormously in their drought responses and subsequent interactions with plants. Hypothesized causes of this variation in drought resilience include soil texture, soil chemistry, and historical precipitation patterns that shaped the starting communities and their constituent species (Evans, Allison, and Hawkes 2022). Currently, the physiological and molecular mechanisms of microbial drought responses and microbe-dependent plant drought responses in diverse natural soils are largely unknown (de Vries et al. 2023). Here, we identify numerous microbial taxa, genes, and functions that characterize soil microbiomes with legacies of chronic water limitation. Soil microbiota from historically dry climates buffered plants from the negative effects of subsequent acute drought, but only for a wild grass species native to the same region, and not for domesticated maize. In particular, microbiota with a legacy of chronic water limitation altered the expression of a small subset of host genes in crown roots, which mediated the effect of acute drought on transpiration and intrinsic water use efficiency. Our results reveal how long-term exposure to water stress alters soil microbial communities at the metagenomic level, and demonstrate the resulting “legacy effects” on neighboring plants in unprecedented molecular and physiological detail.