Hydrothermal activity can generate numerous and diverse hydrocarbon compounds. However, little is known about the influence of such hydrocarbons on deep-sea hydrothermal microbial ecology. We hypothesize that certain bacteria live on these hydrocarbons. Therefore, in this study, the distribution of hydrocarbons and their associated hydrocarbon-degrading bacteria were investigated at deep-sea hydrothermal vents at the Southern Mid-Atlantic Ridge, the Southwest Indian Ridge, and the East Pacific Rise. A variety of hydrocarbon-degrading consortia were obtained from hydrothermal samples collected at the aforementioned sites after low-temperature enrichment under high hydrostatic pressures, and the bacteria responsible for the degradation of hydrocarbons were investigated by DNA-based stable-isotope probing with uniformly 13C-labeled hydrocarbons. Unusually, we identified several previously recognized sulfur-oxidizing chemoautotrophs as hydrocarbon-degrading bacteria, e.g., the SAR324 group, the SUP05 clade, and Sulfurimonas, and for the first time confirmed their ability to degrade hydrocarbons. In addition, Erythrobacter, Pusillimonas, and SAR202 clade were shown to degrade polycyclic aromatic hydrocarbons for the first time. These results together with relatively high abundance in situ of most of the above-described bacteria highlight the potential influence of hydrocarbons in configuring the vent microbial community, and have made the importance of mixotrophs in hydrothermal vent ecosystems evident.