This study aimed to elucidate the role of bacteria colonising mycorrhizal hyphae in organically bound sulfur mobilisation, the dominant soil sulfur source that is not directly plant available. The effect of an intact mycorrhizal symbiosis with access to stable isotope organo-34S enriched soils encased in 35 µm mesh cores was tested in microcosms with Agrostis stolonifera and Plantago lanceolata. Hyphae and associated soil were sampled from static mesh cores with mycorrhizal ingrowth and rotating mesh cores that exclude mycorrhizal ingrowth as well as corresponding rhizosphere soil, while plant shoots were analysed for 34S uptake. Static cores increased uptake of 34S at early stages of plant growth when sulfur demand appeared to be high and harboured significantly larger populations of sulfonate mobilising bacteria. Bacterial and fungal communities were significantly different in the hyphospheres of static cores when compared to rotating cores, not associated with plant hosts. Shifts in bacterial and fungal communities occurred not only in rotated cores but also in the rhizosphere. Arylsulfatase activity was significantly higher in the rhizosphere when cores stayed static, while atsA and asfA gene diversity was distinct in the microcosms with static and rotating cores. This study demonstrated that AM symbioses can promote organo-S mobilization and plant uptake through interactions with hyphospheric bacteria, enabling AM fungal ingrowth into static cores creating a positive feedback-loop, detectable in the microbial rhizosphere communities.