Rapid Assembly and Functional Differentiation of the Soil Surface Microbiome in Temperate Agricultural soil

Abstract

The surface of dryland soils is typically covered by biological soil crusts (BSC) dominated by cyanobacteria, lichens or moss which contribute key ecosystem functions. However, while photosynthetic biota have been observed on the surface of temperate agricultural soils, understanding of the development, biodiversity and functional significance of these communities is extremely limited. We investigated the temporal development of the soil surface community following tillage and during subsequent growth of a wheat crop. Amplicon analysis showed that establishment of the soil surface microbiome was rapid over the winter period, with distinct communities of phototrophs, bacteria and protists detected 60 days after tillage. There was rapid succession with yellow-green algae (Xanthophyceae) dominating early stages of development, followed by Cyanobacteria and Charophytes and finally moss. Temporal dynamics of fungal and protist communities was influenced by eDNA deposition from plant pathogens inhabiting the crop canopy and wild animal parasites. For all groups, assembly processes in the surface soil became increasingly dominated by dispersal limitation over time while assembly of bulk soil communities became predominantly influenced by drift. Metagenome analysis showed that the soil surface had developed a distinct functional profile relative to bulk soil after 9 months, enriched in photosynthetic processes which were largely from eukaryotic algae rather than cyanobacteria. Additionally the 3-Hydroxypropionate bicycle and reductive TCA carbon fixation pathways were enriched in surface soil. The abundance of genes involved in heterotrophic carbon, nitrogen, phosphorus and sulphur cycling processes were also enriched in surface soil. This included reads of carbohydrate active enzymes, nitrification, denitrification and sulphate reduction genes, largely attributed to the enrichment of Actinobacteria, Bacteroidetes and Proteobacteria in the soil surface. Overall, we show overlap in dominant phototrophic taxa between temperate agricultural and BSC in arid soils, but with notable differences, including abundance of Xanthphycae and Charophytes. Furthermore, the functional signatures of the soil surface communities indicate that they may play an important role in the delivery of ecosystem functions in temperate agricultural systems.