Microbial communities in soil provide a wide range of ecosystem services. On the small scale, nutrient rich hotspots in soil developed from the activities of animals or plants are important drivers for the composition of microbial communities and their functional patterns. However, in subsoil, the spatial heterogeneity of microbes with differing lifestyles has been rarely considered so far. In this study, the phylogenetic composition of the bacterial and archaeal microbiome based on 16S rRNA gene pyrosequencing was investigated in the soil compartments bulk soil, drilosphere, and rhizosphere in top- and in the subsoil of an agricultural field. With co-occurrence network analysis, the spatial separation of typically oligotrophic and copiotrophic microbes was assessed. Four bacterial clusters were identified and attributed to bulk topsoil, bulk subsoil, drilosphere, and rhizosphere. The bacterial phyla Proteobacteria and Bacteroidetes, representing mostly copiotrophic bacteria, were affiliated mainly to the rhizosphere and drilosphere—both in topsoil and subsoil. Acidobacteria, Actinobacteria, Gemmatimonadetes, Planctomycetes, and Verrucomicrobia, bacterial phyla which harbor many oligotrophic bacteria, were the most abundant groups in bulk subsoil. The bacterial core microbiome in this soil was estimated to cover 7.6% of the bacterial sequencing reads including both oligotrophic and copiotrophic bacteria. In contrast the archaeal core microbiome includes 56% of the overall archaeal diversity. Thus, the spatial variability of nutrient quality and quantity strongly shapes the bacterial community composition and their interaction in subsoil, whereas archaea build a stable backbone of the soil prokaryotes due to their low variability in the different soil compartments.