Genomic insights into cryptic cycles of microbial hydrocarbon production and degradation in contiguous freshwater and marine microbiomes

• Published in: Microbiome
• Main Authors: Vigneron, Adrien, Cruaud, Perrine, Lovejoy, Connie, Vincent, Warwick F.
• Format: Other/Unknown Material
• Language: English
• Published: BioMed Central 2023
• Subjects: Alkanes; Hydrocarbons; Short hydrocarbon cycle; Biogeochemical cycles; Lakes; Sea; Hydrocarbures; Alcanes; Cycle du carbone (Biogéochimie); Enzymes microbiennes; Lacs; Arctic; Arctic Lake; Arctique*; Phytoplankton
• Online Access: https://hdl.handle.net/20.500.11794/129503; https://doi.org/10.1186/s40168-023-01537-7

Background: Cyanobacteria and eukaryotic phytoplankton produce long-chain alkanes and generate around 100 times greater quantities of hydrocarbons in the ocean compared to natural seeps and anthropogenic sources. Yet, these compounds do not accumulate in the water column, suggesting rapid biodegradation by co-localized microbial populations. Despite their ecological importance, the identities of microbes involved in this cryptic hydrocarbon cycle are mostly unknown. Here, we identifed genes encoding enzymes involved in the hydrocarbon cycle across the salinity gradient of a remote, vertically stratifed, seawater-containing High Arctic lake that is isolated from anthropogenic petroleum sources and natural seeps. Metagenomic analysis revealed diverse hydrocarbon cycling genes and populations, with patterns of variation along gradients of light, salinity, oxygen, and sulfur that are relevant to freshwater, oceanic, hadal, and anoxic deep sea ecosystems. Results Analyzing genes and metagenome-assembled genomes down the water column of Lake A in the Canadian High Arctic, we detected microbial hydrocarbon production and degradation pathways at all depths, from surface freshwaters to dark, saline, anoxic waters. In addition to Cyanobacteria, members of the phyla Flavobacteria, Nitrospina, Deltaproteobacteria, Planctomycetes, and Verrucomicrobia had pathways for alkane and alkene production, providing additional sources of biogenic hydrocarbons. Known oil-degrading microorganisms were poorly represented in the system, while long-chain hydrocarbon degradation genes were identifed in various freshwater and marine lineages such as Actinobacteria, Schleiferiaceae, and Marinimicrobia. Genes involved in sulfur and nitrogen compound transformations were abundant in hydrocarbon producing and degrading lineages, suggesting strong interconnections with nitrogen and sulfur cycles and a potential for widespread distribution in the ocean. Conclusions Our detailed metagenomic analyses across water column gradients in a remote ...