Metagenomics and quantitative stable isotope probing offer insights into metabolism of polycyclic aromatic hydrocarbons degraders in chronically polluted seawater

Bacterial biodegradation is a significant contributor to remineralization of polycyclic aromatic hydrocarbons (PAHs): toxic and recalcitrant components of crude oil as well as byproducts of partial combustion chronically introduced into seawater via atmospheric deposition. The Deepwater Horizon oil spill demonstrated the speed at which a seed PAH-degrading community maintained by low chronic inputs can respond to acute pollution. We investigated the diversity and functional potential of a similar seed community in the Port of Los Angeles, a chronically polluted site, using stable isotope probing with naphthalene, deep-sequenced metagenomes and carbon incorporation rate measurements at the port and in two sites further into the San Pedro Channel. We demonstrate the ability of a local seed community of degraders at the Port of LA to incorporate carbon from naphthalene, leading to a quick shift in the microbial community composition to be dominated by these normally rare taxa. We were able to directly show that assembled genomes belonged to naphthalene degraders by matching their 16S-rRNA gene with experimental stable isotope probing data. Surprisingly, we did not find a full PAH degradation pathway in those genomes and even when combining genes from the entire microbial community. We analyze metabolic pathways identified in 29 genomes whose abundance increased in the presence of naphthalene to generate metagenomic-based recommendations for future optimization of PAHs bioremediation. ImportanceOil spills in the marine environment have a devastating effect on marine life and biogeochemical cycles. Oil-degrading bacteria occur naturally in the ocean, especially where they are supported by chronic inputs of oil, and have a significant role in degradation of oil spills. The most recalcitrant and toxic component of oil is polycyclic aromatic hydrocarbons. Therefore, the bacteria who can break those molecules down are of particular importance. We identified such bacteria at the port of Los Angeles, one of the busiest ports worldwide, and characterized their metabolic capabilities. Based on those analyses we proposed chemical targets to stimulate the activity of these bacteria in case of an oil spill in the port of LA.