PNNL

Abstract

At the interface of plant-soil-microbe interactions lies the rhizosphere, a narrow zone surrounding roots rich in metabolic activity and nutrient cycling. As climate warming and its accompanying water scarcity increases in both frequency and duration, it is unknown how plant-mediated processes such as root exudation will alter and influence soil organic matter composition in the rhizosphere. Here we integrated 16S rRNA gene amplicon sequencing for microbial community analysis, high-resolution organic matter measurements for meta-metabolome characterization, and position-specific 13C-pyruvate labeling to track carbon allocation pathways to fully characterize how microbes and species-specific plant roots influence rhizosphere soil organic carbon turnover. In situ metabolic and microbial rhizosphere profiles of three plant species, Piper auritum, Hibiscus rosa sinensis, and Clitoria fairchildiana revealed drastically different drought-response mechanisms, enhancing our understanding of niche rhizosphere dynamics. Overall, drought conditions intensified the exclusion of phylogenetically distant microbes, sufficiently conserved microbial functional traits, and decreased microbial heterogeneity across roots of all plant species. Yet, individual host rhizosphere profiles responded differently; P. auritum decreased root exudation into the rhizosphere indicating a decreased dependence on surrounding microbes. Meanwhile, H. rosa sinensis and C. fairchildiana responded aptly to water stress through modulating their exudate metabolic composition and, therefore, rhizosphere microbial communities. Our results revealed how plant species-specific microbial interactions systematically progressed with the root metabolome; as roots responded to drought, their associated microbial communities adapted, potentially supplementing drought tolerance strategies for plant roots. These findings have significant implications for maintaining plant health during drought stress and improving plant performance for climate change mitigation in both natural systems and agriculture.