Microbial emergent ecophysiology affects soil carbon accumulation across land use gradients

Agricultural land use intensification has led to loss of soil carbon; restoring soil carbon through regenerative practices offers an opportunity to help mitigate climate change and promote soil health. The soil microbiome is central in transforming plant materials into persistent forms of soil organic carbon. However, there is a poor mechanistic understanding of how microbiomes function, assemble, interact and collectively influence soil carbon changes across land use gradients. Here we present integration of knowledge across scales from field observations and lab experiments to highlight the importance of microbial ecophysiology and their emergent traits in determining the soil carbon balance in multiple paired local contrasts of low and high land use intensity systems in the UK. Across 11 paired contrasts, we observed significantly higher microbial community-level carbon use efficiency (CUE) and increased biomass in low intensity grassland soils compared with high intensity cropland soils. We suggest that less-intensive management practices have more potential for carbon storage through increased microbial CUE. Using proteomics and extracellular enzyme analysis, we demonstrate that reduced CUE in cropland soils was linked to higher microbial investment in stress alleviation and resource acquisition traits. To examine if grassland microbiomes with higher CUE could be recruited to help accumulate soil carbon in cropland soils, in lab mesocosm we reciprocally transferred microbiomes derived from historically undisturbed grassland soil and neighbouring cropland soil into their sterile counterparts from 2 paired contrasts. We fed the microbiomes with plant litter tea and monitored community assembly over 8 months. We observed that soil conditions were more important than inoculum source in determining bacterial assemblage, inoculum source was more important than soil conditions in determining fungal assemblage, whereas both inoculum source and soil conditions mattered equally in shaping the protist assemblage. This highlights the differential response of bacteria, fungi and protists to environmental filtering and raises questions around the persistence and therefore efficacy of microbial inoculations. In terms of soil carbon accumulation, we observed that a grassland microbiome led to positive outcomes in terms of soil carbon changes in cropland soil after 8 months suggesting that the microbial emergent ecophysiology that arises from both initial inoculum as well as the soil conditions matter in determining soil carbon accumulation. Our research highlights the need for careful land management to create the right soil conditions for the promotion of beneficial microbiomes with efficient metabolism for carbon accumulation. This will aid in regenerating degraded soils for sustainable climate-smart agriculture.