Chernozems are counted among the most fertile soils worldwide. Unexpectedly high spore density and species richness of arbuscular mycorrhizal fungi (AMF) were found in a long-term field trial established on such a soil. The purpose of the present study was to estimate bacterial communities associated within spores of selected AMF species from a long-term field trial on a highly fertile Calcic Chernozem to unravel their diversity belonging to different genera and species. We hypothized that high AMF species richness found in the Chernozem soil is reflected in a bacterial diversity with multifunctional traits mediated by indigenous bacterial compositions. The AMF species Funneliformis mosseae, Scutellospora calospora and Septoglomus nigrum were selected, since they occurred abundantly both in reduced and conventional tillage systems. The pure cultures of isolated bacterial strains were tested for ecological functions (traits) such as phosphorus solubilization, siderophore production, indole-3-acetic acid production and 1-aminocyclopropane-1-carboxylate deaminase activity. In addition, antimicrobial activity against both hemibiotrophic and necrotrophic fungi and oomycetes was evaluated. The majority of bacterial strains was exclusively associated with only one of the three AMF species, thus, giving evidence that each AMF species may harbor its own bacterial community. A large number of bacterial communities was shown to exert multifunctional activities ranging from plant growth promotion traits to antimicrobial activity. These findings suggest that the multifunctionality of bacteria intimately associated with AMF could markedly expand the ecological function of an autochthonous AMF population and empower host plants to explore robust ways to cope with changing environmental conditions.