Multi-omics resolved integration reveals microbial niche separation in soil aggregates

The soil matrix is a heterogeneous mixture composed of aggregates – three dimensional complexes composed of organic materials and mineral particles. Soil aggregates vary considerably in physical and chemical properties by size, making them unique habitats for distinct microbial communities and metabolic pathways. Yet, this microscale spatial variability is often overlooked in studies that use homogenized soil cores. We investigated the microbial taxonomy, functional gene composition, and metabolic products observed in four aggregate size fractions ranging from 8 mm to free particles (below 53 μm) collected from agricultural soils under two different management practices. The functional gene composition differed significantly among aggregate sizes, with higher abundances of genes for the degradation of plant-derived compounds in the macroaggregates and for biomass recycling in the two smallest size fractions. These differences corroborated with significant differences in the composition of the metabolome but not specific enzyme activities. Both taxonomic profiling and reconstruction of genomes from metagenomes revealed a higher abundance of ammonia-oxidizing archaea in the macroaggregates in comparison to other aggregate sizes, and analysis of their genomes revealed complementary metabolisms potentially enabling them to colonize different niches within the same habitat. Together, our results show that soil microbial communities and their functions are shaped by the size of soil aggregates, likely driven by differences in resource availability between macro- and microaggregates.