Rapid assembly and functional differentiation of the soil surface microbiome in temperate agricultural soil

Biological soil crusts (BSCs) are formed by phototrophic organisms at the soil surface and play a key role in structuring microbial communities and biogeochemical processes in dryland ecosystems. Similar surface associated communities occur in temperate agricultural soils, but their development, assembly dynamics and functional significance remain poorly understood. We investigated the temporal development of the soil surface microbiome following tillage and during subsequent growth of a winter wheat crop, integrating multi-kingdom amplicon sequencing with metagenomic analysis to track phototrophic, bacterial, fungal and protist communities, together with co-amplified macroscopic phototrophs. Distinct surface communities of phototrophs, bacteria and protists established rapidly, within 4 weeks of tillage, and underwent marked succession from early dominance by yellow-green algae (Xanthophyceae) to cyanobacteria, charophytes and ultimately mosses. Across all taxonomic groups, community assembly at the soil surface increasingly shifted towards dispersal limitation over time, whereas bulk soil communities were predominantly shaped by ecological drift. By the end of the growing season, the soil surface had developed a functional profile distinct from bulk soil, characterised by a greater representation of photosynthetic processes, largely due to eukaryotic algal carbon fixation, alongside increased genetic potential for heterotrophic carbon, nitrogen, phosphorus and sulphur cycling. These functional shifts were associated with enrichment of Actinobacteria, Bacteroidetes and Proteobacteria. Our results demonstrate that the soil surface of temperate agricultural systems represents a dynamic and functionally differentiated microbial habitat, which shares key biological features with dryland BSCs while exhibiting distinct functional and successional trajectories, revealing an overlooked component of managed temperate ecosystems • Soil surface communities establish rapidly in temperate agricultural soil • Dispersal limitation structures surface communities, while drift dominates in bulk soil • Surface soils show a distinct functional signature from phototrophs and heterotrophs