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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

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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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References

  • Agnisola C, Driedzic WR, Foster AR, Houlihan DF, Stewart JM (1991) Oxygen consumption, carbon dioxide production and enzyme activities of isolated working Octopus heart. J Exp Biol 157:543–549

    CAS  Google Scholar 

  • Alegre M, Ciudad CJ, Fillat C, Guinovart JJ (1988) Determination of glucose-6-phosphatase activity using the glucose dehydrogenase-coupled reaction. Anal Biochem 173:185–189

    Article  CAS  PubMed  Google Scholar 

  • Ballantyne JS, Berges JA (1991) Enzyme activities of gill, hepatopancreas, mantle, and adductor muscle of the oyster (Crassostrea virginica) after changes in diet and salinity. Can J Fish Aquat Sci 48:1117–1123

    Article  CAS  Google Scholar 

  • Ballantyne JS, Moon TW (1985) Hepatopancreas mitochondria from Mytilus edulis: substrate preference and effects of pH and osmolarity. Mar Biol 87:239–244

    Article  CAS  Google Scholar 

  • Ballantyne JS, Moyes CD (1987) Osmotic effects on fatty acid, pyruvate, and ketone body oxidation in oyster gill mitochondria. Physiol Zool 60:713–721

    Article  CAS  Google Scholar 

  • Ballantyne JS, Storey KB (1983) Mitochondria from the ventricle of the marine clam, Mercenaria mercenaria: substrate preferences and effects of pH and salt concentration on proline oxidation. Comp Biochem Physiol B 76:133–138

    Google Scholar 

  • Ballantyne JS, Storey KB (1984) Mitochondria from the hepatopancreas of the marine clam Mercenaria mercenaria: substrate preferences and salt and pH effects on the oxidation of palmitoyl-L-carnitine and succinate. J Exp Zool 230:165–174

    Article  CAS  PubMed  Google Scholar 

  • Ballantyne JS, Hochachka PW, Mommsen TP (1981) Studies on the metabolism of the migratory squid, Loligo opalescens: enzymes of tissues and heart mitochondria. Mar Biol Lett 2:75–85

    CAS  Google Scholar 

  • Bar N (2014) Physiological and hormonal changes during prolonged starvation in fish. Can J Fish Aquat Sci 71:1447–1458

    Article  CAS  Google Scholar 

  • Bar N, Volkoff H (2012) Adaptation of the physiological, endocrine, and digestive system functions to prolonged food deprivation in fish. In: McCue M (ed) Comparative physiology of fasting, starvation, and food limitation. Springer, Berlin, pp 69–89

    Chapter  Google Scholar 

  • Beis A, Zammit VA, Newsholme EA (1980) Activities of 3-hydroxybutyrate dehydrogenase, 3-oxoacid CoA-transferase and acetoacetyl-CoA thiolase in relation to ketone-body utilisation in muscles from vertebrates and invertebrates. Eur J Biochem 104:209–215

    Article  CAS  PubMed  Google Scholar 

  • Black D, Love RM (1986) The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J Comp Physiol B 156:469–479

    Article  CAS  Google Scholar 

  • Blier P, Guderley H (1986) The enzymatic and metabolic effects of extended food deprivation in Rana pipiens. Physiol Zool 59:230–239

    Article  CAS  Google Scholar 

  • Boucher-Rodoni R, Mangold K (1985) Ammonia excretion during feeding and starvation in Octopus vulgaris. Mar Biol 86:193–197

    Article  CAS  Google Scholar 

  • Brooks SP (1994) A program for analyzing enzyme rate data obtained from a microplate reader. Biotechniques 17:1154–1161

    CAS  PubMed  Google Scholar 

  • Cahill GF Jr (2006) Fuel metabolism in starvation. Annu Rev Nutr 26:1–22

    Article  CAS  PubMed  Google Scholar 

  • Castro BG, Garrido JL, Sotelo CG (1992) Changes in composition of digestive gland and mantle muscle of the cuttlefish Sepia officinalis during starvation. Mar Biol 114:11–20

    CAS  Google Scholar 

  • Cherel Y, Burnol AF, Leturque A, Le Maho Y (1988) In vivo glucose utilization in rat tissues during the three phases of starvation. Metabolism 37:1033–1039

