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Hypoxia-driven selective degradation of cellular proteins in jumbo squids during diel migration to the oxygen minimum zones

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Abstract

The jumbo squid, Dosidicus gigas, is an oceanic top predator in the eastern tropical Pacific that undergoes diel vertical migrations into mesopelagic oxygen minimum zones (OMZs). Besides glycogen breakdown, the pathways of the squid’s metabolic (suppression) strategy are poorly understood. Here, juvenile D. gigas were exposed to oxygen levels found in the OMZ off Gulf of California (1 % O2, 1 kPa at 10 °C) with the aim to identify, via proteomic tools, eventual anaerobic protein degradation as potential energy source at such depths. Under hypoxia, total protein concentration decreased nonsignificantly from 79.2 ± 12.4 mg g−1 wet mass to 74.7 ± 11.7 mg g−1 wet mass (p > 0.05). Yet, there was a significant decrease in heat-shock protein (Hsp) 90 and α-actinin contents (p < 0.05). The lower α-actinin concentration at late hypoxia was probably related to decreased protection of the Hsp90 chaperon machinery resulting in increased ubiquitination (p < 0.05) and subsequent degradation. Thus, the present findings indicate that D. gigas might degrade, at least under progressing hypoxia, specific mantle proteins anaerobically to increase/maintain anaerobic ATP production and extend hypoxia exposure time. Moreover, the ubiquitin–proteasome system seems to play an important role in hypoxia tolerance, but further investigations are necessary to discover its full potential and pathways.

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Acknowledgments

The authors would like to thank Brad Seibel for making the participation in the research cruise aboard RV New Horizon possible, and Unai Markaida for his assistance in collecting the specimens. We also thank IPATIMUP (Porto, Portugal) for help processing our samples. This work was supported by research grants to R.R. from the Portugal–US Research Networks Program (FLAD/US National Science Foundation Research Grant) and The Portuguese Foundation for Science and Technology (FCT, Ciência 2007 Program).

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  1. Laboratório Marítimo da Guia, Centre of Oceanography, University of Science in Lisbon, Av. Nossa Senhora do Cabo 939, 2750-374, Cascais, Portugal

    Katja Trübenbach & Rui Rosa

  2. Department of Chemistry and Biochemistry, University of Science in Lisbon, Campo Grande, 1749-016, Lisbon, Portugal

    Gonçalo da Costa, Cristina Ribeiro-Silva, Raquel Mesquita Ribeiro & Carlos Cordeiro

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  1. Katja Trübenbach
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Correspondence to Katja Trübenbach.

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Trübenbach, K., da Costa, G., Ribeiro-Silva, C. et al. Hypoxia-driven selective degradation of cellular proteins in jumbo squids during diel migration to the oxygen minimum zones. Mar Biol 161, 575–584 (2014). https://doi.org/10.1007/s00227-013-2360-z

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