The summer surface waters of the Arctic Ocean (AO) are among the most oligotrophic marine ecosystems on Earth. The AO is also influenced by variable sea ice and sunlight. Little is known about how marine bacteria have adapted to survive this extreme Arctic habitat. Volatile organic compounds (VOCs) are increasingly recognized as important resources for bacterial metabolism in oligotrophic oceans. Studies show that the AO is a net sink for VOCs, leading to the hypothesis that Arctic Ocean bacteria consume VOCs. To test this hypothesis, we investigated a genome catalogue of AO prokaryotes for the presence of VOC-degradation pathways. A carboxylation pathway for acetone degradation dominated the surface waters. The key enzyme (acetone carboxylase) allows bacteria to access CO₂ through acetone carboxylation, suggesting a type of heterotrophic CO₂ fixation may operate in the AO. The acetone-consuming bacteria were mostly represented by a single population of Porticoccus bacteria (SP-01). The genome encoded few organic carbon transporters, but proteorhodopsin genes were identified, indicating heterotrophic metabolism could be supplemented with energy from sunlight. Metatranscriptome analysis revealed that acetone carboxylase and proteorhodopsin were among the most highly expressed genes, indicating significant investment in the exploitation of acetone and sunlight in carbon and energy metabolism. From 2004 to 2017, SP-01 had a 1-8% annual average abundance, peaking in 2017, a year distinguished by a longer ice-free period. The future relevance of bacteria, such as SP-01, adapted to AO oligotrophic surface water may increase with a warming Arctic, when ice-free conditions prevail and ocean stratification and subsequent oligotrophication intensify.