Genomic and metatranscriptomic analyses reveal an active microbial hydrocarbon cycle in the photic zone

Natural hydrocarbon seeps and hydrocarbons resulting from human activities are the primary conduits by which oil enters the sea. Marine Cyanobacteria, among the most abundant photosynthetic organisms in the world, produce alkanes, an additional hydrocarbon source to the sea. Alkane production proceeds via metabolism of fatty acid intermediates with a fatty acyl-ACP reductase (FAAR) and an aldehyde-deformylating oxygenase (ADO). These alkanes can be consumed with alkane hydroxylases, including alkane 1-monooxygenase (alkB). The production and consumption of alkanes in the photic zone is termed the short-term hydrocarbon cycle (STHC). Yet, an active STHC has not been substantiated through gene expression analyses. To determine if the STHC is active in the marine photic zone we evaluated over 9000 genomes to which metatranscriptome reads from a site in the Gulf of Mexico were recruited. In these samples, FAAR and ADO expression was dominated by Prochlorococcus and to a lesser extent Synechococcus . Bacterial alkane consumption via alkB was dominated by Pseudomonadota, SAR324, and Bacteroidota alkB gene expression. Additionally, archaeal alkane consumption utilizing this same n-alkane degradation pathway was observed in the transcript data by Thermoplasmatota, classified as Marine Group II and III, the most abundant planktonic archaeal groups. Active production of alkanes in the photic zone would be an important component of marine hydrocarbon cycle and more broadly of carbon cycling. Further, consumption of hydrocarbons, regardless of source, is a fundamentally important ecosystem cleanup service provided by microbes in the ocean.