Functional consequences of land-use history: Plant community and soil microbiome mediation of nutrient loss, soil aggregate stability, and soil erosion

Alterations in land-use practices pose serious threats to biodiversity and ecosystem functioning, affecting ecosystem services such as soil stability and nutrient cycling. Conversely, the collective interactions between plants, soils, and associated soil microbiomes play a critical role in the maintenance of various ecosystem services. We found evidence of the degradation of soil microbiomes with land-use, as microbial composition, measured by amplicon sequencing targeting bacteria (16S), fungi (ITS), and AM fungi (LSU), differed between unplowed prairies, post-agricultural grasslands, and annual agricultural fields across Kansas (p = 0.003, 0.001, and 0.01, respectively). We then tested functional impacts on soil ecosystem services of the soil microbiome differences by conducting a greenhouse experiment that manipulated full-factorial combinations of soil microbiome composition of land-use history and plant assemblage. Specifically, we examined soil detachment, water-stable macroaggregates, and nitrate leaching through the soil profile, as well as plant and AM fungal biomass. Soil microbiomes, plant composition, and their interactions had strong influences on every metric of ecosystem function. Notably, native plant communities were more sensitive to degradation of the microbiome. Furthermore, living soil microbiomes, regardless of land-use history, reduced soil detachment, promoted formation of water-stable macroaggregates, and facilitated greater nitrate retention, highlighting the importance of soil microbiomes for many physical and biogeochemical processes. Moreover, the realized functional benefits of microbiome composition depended on the plant community. These results highlight the complexities of plant-soil-microbial interactions in the context of land-use histories, displaying the importance of intact microbiomes, especially AM fungi, in mitigating environmental consequences of agricultural intensification.