Biochemical Barriers on the Path to Ocean Anoxia?

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 seve...

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Autores principales: Stephen Giovannoni, Francis Chan, Edward Davis, Curtis Deutsch, Sarah Wolf
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Lenguaje:EN
Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:240ae37c976a4e298b264e095495808d2021-11-10T18:37:51ZBiochemical Barriers on the Path to Ocean Anoxia?10.1128/mBio.01332-212150-7511https://doaj.org/article/240ae37c976a4e298b264e095495808d2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01332-21https://doaj.org/toc/2150-7511ABSTRACT 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.Stephen GiovannoniFrancis ChanEdward DavisCurtis DeutschSarah WolfAmerican Society for Microbiologyarticledissolved organic matterocean respirationoxygen minimum zonesoxygenase Kmocean respirationdissolved organic matterMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution DOAJ
collection DOAJ
language EN
topic dissolved organic matter
ocean respiration
oxygen minimum zones
oxygenase Km
ocean respiration
dissolved organic matter
Microbiology
QR1-502
spellingShingle dissolved organic matter
ocean respiration
oxygen minimum zones
oxygenase Km
ocean respiration
dissolved organic matter
Microbiology
QR1-502
Stephen Giovannoni
Francis Chan
Edward Davis
Curtis Deutsch
Sarah Wolf
Biochemical Barriers on the Path to Ocean Anoxia?
description 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.
format article
author Stephen Giovannoni
Francis Chan
Edward Davis
Curtis Deutsch
Sarah Wolf
author_facet Stephen Giovannoni
Francis Chan
Edward Davis
Curtis Deutsch
Sarah Wolf
author_sort Stephen Giovannoni
title Biochemical Barriers on the Path to Ocean Anoxia?
title_short Biochemical Barriers on the Path to Ocean Anoxia?
title_full Biochemical Barriers on the Path to Ocean Anoxia?
title_fullStr Biochemical Barriers on the Path to Ocean Anoxia?
title_full_unstemmed Biochemical Barriers on the Path to Ocean Anoxia?
title_sort biochemical barriers on the path to ocean anoxia?
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/240ae37c976a4e298b264e095495808d
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AT francischan biochemicalbarriersonthepathtooceananoxia
AT edwarddavis biochemicalbarriersonthepathtooceananoxia
AT curtisdeutsch biochemicalbarriersonthepathtooceananoxia
AT sarahwolf biochemicalbarriersonthepathtooceananoxia
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