The pelagic red crab, Pleuroncodes planipes, is abundant throughout the Eastern Tropical Pacific in both benthic
and pelagic environments to depths of several hundred meters. The oxygen minimum zones in this region
reaches oxygen levels as low as 0.1 kPa at depths within the crabs vertical range. Crabs maintain aerobic metabolism
to a critical PO2 of ~0.27 ± 0.2 kPa (10 °C), in part by increasing ventilation as oxygen declines. At
subcritical oxygen levels, they enhance anaerobic ATP production slightly as indicated by modest increases in
lactate levels. However, hypoxia tolerance is primarily mediated via a pronounced suppression of aerobic metabolism
(~70%). Metabolic suppression is achieved, primarily, via reduced protein synthesis, which is a major
sink for metabolic energy. Posttranslational modifications on histone H3 suggest a condensed chromatin state
and, hence, decreased transcription. Under hypoxia, p-H3S10, Ac-H3K9, Ac-H3K14 were 39, 68, and 36% of
control values, respectively. We also report a net decrease in protein translation. In particular, eEF2 activity is
reduced due to a ~5-fold increase in inhibitory phosphorylation and a significant decrease in protein level.
Elevated heat shock proteins suggest that, despite impressive tolerance, the cellular stress response is triggered
during hypoxia. We discuss the implications for pelagic ecology and biogeochemical cycles.
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Hypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cycles
The effects of regional variations in oxygen and temperature levels with depth were assessed for the metabolism
and hypoxia tolerance of dominant euphausiid species. The physiological strategies employed by these species facilitate
prediction of changing vertical distributions with expanding oxygen minimum zones and inform estimates of the contribution
of vertically migrating species to biogeochemical cycles. The migrating species from the Eastern Tropical Pacific
(ETP), Euphausia eximia and Nematoscelis gracilis, tolerate a Partial Pressure (PO2) of 0.8 kPa at 10 8C (15 mM O2) for
at least 12 h without mortality, while the California Current species, Nematoscelis difficilis, is incapable of surviving even
2.4 kPa PO2 (32 mM O2) for more than 3 h at that temperature. Euphausia diomedeae from the Red Sea migrates into an
intermediate oxygen minimum zone, but one in which the temperature at depth remains near 22 8C. Euphausia diomedeae
survived 1.6 kPa PO2 (22 mM O2) at 228C for the duration of six hour respiration experiments. Critical oxygen
partial pressures were estimated for each species, and, for E. eximia, measured via oxygen consumption (2.1 kPa, 10 8C,
n¼2) and lactate accumulation (1.1 kPa, 10 8C). A primary mechanism facilitating low oxygen tolerance is an ability to
dramatically reduce energy expenditure during daytime forays into low oxygen waters. The ETP and Red Sea species
reduced aerobic metabolism by more than 50% during exposure to hypoxia. Anaerobic glycolytic energy production, as
indicated by whole-animal lactate accumulation, contributed only modestly to the energy deficit. Thus, the total metabolic
rate was suppressed by 49–64%. Metabolic suppression during diel migrations to depth reduces the metabolic
contribution of these species to vertical carbon and nitrogen flux (i.e., the biological pump) by an equivalent amount.
Growing evidence suggests that metabolic suppression is a widespread strategy among migrating zooplankton in oxygen
minimum zones and may have important implications for the economy and ecology of the oceans. The interacting effects
of oxygen and temperature on the metabolism of oceanic species facilitate predictions of changing vertical distribution
with climate change.
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- NSF-PAR ID:
- 10086414
- Date Published:
- Journal Name:
- Integrative and comparative biology
- Volume:
- 56
- Issue:
- 4
- ISSN:
- 1557-7023
- Page Range / eLocation ID:
- 510-523
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/doi:10.1093/icb/icw091
