Hydrocarbon metabolism and petroleum seepage as ecological and evolutionary drivers for <i>Cycloclasticus</i>

Aqueous-soluble hydrocarbons dissolve into the ocean's interior and structure deep-sea microbial populations influenced by natural oil seeps and spills. Among these hydrocarbons, n-pentane, is a seawater-soluble, volatile compound abundant in petroleum products and reservoirs, which partially partitions to the deep-water column following release from the seafloor. In this study, we explore the ecology and niche partitioning of two free-living Cycloclasticus strains recovered from seawater incubations with n-pentane and distinguish them as an open ocean variant and a seep-proximal variant, each with distinct capabilities for hydrocarbon catabolism. Comparative metagenomic analysis indicates the variant more frequently observed further from natural seeps encodes more general pathways for hydrocarbon consumption, including short-chain alkanes, aromatics, and long-chain alkanes, and also possesses redox versatility in the form of respiratory nitrate reduction and thiosulfate oxidation; in contrast, the seep variant specializes in short-chain alkanes and relies strictly on oxygen as the terminal electron acceptor. Both variants observed in our work were dominant ecotypes of Cycloclasticus observed during the Deepwater Horizon disaster, a conclusion supported by 16S rRNA gene analysis and read-recruitment of sequences collected from the submerged oil plume during active flow. A comparative genomic analysis of Cycloclasticus across various ecosystems suggests distinct strategies for hydrocarbon transformations among each clade. Our findings suggest Cycloclasticus is a versatile and opportunistic consumer of hydrocarbons and may have a greater role in the cycling of sulfur and nitrogen, thus contributing broad ecological impact to various ecosystems globally.