Activity and diversity of aerobic methanotrophs in a coastal marine oxygen minimum zone

The pelagic ocean is a sink for the potent greenhouse gas methane, with methane consumption regulated primarily by aerobic methane-oxidizing bacteria (MOB). Marine oxygen minimum zones (OMZs) contain the largest pool of pelagic methane in the oceans but remain largely unexplored for their potential to harbor MOB communities and contribute to methane cycling. Here, we present meta-omic and geochemical evidence that aerobic MOB are present and active in a coastal OMZ, in Golfo Dulce, Costa Rica. Oxygen concentrations were < 50 nM below 85 m, and sulfide accumulated below 140 m, with methane concentrations ranging from trace levels above the oxycline to ~78 nM at 180 m. The upper OMZ (90 m) was characterized by an abundant MOB and methylotroph community representing diverse lineages of the Methylophilaceae, Methylophaga, and Methylococcales. Of these, Type I methanotrophs of the Order Methylococcales dominated , representing >5% of total 16S rRNA genes and >19% of 16S rRNA transcripts. This peak in ribosomal abundance and activity was affiliated with methane oxidation rates of 2.6 ± 0.7 nM d^-1, measured in seawater incubations with estimated O₂ concentrations of 50 nM. Rates fell to zero with the addition of acetylene, an inhibitor of aerobic methanotrophy. In contrast, methane oxidation was below detection at lower depths in the OMZ (100 m and 120 m). Metatranscriptome sequencing indicated a peak at 90 m in the expression of pathways essential to Methylococcales, including aerobic methanotrophy and the RuMP pathway of carbon assimilation, as well as the serine pathway of Type II methanotrophs. Preliminary analysis of single-cell genomes suggests distinct adaptations by Methylococcales from the Golfo Dulce, helping explain the persistence of putative aerobic methanotrophs under very low oxygen in this OMZ. Taken together, these data suggest the boundary layers of OMZs, despite extreme oxygen depletion, are a niche for aerobic MOBs and therefore potentially important zones of pelagic methane loss.