Abstract
Coral reefs are naturally exposed to daily and seasonal variations in environmental oxygen levels, which can be exacerbated in intensity and duration by anthropogenic activities. However, coral’s diel oxygen dynamics and fermentative pathways remain poorly understood. Here, continuous oxygen microelectrode recordings in the coral diffusive boundary layer revealed hyperoxia during daytime and hypoxia at nighttime resulting from net photosynthesis and net respiration, respectively. The activities of the metabolic enzymes citrate synthase (CS), malate dehydrogenase, and strombine dehydrogenase remained constant throughout the day/night cycle, suggesting that energy metabolism was regulated through adjustments in metabolite fluxes and not through changes in enzyme abundance. Liquid chromatography-mass spectrometry analyses identified strombine as coral’s main fermentative end product. Strombine levels peaked as oxygen became depleted at dusk, indicating increased fermentation rates at the onset of nightly hypoxia, and again at dawn as photosynthesis restored oxygen and photosynthate supply. When these peaks were excluded from the analyses, average strombine levels during the day were nearly double those at night, indicating sifnificant fermentation rates even during aerobic conditions. These results highlight the dynamic changes in oxygen levels in the coral diffusive boundary layer, and the importance of fermentative metabolism for coral biology.
Highlights
The continuous anaerobic production of ATP depends on the ability to regenerate N AD+ from NADH in the last step of fermentation
Hyperoxia resulted from photosynthetic activity by the coral endosymbionts, while average diffusive boundary layer (DBL) [O2] levels at night were within the range of nominal hypoxia (~ 60–90 μM O222) and can be attributed to aerobic respiration by coral, algae and other microbes combined with the absence of photosynthetic activity
Studying potential changes in anaerobic metabolism required a better understanding of A. yongei fermentation, which led to the identification of strombine as corals’ main fermentative end-product, and of strombine dehydrogenase (SDH) as the main terminal dehydrogenase
Summary
The continuous anaerobic production of ATP depends on the ability to regenerate N AD+ from NADH in the last step of fermentation. In most vertebrates, this reaction is catalyzed by lactate dehydrogenase (LDH) and is coupled to the oxidation of pyruvate into lactate. Substrate utilization of opine dehydrogenases is notoriously promiscuous, and in vitro enzymatic assays do not necessarily reflect their in vivo function[18,19,20]. We sought to characterize the main fermentative pathway utilized by corals by measuring the enzymatic activities of terminal dehydrogenases, and by identifying coral fermentative end products using highly sensitive liquid chromatography (LC) and mass spectrometry (MS) methods. We quantified metabolite abundance at various time points which, combined with the O 2 microelectrode measurements and the enzymatic assays, allowed us to explore the importance of coral fermentation in relation to [ O2] in the DBL throughout a complete diel cycle
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