Oxygen-dependent metabolism of dissolved organic matter in hypoxic marine environments

Low-oxygen marine environments are dynamic hotspots where microbial activity and dissolved organic matter (DOM) cycling are altered, with implications for understanding ecosystem responses to intensifying anthropogenic pressures. The hypoxic barrier hypothesis (HBH) proposed a mechanism by which DOM cycling could be altered under hypoxia by the inhibition of non-respiratory oxidase enzymes, whereas respiration continued. To investigate oxygen-dependent changes in DOM composition and consequences of the HBH, we combined controlled mesocosm experiments with non-targeted metabolomics to identify classes of compounds that accumulate in hypoxic treatments. Many of these compounds require non-respiratory oxidase enzymes for catabolism in KEGG metabolic maps, and when tested in experiments with microbial communities, their catabolism was inhibited by hypoxia, validating the concept of oxygen-dependent dissolved organic matter (ODDOM). The identified ODDOM molecules displayed chemical characteristics associated with increased DOM stability, including increased aromaticity, carbon oxidation state, and decreased saturation. In a meta-analysis of FT-ICR-MS datasets from three oceanographic cruises that included samples collected across oxygen gradients and within oxygen minimum zone (OMZ) waters, molecules with chemical properties similar to the mesocosm-derived ODDOM accumulated within the oxycline of the North Pacific Ocean. In the mesocosm experiments, the growth of many microbial taxa was unaffected by hypoxia, and others were either stimulated or inhibited by hypoxia, suggesting unexplored complexity in microbial adaptations to oxygen concentrations in this range. These findings suggest that hypoxia can mechanistically constrain enzymatic pathways determining DOM bioavailability, with implications for microbial carbon cycling and microbial evolution in expanding ocean oxygen minimum zones.