    Article  CAS  PubMed  Google Scholar 

  • Crabtree B, Higgins SJ, Newsholme EA (1972) The activities of pyruvate carboxylase, phosphoenolpyruvate carboxylase and fructose diphosphatase in muscles from vertebrates and invertebrates. Biochem J 130:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Driedzic WR (2015) Rainbow smelt: the unusual case of cryoprotection by sustained glycerol production in an aquatic animal. J Comp Physiol B 185:487–499

    Article  CAS  PubMed  Google Scholar 

  • Driedzic WR, Sidell BD, Stewart JM, Johnston IA (1990) Maximal activities of enzymes of energy metabolism in cephalopod systemic and branchial hearts. Physiol Zool 63:615–629

    Article  Google Scholar 

  • Fields JHA, Hochachka PW (1982) Glucose and proline metabolism in Nautilus. Pac Sci 36:337–341

    CAS  Google Scholar 

  • Fiorito G, Affuso A, Basil J, Cole A, de Girolamo P, D’Angelo L, Dickel L et al (2015) Guidelines for the care and welfare of cephalopods in research—a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab Anim 49(2 suppl):1–90

    Article  PubMed  Google Scholar 

  • Foster GD, Moon TW (1991) Hypometabolism with fasting in the yellow perch (Perca flavescens): a study of enzymes, hepatocyte metabolism, and tissue size. Physiol Zool 64:259–275

    Article  CAS  Google Scholar 

  • Gabr HR, Hanlon RT, Hanafy MH, El-Etreby SG (1999) Reproductive versus somatic tissue allocation in the cuttlefish Sepia dollfusi Adam (1941). Bull Mar Sci 65:159–173

    Google Scholar 

  • Gibson DM, Harris RA (2002) Metabolic regulation in mammals. Taylor Francis, London

    Google Scholar 

  • Grigoriou P, Richardson CA (2009) Effect of body mass, temperature and food deprivation on oxygen consumption rate of common cuttlefish Sepia officinalis. Mar Biol 156:2473–2481

    Article  Google Scholar 

  • Hochachka PW (1995) Oxygen efficient design of cephalopod muscle metabolism. Mar Freshw Behav Physiol 25:61–67

    Article  Google Scholar 

  • Hochachka PW, Fields JHA (1982) Arginine, glutamate, and proline as substrates for oxidation and for glycogenesis in cephalopod tissues. Pac Sci 36:325–335

    CAS  Google Scholar 

  • Hochachka PW, Mommsen TP, Storey J, Storey KB, Johansen K, French CJ (1983) The relationship between arginine and proline metabolism in cephalopods. Mar Biol Lett 4:1–21

    CAS  Google Scholar 

  • Horio Y, Tanaka T, Taketoshi M, Uno T, Wada H (1988) Rat cytosolic aspartate aminotransferase: regulation of its mRNA and contribution to gluconeogenesis. J Biochem 103:805–808

    CAS  PubMed  Google Scholar 

  • Horst C, Becker W (1986) Nutritive medium chain triacylglycerols cause a rapid increase of ketone bodies in the hemolymph of Biomphalaria glabrata (Gastropoda: Pulmonata). Comp Biochem Physiol B 85:875–878

    Google Scholar 

  • Horst C, Becker W, Kemper A (1986) Short-term alterations of the ketone body content in the hemolymph of Biomphalaria glabrata (Gastropoda: Pulmonata). Comp Biochem Physiol B 84:555–557

    Google Scholar 

  • Islinger M, Cardoso MJR, Schrader M (2010) Be different—the diversity of peroxisomes in the animal kingdom. Biochim Biophys Acta Cell Res 1803(8):881–897

    Article  CAS  Google Scholar 

  • Laffel L (1999) Ketone bodies: a review of physiology, pathophysiology and application of monitoring to diabetes. Diabetes Metab Res Rev 15:412–426

    Article  CAS  PubMed  Google Scholar 

  • Lamarre SG, Ditlecadet D, McKenzie DJ, Bonnaud L, Driedzic WR (2012) Mechanisms of protein degradation in mantle muscle and proposed gill remodeling in starved Sepia officinalis. Am J Physiol Reg Integr Comp Physiol 303:R427–R437

    Article  CAS  Google Scholar 

  • Lamarre S, Macmillan L, Morrow GP, Randell E, Pongnopparat T, Brosnan ME, Brosnan JT (2014) An isotope-dilution, GC–MS assay for formate and its application to human and animal metabolism. Amino Acids 46:1885–1891

