Continental-scale drivers of soil microbial extracellular polymeric substances

Extracellular polymeric substances (EPS) are a vital component of microbial residues which contribute to soil organic carbon (SOC). However, despite various conjectures and hypotheses regarding soil EPS controls, empirical research and experimental evidence to validate these theories have remained highly limited. In this study, we addressed this knowledge gap by conducting extensive soil sampling across Europe, encompassing diverse climates and bedrock and land use types, to systematically investigate soil EPS contents and large-scale controls. We found that bedrock and land use significantly influenced the soil EPS concentration, the contribution of EPS-carbon (C) to SOC, as well as the microbial EPS production efficiency. The average soil EPS concentration was 956 ± 55 µg g⁻¹ soil (n = 92 sites), with EPS-C contributing on average 1.6 ± 0.1% to SOC. Soil EPS concentrations were significantly higher on carbonate bedrock than on silicate and sedimentary geologies. In terms of land use, grassland soils had significantly higher EPS concentrations compared to cropland soils but did not differ from woodland soils. Further detailed investigations of proximate soil physicochemical drivers of EPS content across the transect showed slightly different drivers for EPS polysaccharides and EPS proteins. For instance, EPS polysaccharides were affected by bedrock but not by land use, while the pattern was inverse for EPS proteins. Microbial EPS production efficiency, which expresses the EPS-C content per microbial biomass C, was significantly negatively correlated with microbial carbon use efficiency, reflecting the trade-off between C allocation for growth and extracellular production. EPS production efficiency increased under harsh environmental conditions (e.g., low soil moisture content, high drought index), but was unaffected by pH extremes. On a large scale, soil EPS accumulation was promoted by its production efficiency and by soil factors promoting the sorption and stabilization of EPS, such as clay content, exchangeable Ca and Fe oxides. These findings underscore the significant yet overlooked role of EPS as a critical component of the soil-stable C pool, as it influences microbial C allocation and SOC stabilization and should be further studied to better understand soil C cycling.