Biochemical Barriers on the Path to Ocean Anoxia?

Declining ocean oxygen associated with global warming and climate change is impacting marine ecosystems across scales from microscopic planktonic communities to global fisheries. We report a fundamental dichotomy in the affinities of enzymes for oxygen—the terminal proteins catalyzing respiration are active at much lower oxygen concentrations than oxygenase enzymes involved in organic matter catabolism. ABSTRACT The kinetics of microbial respiration suggests that, if excess organic matter is present, oxygen should fall to nanomolar levels in the range of the Michaelis-Menten constants (Km). Yet even in many biologically productive coastal regions, lowest observed O2 concentrations often remain several orders of magnitude higher than respiratory Km values. We propose the hypoxic barrier hypothesis (HBH) to explain this apparent discrepancy. The HBH postulates that oxidative enzymes involved in organic matter catabolism are kinetically limited by O2 at concentrations far higher than the thresholds for respiration. We found support for the HBH in a meta-analysis of 1,137 O2 Km values reported in the literature: the median value for terminal respiratory oxidases was 350 nM, but for other oxidase types, the median value was 67 μM. The HBH directs our attention to the kinetic properties of an important class of oxygen-dependent reactions that could help explain the trajectories of ocean ecosystems experiencing O2 stress. IMPORTANCE Declining ocean oxygen associated with global warming and climate change is impacting marine ecosystems across scales from microscopic planktonic communities to global fisheries. We report a fundamental dichotomy in the affinities of enzymes for oxygen—the terminal proteins catalyzing respiration are active at much lower oxygen concentrations than oxygenase enzymes involved in organic matter catabolism. We hypothesize that this dichotomy in oxygen affinities will cause some types of organic matter to accumulate in hypoxic ecosystems and will slow rates of oxygen decline. This proposed biochemical barrier may explain why many ocean ecosystems rarely reach anoxia. Competition between intracellular enzymes for oxygen may also have impacted microbial strategies of adaptation to low oxygen, requiring cells to regulate oxygen respiration so that it does not compete with other cellular processes that also require oxygen.

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