Abstract Members of the genus Sulfurimonas (phylum Campylobacterota) dominate microbial communities of benthic and pelagic redox clines, playing a key role in the biogeochemistry of these environments. Investigating neutrally buoyant hydrothermal plumes of the Central Arctic Ocean, we found a novel type of Sulfurimonas that inhabits hydrogen-rich and oxygen-saturated environments close to the freezing point. Using omics’ approaches, we compared the diversity and distribution of Sulfurimonas from Gakkel Ridge hydrothermal plumes with those from different Mid Ocean Ridges and other Sulfurimonas-hosting environments. A single and new Sulfurimonas species, U Sulfurimonas pluma , was found to be globally abundant and active in cold (<0-4 °C), oxygen-saturated hydrothermal plumes. U S. pluma features substantial genome reduction and specific genomic traits (e.g., oxygen detoxification mechanisms, acquisition of A2-type oxidase, loss of nitrate and nitrite reductases) compared to other Sulfurimonas species. These traits are indicative for adaptation to an obligate aerobic chemolithotrophic life style in hydrogen-rich plumes, U S. pluma dominates microbial communities of metal-rich neutrally-buoyant hydrothermal plumes, suggesting a so far neglected roles of Sulfurimonas in ocean biogeochemistry and food webs.