    Article  CAS  PubMed  Google Scholar 

  • Lamarre SG, MacCormack TJ, Sykes A, Speers-Roesch B, Callaghan NI, Driedzic WR (2016) Metabolic rate and rates of protein turnover in food deprived cuttlefish, Sepia officinalis (Linnaeus 1758). ​Am J Physiol Reg Integr Comp Physiol. doi:10.1152/ajpregu.00459.2015

    Google Scholar 

  • Lee PG (1995) Nutrition of cephalopods: fueling the system. Mar Freshw Behav Physiol 25:35–51

    Article  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156:1–18

    Article  Google Scholar 

  • McMurray CH, Blanchflower WJ, Rice DA (1984) Automated kinetic method for d-3-hydroxybutyrate in plasma or serum. Clin Chem 30:421–425

    CAS  PubMed  Google Scholar 

  • Metón I, Mediavilla D, Caseras A, Cantó E, Fernández F, Baanante IV (1999) Effect of diet composition and ration size on key enzyme activities of glycolysis–gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br J Nutr 82:223–232

    PubMed  Google Scholar 

  • Meyer R, Becker W, Klimkewitz M (1986) Investigations on the ketone body metabolism in Biomphalaria glabrata: influence of starvation and of infection with Schistosoma mansoni. J Comp Physiol B 156:563–571

    Article  CAS  Google Scholar 

  • Moltschaniwskyj N, Johnston D (2006) Evidence that lipid can be digested by the dumpling squid Euprymna tasmanica, but is not stored in the digestive gland. Mar Biol 149:565–572

    Article  CAS  Google Scholar 

  • Mommsen TP, Hochachka PW (1981) Respiratory and enzymatic properties of squid heart mitochondria. Eur J Biochem 120:345–350

    Article  CAS  PubMed  Google Scholar 

  • Mommsen TP, Ballantyne J, MacDonald D, Gosline J, Hochachka PW (1981) Analogues of red and white muscle in squid mantle. Proc Natl Acad Sci 78:3274–3278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mommsen TP, Hochachka PW, French CJ (1983) Metabolism of arginine, proline, and ornithine in tissues of the squid, Illex illecebrosus. Can J Zool 61:1835–1846

    Article  CAS  Google Scholar 

  • Moon TW, Johnston IA (1980) Starvation and the activities of glycolytic and gluconeogenic enzymes in skeletal muscles and liver of the plaice, Pleuronectes platessa. J Comp Physiol 136:31–38

    Article  CAS  Google Scholar 

  • Morillo-Velarde PS, Valverde JC, Serra Llinares RM, García BG (2013) Changes in lipid composition of different tissues of common octopus (Octopus vulgaris) during short-term starvation. Aquacult Res 44:1177–1189

    Article  CAS  Google Scholar 

  • Moyes CD, Suarez RK, Hochachka PW, Ballantyne JS (1990) A comparison of fuel preferences of mitochondria from vertebrates and invertebrates. Can J Zool 68:1337–1349

    Article  Google Scholar 

  • Navarro JC, Monroig O, Sykes AV (2014) Nutrition as a key factor for cephalopod aquaculture. In: Iglesias J, Fuentes L, Villanueva R (eds) Cephalopod culture. Springer, New York, pp 77–95

    Chapter  Google Scholar 

  • Newsholme EA, Crabtree B (1986) Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. J Exp Zool 239:159–167

    Article  CAS  PubMed  Google Scholar 

  • O’Dor RK, Webber DM (1986) The constraints on cephalopods: why squid aren’t fish. Can J Zool 64:1591–1605

    Article  Google Scholar 

  • O’Dor RK, Mangold K, Boucher-Rodoni R, Wells MJ, Wells J (1984) Nutrient absorption, storage and remobilization in Octopus vulgaris. Mar Behav Physiol 11:239–258

    Article  Google Scholar 

  • Pande SV, Lee TS, Murthy MS (1990) Freeze-thawing causes masking of membrane-bound outer carnitine palmitoyltransferase activity: implications for studies on carnitine palmitoyltransferases deficiency. BBA Lipid Lipid Met 1044:262–268

    Article  CAS  Google Scholar 

  • Pilkis SJ, El-Maghrabi MR, Claus TH (1988) Hormonal regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Biochem 57:755–783

    Article  CAS  PubMed  Google Scholar 

  • Robinson AM, Williamson DH (1980) Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiol Rev 60:143–187

    CAS  PubMed  Google Scholar 

  • Robison B, Seibel B, Drazen J (2014) Deep-sea octopus (Graneledone boreopacifica) conducts the longest-known egg-brooding period of any animal. PLoS One 9:e103437

