Distinct Microbial Life History Strategies Across Soil Depth Profiles: Metagenome Analysis of a Long-Term Temperate Agricultural Field Experiment

Microorganisms play essential roles in soils as they mediate a range of soil processes, including nutrient cycling. Yet, research has predominantly focused on topsoil, overlooking the crucial contributions of subsoil microbial communities to agroecosystem functioning via nutrient cycling, carbon sequestration, water filtration, and pollutant degradation. This study investigates how distinct cropping systems influence the taxonomic and functional profile of soil microbiomes across a 0-90 cm depth gradient in the 42-year-old DOK long-term field experiment in Switzerland. Independent from cropping system, there were profound differences along the depth profile in soil organic carbon stocks, microbial biomass, extracellular enzymatic activities, and community composition, with subsoil bacterial communities showing greater homogeneity than fungal communities. Community composition analysis revealed that the surface layer (0-5 cm) harbored distinct microbial assemblages compared to all other soil depths. Bacterial metagenomic analysis revealed the soil system to be divided into two distinctively functioning compartments separated at the plowing boundary (ca. 25 cm depth): a dynamic topsoil directly influenced by agricultural practices and a more isolated subsoil environment. Furthermore, the functional genetic potential indicated depth-specific life history strategies with topsoils harboring dual characteristics: enriched primary metabolism genes supporting copiotrophic traits (e.g., rapid growth, cell division) alongside oligotrophic environmental response mechanisms (e.g., transcription regulation, stress response, motility). Conversely, subsoil communities showed specialized oligotrophic strategies including enhanced nutrient acquisition, complex transport systems, and extensive repair mechanisms prioritizing component recycling over replacement. While cropping systems significantly influenced topsoil microbial communities with farmyard manure application as the primary driver, subsoil communities remained largely management-independent, except fungal communities which showed responses down to 70 cm. This study provides novel insights into how soil depth and cropping systems shape microbial life history strategies throughout the soil profile and expands our understanding of how microbial communities adapt their genetic potential to different levels of nutrient availability along the soil depth profile.