Unrecognized diversity of microbes linking methanotrophy to nitrogen loss in marine oxygen minimum zones

Abstract

Methane (CH4) is a potent greenhouse gas with 25 times the warming potential of carbon dioxide (CO2) on a per mol basis. Marine oxygen minimum zones (OMZs) are enriched in CH4 compared to oxygenated water columns and are predicted to expand under global warming. OMZs are also key sites for microbially-mediated nitrogen (N) loss, which has been shown in other systems to be linked to CH4 consumption. Diverse groups of microorganisms mediate the global cycling of both CH4 and N. Microbial genes encoding the enzyme used in CH4 oxidation, particulate methane monooxygenase (pmo), have previously been detected in OMZs. However, the genomic diversity and ecological importance of the OMZ CH4-cycling community are unclear, as is the mechanism by which CH4 consumption is carried out by these microbes. This thesis uses a combination of metagenomics, metatranscriptomics, and biogeochemical measurements to explore the activity and diversity of methanotrophic microbes in OMZs. OMZs were found to harbor at least two metabolic strategies for CH4 consumption. First, we found evidence that bacteria belonging to the recently discovered NC10 phylum are present and transcriptionally active at the functionally anoxic core of the OMZ. NC10 bacteria link anaerobic CH4 oxidation to nitrite (NO2-)-driven denitrification through a unique O2-producing intra-aerobic methanotrophy pathway. rRNA and mRNA transcripts assignable to NC10 peaked within the OMZ and included genes mediating this unique methanotrophic pathway. Second, metagenomic binning uncovered a separate and distinct methanotrophic strategy that is present and active within and just below the oxycline. In this strategy, gammaproteobacteria, designated phylogenetically as belonging to the OPU3 clade, were found to carry and express genes for methanotrophy and partial denitrification, thereby supporting respiration under low O2 concentrations and allowing for available O2 to be used directly for CH4 oxidation. These findings confirm OMZs as a niche for diverse and previously overlooked forms of denitrification-linked methanotrophy. Further characterization of these niches and the environmental constraints on OMZ CH4 consumption is critical for predicting the effects of OMZ expansion on global C cycling, greenhouse gas consumption, and N loss.