Methylated cycloalkanes fuel a novel genus in the Porticoccaceae family (Ca. Reddybacter gen. nov).

Cycloalkanes are abundant and toxic compounds in subsurface petroleum reservoirs and their fate is important to ecosystems impacted by natural oil seeps and spills. This study focuses on the microbial metabolism of methylcyclohexane (MCH) and methylcyclopentane (MCP) in the deep Gulf of Mexico. MCH and MCP are often abundant cycloalkanes observed in petroleum and will dissolve into the water column when introduced at the seafloor via a spill or natural seep. We conducted incubations with deep Gulf of Mexico (GOM) seawater amended with MCH and MCP at four stations. Within incubations with active respiration of MCH and MCP, we found that a novel genus of bacteria belonging to the Porticoccaceae family (Candidatus Reddybacter) dominated the microbial community. Using metagenome-assembled genomes, we reconstructed the central metabolism of Candidatus Reddybacter, identifying a novel clade of the particulate hydrocarbon monooxygenase (pmo) that may play a central role in MCH and MCP metabolism. Through comparative analysis of 174 genomes, we parsed the taxonomy of the Porticoccaceae family and found evidence suggesting the acquisition of pmo and other genes related to the degradation of cyclic and branched hydrophobic compounds were likely key events in the ecology and evolution of this group of organisms.

Microbial production and consumption of hydrocarbons in the global ocean.

Seeps, spills and other oil pollution introduce hydrocarbons into the ocean. Marine cyanobacteria also produce hydrocarbons from fatty acids, but little is known about the size and turnover of this cyanobacterial hydrocarbon cycle. We report that cyanobacteria in an oligotrophic gyre mainly produce n-pentadecane and that microbial hydrocarbon production exhibits stratification and diel cycling in the sunlit surface ocean. Using chemical and isotopic tracing we find that pentadecane production mainly occurs in the lower euphotic zone. Using a multifaceted approach, we estimate that the global flux of cyanobacteria-produced pentadecane exceeds total oil input in the ocean by 100- to 500-fold. We show that rapid pentadecane consumption sustains a population of pentadecane-degrading bacteria, and possibly archaea. Our findings characterize a microbial hydrocarbon cycle in the open ocean that dwarfs oil input. We hypothesize that cyanobacterial hydrocarbon production selectively primes the ocean's microbiome with long-chain alkanes whereas degradation of other petroleum hydrocarbons is controlled by factors including proximity to petroleum seepage.