Drought legacy effects on plant growth and plant–soil feedback are mediated by soil microbial communities independently of root exudates and root litter

Abstract

Extreme droughts alter vegetation dynamics worldwide and the effects often persist after the drought ended. Indirect drought effects mediated by the soil microbial community can continue to affect plant growth during drought recovery and may impact plant–soil feedback (PSF), the effect a species has on its own growth via its rhizosphere microbiome. Changes in plant inputs to the soil, such as root exudates and litter, may drive these drought legacy effects through changes in soil bacterial and fungal communities. In a three‐stage greenhouse experiment, we assessed drought legacy effects on plant biomass and PSF of three common grassland species. In a first conditioning phase, soil was conditioned directly by plants under drought and ambient conditions. In a second conditioning phase, soil was conditioned by the addition of either conditioned soil inoculum or root exudates or root litter produced in the first phase by droughted or non‐droughted plants. In the feedback phase, a new set of plants was grown in soil conditioned by the same species compared to soil conditioned by another species across all soil conditioning types and their biomass linked to soil microbial community data. We found that only soil conditioning with plants, but not inoculum, exudates or litter, resulted in a consistent negative drought legacy effect on plant growth, which was linked to lower microbial biomass and shifts in bacterial and fungal community composition. We could identify a set of fungal and bacterial taxa which were differentially abundant in drought and well‐watered soil and accurately predicted plant growth. PSF in plant‐conditioned soil differed between species, but was only affected by drought in Rumex acetosa. This pattern was not reproduced through the addition of inoculum, root exudates or root litter. Synthesis. Our results show that drought indirectly restricts plant growth, which is not mediated by root exudates or root litter, but through altering microbial biomass and community composition. These findings suggest that plant recovery from extreme drought is obstructed by persistent changes in soil microbial communities.