Soil microenvironment and microbial community composition jointly regulate carbon accrual in agricultural soils

Abstract

Much of the persistent soil organic carbon (SOC) pool is microbial in origin: microorganisms process plant carbon into biomass and their necromass can associate with mineral surfaces, contributing to long-term carbon persistence. This has generated interest in microbial interventions such as inoculation to restore carbon in degraded croplands, yet their efficacy remains uncertain. The uncertainty reflects a more fundamental, unresolved question: are microbially-mediated carbon transformations governed principally by the composition of the microbial community or by the soil microenvironment? To disentangle these drivers, we conducted a reciprocal microbial community transplant experiment, introducing communities of contrasting origin from locally adjacent grassland and cropland soils into sterilised grassland and cropland soils, and incubating them for eight months with regular organic inputs. This design decouples the inoculum from the microenvironment, allowing their individual and interactive contributions to be quantified. Fungal assembly was influenced more by the inoculum, consistent with dispersal limitation, whereas bacterial assembly was governed more by the microenvironment, consistent with environmental selection. Despite receiving the same organic carbon inputs, grassland and cropland recipient soils showed distinct SOC trajectories, indicating that the soil microenvironment strongly constrained net carbon retention. Within this constraint, community composition also mattered: introducing grassland rather than cropland communities increased fungal diversity and fungal necromass and led to better SOC outcomes, expressed as net gain or reduced loss. These results show that SOC accrual emerges from interactions between the soil microenvironment and microbial community composition, with fungal community assembly particularly associated with necromass accumulation and carbon retention. They highlight the need to consider both soil conditions and microbial community composition when developing strategies to enhance SOC accrual. Significance Statement Restoring carbon in degraded agricultural soils offers an opportunity to mitigate climate change while improving soil health and supporting food security. Because much of the persistent soil carbon pool is microbial in origin, there is growing interest in using microbial interventions to enhance carbon retention in degraded farmland. Yet it remains unclear whether soil carbon outcomes are governed more by which microbes are present or by the soil conditions in which they operate. Using a reciprocal transplant experiment that exchanged microbial communities between grassland and cropland soils, we show that soil conditions strongly constrain carbon retention, while community composition—particularly the diversity of fungi—modulates the outcome within that constraint. Preserving and rebuilding soil carbon will therefore require consideration of both soil conditions and its microbial community.