Oceanic oxygen minimum zones (OMZs) are globally significant sites of biogeochemical cycling where microorganisms deplete dissolved oxygen (DO) to concentrations <20 µM. Amid intense competition for DO in these metabolically challenging environments, aerobic nitrite oxidation may consume significant amounts of DO and help maintain low DO concentrations, but this remains unquantified. Using parallel measurements of oxygen consumption rates and 15N-nitrite oxidation rates applied to both water column profiles and oxygen manipulation experiments, we show that the contribution of nitrite oxidation to overall DO consumption systematically increases as DO declines below 2 µM. Nitrite oxidation can account for all DO consumption only under DO concentrations <393 nM found in and below the secondary chlorophyll maximum. These patterns are consistent across sampling stations and experiments, reflecting coupling between nitrate reduction and nitrite-oxidizing Nitrospina with high oxygen affinity (based on isotopic and omic data). Collectively our results demonstrate that nitrite oxidation plays a pivotal role in the maintenance and biogeochemical dynamics of OMZs.

Oceanic oxygen minimum zones (OMZs) play a pivotal role in biogeochemical cycles due to extensive microbial activity. How OMZ microbial communities assemble and respond to environmental variation is therefore essential to understanding OMZ functioning and ocean biogeochemistry. Sampling along depth profiles at five stations in the eastern tropical North Pacific Ocean (ETNP), we captured systematic variations in dissolved oxygen (DO) and associated variables (nitrite, chlorophyll, and ammonium) with depth and between stations. We quantitatively analysed relationships between oceanographic gradients and microbial community assembly and activity based on paired 16S rDNA and 16S rRNA sequencing. Overall microbial community composition and diversity were strongly related to regional variations in density, DO, and other variables (regression and redundancy analysis r 2 = 0.68-0.82), displaying predictable patterns with depth and between stations. Although similar factors influenced the active community, diversity was substantially lower within the OMZ. We also identified multiple active microbiological networks that tracked specific gradients or featuresparticularly subsurface ammonium and nitrite maxima. Our findings indicate that overall microbial community assembly is consistently shaped by hydrography and biogeochemistry, while active segments of the community form discrete networks inhabiting distinct portions of the water column, and that both are tightly tuned to environmental conditions in the ETNP.

Aquatic ecosystems are globally significant sources of the greenhouse gas methane to the atmosphere. Until recently, methane production was thought to be a strictly anaerobic process confined primarily to anoxic sediments. However, supersaturation of methane in oxygenated waters has been consistently observed in lakes and the ocean (termed the ‘methane paradox’), indicating that methane can be produced under oxic conditions through unclear mechanisms. Here we show aerobic methane production from multiple sources in freshwater incubation experiments under different treatments and based on biogeochemical, metagenomic, and metatranscriptomic data. We find that aerobic methane production appears to be associated with (bacterio)chlorophyll metabolism and photosynthesis, as well as with Proteobacterial degradation of methylphosphonate. Genes encoding pathways for putative photosynthetic- and methylphosphonate-based methane production also co-occur in Proteobacterial metagenome-assembled genomes. Our findings provide insight into known mechanisms of aerobic methane production, and suggest a potential co-occurring mechanism associated with bacterial photosynthesis in aquatic ecosystems.

Aquatic ecosystems are globally significant sources of the greenhouse gas methane (CH4) to the atmosphere. However, CH4 is produced ‘paradoxically’ in oxygenated water via at least three mechanisms, fundamentally limiting our understanding of overall CH4 production. Here we resolve these CH4 production mechanisms through CH4 measurements, δ13CH4 analyses, 16S rRNA sequencing, and metagenomics/transcriptomics applied to freshwater incubation experiments with multiple time points and treatments (addition of a methanogenesis inhibitor, dark, high-light). We captured significant paradoxical CH4 production, but show that methanogenesis was an unlikely CH4 source. In contrast, abundant freshwater bacteria metabolized methylphosphonate—similar to observations in marine ecosystems. Metatranscriptomics and stable isotopic analyses applied to experimental treatments also identified a potential CH4 production mechanism linked to (bacterio)chlorophyll metabolism by Cyanobacteria and especially Proteobacteria. Variability in these mechanisms across experiments indicates that multiple, widely-distributed bacterial groups and pathways can produce substantial quantities of CH4 in aquatic ecosystems.

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