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

Abstract

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. ImportanceHydrocarbons in the long-term hydrocarbon cycle (LTHC) are produced over long-time scales. In comparison, hydrocarbons, specifically n-alkanes, are produced on short time scales by Cyanobacteria as part of basic cellular processes in the short-term hydrocarbon cycle (STHC). Cyanobacterial production of n-alkanes leads to an additional annual input of more than 100 million tons of hydrocarbons to the ocean. Despite the difference in time scale and source, these hydrocarbon cycles are intrinsically linked by microbes that consume n-alkanes using the same pathways for degradation. Here we show that the production and consumption in the STHC is an active cycle in the sunlit ocean, as determined by analysis of genomes and metatranscriptomes. Importantly an active STHC could support a population of alkane degrading bacteria, 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 ultimately for marine ecosystem health.