AM fungi are crucial for enhancing productivity of many land plants. This study aimed to uncover the role of bacteria colonising AM fungi in sulfonate and sulfate ester mobilisation, the dominant organo-S pools in soil unavailable directly to plants. The effect of an intact AM symbiosis with access to stable isotope organo-34S enriched soils encased in 35 µm mesh cores was tested in microcosms with A. stolonifera and P. lanceolata. At 3 month intervals, the plant shoots were analysed for 34S uptake. After 9 months, hyphae and associated soil was picked from static (mycorrhizal) and rotating (severed hyphae) cores and corresponding rhizosphere soil was sampled for bacterial analysis. An intact AM symbiosis increased uptake of 34S from organo-34S enriched soil at early stages of growth when S demand is high. The static (mycorrhizal) treatments were shown to harbour larger populations of cultivable heterotrophs and sulfonate mobilising bacteria. Microbial communities were significantly different in the hyphosphere and rhizosphere of mycorrhizal and severed hyphae treatments. Sulfate ester (arylsulfatase enzyme assay, atsA gene) and sulfonate mobilising activity (asfA gene) was altered by an intact AM symbiotic partnership which stimulated Azospirillum, Burkholderia and Polaromonas species. NGS revealed that AM symbiosis led to familial population shifts, reduced diversity and dominance of the Planctomycetes and Proteobacteria. The observed AM induced modifications to microbial communities involved in sulfate ester and sulfonate mobilisation provide a mechanism for the observed increased 34S-uptake in the static mycorrhizal treatments.