Land use effects on soil microbiome composition and traits with consequences for its ecosystem carbon use efficiency

Abstract

The soil microbiome determines the fate of belowground inputs of plant fixed carbon. The shifts in soil properties caused by changes in land use leads to modifications in microbiome structure and function, resulting in either loss or gain of soil organic carbon (SOC). Soil pH is the primary factor regulating microbiome characteristics leading to distinct pathways of microbial carbon cycling, but the underlying mechanisms remain understudied. Here, the taxa-trait relationships behind the variable fate of SOC were investigated across two temperate paired land use intensity contrasts with differing soil pH using metaproteomics, metabarcoding and a 13C labelled litter decomposition experiment. 13C incorporation into microbial biomass increased with land use intensification in low pH soils but decreased in high pH soils, impacting ecosystem carbon use efficiency (CUE) in opposing directions. Reduction in biosynthesis traits across land use intensity contrasts was due to increased abundance of proteins linked to resource acquisition and stress tolerance. These community-level trait trade-offs were underpinned by land use intensification-induced changes in dominant taxa with distinct traits. These trait changes alter the balance of decomposition and stabilisation of carbon in soil through divergent pH-controlled pathways. In low pH soils, land use intensification alleviates microbial abiotic stress resulting in increased CUE but promotes decomposition and SOC loss. In contrast, in high pH soils, land use intensification increases microbial physiological constraints and decreases CUE, leading to reduced necromass build-up and SOC stabilisation. We demonstrate how microbial CUE can be decoupled from SOC highlighting the need for its careful consideration in predicting or managing SOC storage for soil health and climate change mitigation.