Ecosystem-scale genomic and metatranscriptomic evidence for a coupled, active short-term hydrocarbon cycle in the...

Natural hydrocarbon seeps and human activities are the primary pathways by which oil enters the sea. Marine Cyanobacteria, among the most abundant photosynthetic organisms in the world, continuously produce alkanes, an additional substantial hydrocarbon source to the sea. These alkanes form the basis of the short-term hydrocarbon cycle (STHC). Alkane production proceeds via fatty acyl-ACP reductase (faar) and aldehyde deformylating oxygenase (ado), and degradation occurs via alkane monooxygenases (alkB/cyp153). Although alkane biosynthesis and degradation pathways have been characterized, ecosystem-scale evidence for their concurrent expression in situ is lacking. Here, we integrated genomic annotation and analysis of >9,000 marine bacterial and archaeal genomes representing globally distributed microbial lineages, including cultured isolates, and predominantly uncultured taxa, with metatranscriptomic read mapping. Expression of faar and ado was dominated by Prochlorococcus and, to a lesser extent, Synechococcus. Bacterial alkane consumption via alkB was dominated by Pseudomonadota, SAR324, and Bacteroidota. Archaeal alkane consumption utilizing this same 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 the marine hydrocarbon cycle, and more broadly, of carbon cycling. Furthermore, consumption of hydrocarbons, regardless of source, is a fundamentally important ecosystem cleanup service provided by microbes in the ocean. The simultaneous transcription of alkane biosynthesis and degradation genes provides ecosystem-scale evidence for a coupled and active microbial STHC that is independent of external petroleum inputs.IMPORTANCEHydrocarbons in the long-term hydrocarbon cycle (LTHC) are produced over long time scales, whereas cyanobacterial n-alkane production occurs on short time scales in the short-term hydrocarbon cycle (STHC). Continuous in situ cyanobacterial production contributes >100 million tons of hydrocarbons annually to the ocean. Despite differences in source and timescale, these cycles are linked by microbes that degrade n-alkanes using the same pathways. Here, we demonstrate that alkane production and degradation genes are concurrently expressed in the sunlit ocean, providing evidence for an active STHC based on annotation of >9,000 genomes representing globally distributed microbial lineages, including predominantly uncultured taxa, and metatranscriptomic read mapping. Importantly, an active STHC may support a population of alkane-degrading bacteria and archaea, enabling a rapid response to oil input from a geological reservoir as part of the LTHC, through natural or anthropogenic activities, with implications for bioremediation and marine ecosystem health.