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J Exp Biol. 2014 Jul 15;217(Pt 14):2555-68. doi: 10.1242/jeb.100487. Epub 2014 May 22.

Metabolic suppression during protracted exposure to hypoxia in the jumbo squid, Dosidicus gigas, living in an oxygen minimum zone.

Author information

1
University of Rhode Island, Center for Biotechnology and Life Science, Kingston, RI 02881, USA Seibel@uri.edu.
2
Alfred Wegener Institute, Am Handelshafen 12, D-27570 Bremerhaven, Germany.
3
Laboratório Marítimo da Guia, Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Av. Nossa Senhora do Cabo, 939, 2750-374 Cascais, Portugal.
4
Carleton University Institute of Biochemistry, Carleton University, 1125 Colonel By Drive, Ottawa, ON, Canada K1S 5B6.

Abstract

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.

KEYWORDS:

Antioxidant; Cephalopoda; Climate change; Critical oxygen partial pressure; Epigenetics; Metabolic scaling; Ocean acidification; Stress response; Vertical migration

PMID:
24855676
DOI:
10.1242/jeb.100487
[Indexed for MEDLINE]
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