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Enzymatic capacities of metabolic fuel use in cuttlefish (Sepia officinalis) and responses to food deprivation: insight into the metabolic organization and starvation survival strategy of cephalopods

Abstract

Food limitation is a common challenge for animals. Cephalopods are sensitive to starvation because of high metabolic rates and growth rates related to their “live fast, die young” life history. We investigated how enzymatic capacities of key metabolic pathways are modulated during starvation in the common cuttlefish (Sepia officinalis) to gain insight into the metabolic organization of cephalopods and their strategies for coping with food limitation. In particular, lipids have traditionally been considered unimportant fuels in cephalopods, yet, puzzlingly, many species (including cuttlefish) mobilize the lipid stores in their digestive gland during starvation. Using a comprehensive multi-tissue assay of enzymatic capacities for energy metabolism, we show that, during long-term starvation (12 days), glycolytic capacity for glucose use is decreased in cuttlefish tissues, while capacities for use of lipid-based fuels (fatty acids and ketone bodies) and amino acid fuels are retained or increased. Specifically, the capacity to use the ketone body acetoacetate as fuel is widespread across tissues and gill has a previously unrecognized capacity for fatty acid catabolism, albeit at low rates. The capacity for de novo glucose synthesis (gluconeogenesis), important for glucose homeostasis, likely is restricted to the digestive gland, contrary to previous reports of widespread gluconeogenesis among cephalopod tissues. Short-term starvation (3–5 days) had few effects on enzymatic capacities. Similar to vertebrates, lipid-based fuels, putatively mobilized from fat stores in the digestive gland, appear to be important energy sources for cephalopods, especially during starvation when glycolytic capacity is decreased perhaps to conserve available glucose.

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Acknowledgments

We thank the staff and students at Centro de Ciências do Mar do Algarve for their hospitality and invaluable help during our research, in particular Juan Carlos Capaz, Ana Couto, Ana Oliveira, João Reis, Tania Rodríguez-González, and Cátia Silva. We also thank Dr. Matthew Nosworthy for skilled assistance during a portion of this study and Dr. Kurt Gamperl for loaning us certain equipment. Funding was provided by an NSERC Postdoctoral Fellowship to B.S.-R., an NSERC Canada Graduate Scholarship-Master’s and a New Brunswick Innovation Foundation scholarship to N.I.C., and NSERC Discovery Grants to W.R.D., T.J.M., and S.G.L. AVS was supported by Fundação para a Ciência e a Tecnologia through Programa Investigador FCT 2014 (IF/00576/2014) and project SEPIATECH (31-03-05-FEP-2), funded by the Portuguese Government Program PROMAR.

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Correspondence to Ben Speers-Roesch.

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Communicated by H.V. Carey.

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Speers-Roesch, B., Callaghan, N.I., MacCormack, T.J. et al. Enzymatic capacities of metabolic fuel use in cuttlefish (Sepia officinalis) and responses to food deprivation: insight into the metabolic organization and starvation survival strategy of cephalopods. J Comp Physiol B 186, 711–725 (2016). https://doi.org/10.1007/s00360-016-0991-3

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  • DOI: https://doi.org/10.1007/s00360-016-0991-3

Keywords

  • Cephalopod
  • Energy metabolism
  • Metabolic fuel preference
  • Enzyme activity
  • Starvation
  • Fasting
  • Lipid
  • Ketone body
  • Amino acid
  • Glucose
  • Glycolysis
  • Gluconeogenesis
  • Digestive gland