Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone
The jumbo squid, Dosidicus gigas, can survive extended forays into the oxygen minimum zone (OMZ) of the Eastern Pacific Ocean. Previous studies have demonstrated reduced oxygen consumption and a limited anaerobic contribution to ATP production, suggesting the capacity for substantial metabolic suppr...
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ftunisfloridatam:oai:digitalcommons.usf.edu:msc_facpub-3407 2023-05-15T17:52:05+02:00 Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone Seibel, Brad A. Häfker, N. Sören Trübenbach, Katja Zhang, Jing Tessier, Shannon N. Pörtner, Hans-Otto Rosa, Rui Storey, Kenneth B. 2014-01-01T08:00:00Z https://digitalcommons.usf.edu/msc_facpub/2341 https://doi.org/10.1242/jeb.100487 unknown Digital Commons @ University of South Florida https://digitalcommons.usf.edu/msc_facpub/2341 https://doi.org/10.1242/jeb.100487 Marine Science Faculty Publications Climate change Vertical migration Ocean acidification Critical oxygen partial pressure Cephalopoda Epigenetics Stress response Antioxidant Metabolic scaling Life Sciences article 2014 ftunisfloridatam https://doi.org/10.1242/jeb.100487 2022-04-07T17:43:38Z The jumbo squid, Dosidicus gigas, can survive extended forays into the oxygen minimum zone (OMZ) of the Eastern Pacific Ocean. Previous studies have demonstrated reduced oxygen consumption and a limited anaerobic contribution to ATP production, suggesting the capacity for substantial metabolic suppression during hypoxic exposure. Here, we provide a more complete description of energy metabolism and explore the expression of proteins indicative of transcriptional and translational arrest that may contribute to metabolic suppression. We demonstrate a suppression of total ATP demand under hypoxic conditions (1% oxygen, PO2=0.8 kPa) in both juveniles (52%) and adults (35%) of the jumbo squid. Oxygen consumption rates are reduced to 20% under hypoxia relative to air-saturated controls. Concentrations of arginine phosphate (Arg-P) and ATP declined initially, reaching a new steady state (~30% of controls) after the first hour of hypoxic exposure. Octopine began accumulating after the first hour of hypoxic exposure, once Arg-P breakdown resulted in sufficient free arginine for substrate. Octopine reached levels near 30 mmol g−1 after 3.4 h of hypoxic exposure. Succinate did increase through hypoxia but contributed minimally to total ATP production. Glycogenolysis in mantle muscle presumably serves to maintain muscle functionality and balance energetics during hypoxia. We provide evidence that post-translational modifications on histone proteins and translation factors serve as a primary means of energy conservation and that select components of the stress response are altered in hypoxic squids. Reduced ATP consumption under hypoxia serves to maintain ATP levels, prolong fuel store use and minimize the accumulation of acidic intermediates of anaerobic ATP-generating pathways during prolonged diel forays into the OMZ. Metabolic suppression likely limits active, daytime foraging at depth in the core of the OMZ, but confers an energetic advantage over competitors that must remain in warm, oxygenated surface waters. Moreover, the capacity for metabolic suppression provides habitat flexibility as OMZs expand as a result of climate change. Article in Journal/Newspaper Ocean acidification Digital Commons University of South Florida (USF) Pacific Journal of Experimental Biology |
institution |
Open Polar |
collection |
Digital Commons University of South Florida (USF) |
op_collection_id |
ftunisfloridatam |
language |
unknown |
topic |
Climate change Vertical migration Ocean acidification Critical oxygen partial pressure Cephalopoda Epigenetics Stress response Antioxidant Metabolic scaling Life Sciences |
spellingShingle |
Climate change Vertical migration Ocean acidification Critical oxygen partial pressure Cephalopoda Epigenetics Stress response Antioxidant Metabolic scaling Life Sciences Seibel, Brad A. Häfker, N. Sören Trübenbach, Katja Zhang, Jing Tessier, Shannon N. Pörtner, Hans-Otto Rosa, Rui Storey, Kenneth B. Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone |
topic_facet |
Climate change Vertical migration Ocean acidification Critical oxygen partial pressure Cephalopoda Epigenetics Stress response Antioxidant Metabolic scaling Life Sciences |
description |
The jumbo squid, Dosidicus gigas, can survive extended forays into the oxygen minimum zone (OMZ) of the Eastern Pacific Ocean. Previous studies have demonstrated reduced oxygen consumption and a limited anaerobic contribution to ATP production, suggesting the capacity for substantial metabolic suppression during hypoxic exposure. Here, we provide a more complete description of energy metabolism and explore the expression of proteins indicative of transcriptional and translational arrest that may contribute to metabolic suppression. We demonstrate a suppression of total ATP demand under hypoxic conditions (1% oxygen, PO2=0.8 kPa) in both juveniles (52%) and adults (35%) of the jumbo squid. Oxygen consumption rates are reduced to 20% under hypoxia relative to air-saturated controls. Concentrations of arginine phosphate (Arg-P) and ATP declined initially, reaching a new steady state (~30% of controls) after the first hour of hypoxic exposure. Octopine began accumulating after the first hour of hypoxic exposure, once Arg-P breakdown resulted in sufficient free arginine for substrate. Octopine reached levels near 30 mmol g−1 after 3.4 h of hypoxic exposure. Succinate did increase through hypoxia but contributed minimally to total ATP production. Glycogenolysis in mantle muscle presumably serves to maintain muscle functionality and balance energetics during hypoxia. We provide evidence that post-translational modifications on histone proteins and translation factors serve as a primary means of energy conservation and that select components of the stress response are altered in hypoxic squids. Reduced ATP consumption under hypoxia serves to maintain ATP levels, prolong fuel store use and minimize the accumulation of acidic intermediates of anaerobic ATP-generating pathways during prolonged diel forays into the OMZ. Metabolic suppression likely limits active, daytime foraging at depth in the core of the OMZ, but confers an energetic advantage over competitors that must remain in warm, oxygenated surface waters. Moreover, the capacity for metabolic suppression provides habitat flexibility as OMZs expand as a result of climate change. |
format |
Article in Journal/Newspaper |
author |
Seibel, Brad A. Häfker, N. Sören Trübenbach, Katja Zhang, Jing Tessier, Shannon N. Pörtner, Hans-Otto Rosa, Rui Storey, Kenneth B. |
author_facet |
Seibel, Brad A. Häfker, N. Sören Trübenbach, Katja Zhang, Jing Tessier, Shannon N. Pörtner, Hans-Otto Rosa, Rui Storey, Kenneth B. |
author_sort |
Seibel, Brad A. |
title |
Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone |
title_short |
Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone |
title_full |
Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone |
title_fullStr |
Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone |
title_full_unstemmed |
Metabolic Suppression During Protracted Exposure to Hypoxia in the Jumbo Squid, Dosidicus gigas , Living in an Oxygen Minimum Zone |
title_sort |
metabolic suppression during protracted exposure to hypoxia in the jumbo squid, dosidicus gigas , living in an oxygen minimum zone |
publisher |
Digital Commons @ University of South Florida |
publishDate |
2014 |
url |
https://digitalcommons.usf.edu/msc_facpub/2341 https://doi.org/10.1242/jeb.100487 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Ocean acidification |
genre_facet |
Ocean acidification |
op_source |
Marine Science Faculty Publications |
op_relation |
https://digitalcommons.usf.edu/msc_facpub/2341 https://doi.org/10.1242/jeb.100487 |
op_doi |
https://doi.org/10.1242/jeb.100487 |
container_title |
Journal of Experimental Biology |
_version_ |
1766159424893747200 |