Hydrothermal plumes are highly diluted fluids which introduce reduced chemical species up to thousands of kilometres away from the source into the deep sea. Despite their considerable spatial scale and the impact they have on the ocean biogeochemical cycles, plume-based studies are scarce. Here we analysed the plume microbial ecology of a deep-sea and a mesopelagic volcano, Brothers and Macauley, on the Kermadec intra-oceanic Arc (South Pacific Ocean). Based on on-board 16S rRNA gene analysis, CARD-FISH, multi-omics approach and an extensive geochemical dataset, we report a SUP05-clade niche differentiation. Niche partitioning was evident in plumes emanating from caldera and the cone of Brothers volcano, potentially owing to the ability of SUP05 to adapt the metabolism to fluctuating environmental conditions. Low-abundant SUP05 was omnipresent, expressing a wide variety of transporters and displaying a heterotrophic lifestyle. Moreover, the mesopelagic plume was dominated by a new SUP05 species, provisionally named Candidatus Thioglobus vadi (CTV), which is found habiting coastal waters. We hypothesise that CTV could be oxidizing iron due to its occupancy of high dFe niches and highly expressed cytochromes. Taken together, we propose that the niche partitioning between SUP05 derives from small variation of environmental parameters and depth across large spatial scales.