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosa R, Pereira J, Nunes ML (2005) Biochemical composition of cephalopods with different life strategies, with special reference to a giant squid, Architeuthis sp. Mar Biol 146:739–751

    Article  CAS  Google Scholar 

  • Secor SM, Carey HV (2016) Integrative physiology of fasting. Compr Physiol 6:773–825

    Article  PubMed  Google Scholar 

  • Seibel BA, Hochberg FG, Carlini DB (2000) Life history of Gonatus onyx (Cephalopoda: Teuthoidea): deep-sea spawning and post-spawning egg care. Mar Biol 137:519–526

    Article  Google Scholar 

  • Semmens JM (1998) An examination of the role of the digestive gland of two loliginid squids, with respect to lipid: storage or excretion? Proc Roy Soc Lond B 265:1685–1690

    Article  CAS  Google Scholar 

  • Sidell BD, Driedzic WR, Stowe DB, Johnston IA (1987) Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol Zool 60:221–232

    Article  Google Scholar 

  • Speers-Roesch B, Treberg JR (2010) The unusual energy metabolism of elasmobranch fishes. Comp Biochem Physiol A 155:417–434

    Article  Google Scholar 

  • Stewart JM, Brass ME, Carlin RC, Black H (1992) Maximal enzyme activities of energy production pathways in the heart, hepatopancreas, and white muscle of the giant scallop (Placopecten magellanicus) and lobster (Homarus americanus). Can J Zool 70:720–724

    Article  CAS  Google Scholar 

  • Stio M, Vanni P, Pinzauti G (1988) A continuous spectrophotometric assay for the enzymatic marker glucose 6-phosphatase. Anal Biochem 174:32–37

    Article  CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (1979) Octopine metabolism in the cuttlefish, Sepia officinalis: octopine production by muscle and its role as an aerobic substrate for non-muscular tissues. J Comp Physiol 131:311–319

    Article  CAS  Google Scholar 

  • Storey KB, Storey JM (1983) Carbohydrate metabolism in cephalopod molluscs. In: Hochachka PW, Wilbur KM (eds) The mollusca, vol 1. Academic Press, New York, pp 91–136

    Google Scholar 

  • Storey KB, Storey JM, Johansen K, Hochachka PW (1979) Octopine metabolism in Sepia officinalis: effect of hypoxia and metabolite loads on the blood levels of octopine and related compounds. Can J Zool 57:2331–2336

    Article  CAS  Google Scholar 

  • Stuart JA, Ballantyne JS (1996) Correlation of environment and phylogeny with the expression of β-hydroxybutyrate dehydrogenase in the mollusca. Comp Biochem Physiol B 114:153–160

    Article  Google Scholar 

  • Suarez RK (2012) Energy and metabolism. Compr Physiol 2:2527–2540

    PubMed  Google Scholar 

  • Sykes AV, Domingues P, Andrade JP (2014) Sepia officinalis. In: Iglesias J, Fuentes L, Villanueva R (eds) Cephalopod culture. Springer, New York, pp 175–204

    Chapter  Google Scholar 

  • Voogt PA (1983) Lipids: their distribution and metabolism. In: Hochachka PW, Wilbur KM (eds) The mollusca, vol 1. Academic Press, New York, pp 329–370

    Google Scholar 

  • Weber JM (2011) Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214:286–294

    Article  CAS  PubMed  Google Scholar 

  • Wells MJ, Clarke A (1996) Energetics: the costs of living and reproducing for an individual cephalopod. Phil Trans R Soc B 351:1083–1104

    Article  Google Scholar 

  • Yang J, Kalhan SC, Hanson RW (2009) What is the metabolic role of phosphoenolpyruvate carboxykinase? J Biol Chem 284:27025–27029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zammit VA, Beis A, Newsholme EA (1979) The role of 3-oxo acid-CoA transferase in the regulation of ketogenesis in the liver. FEBS Lett 103:212–215

    Article  CAS  PubMed  Google Scholar 

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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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Authors and Affiliations

  1. Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Ben Speers-Roesch & William R. Driedzic

  2. Department of Biology, Mount Allison University, Sackville, NB, Canada

    Neal I. Callaghan & Tyson J. MacCormack

  3. Département de Biologie, Université de Moncton, Moncton, NB, Canada

    Simon G. Lamarre

  4. CCMAR, Centro de Ciências do Mar do Algarve, Campus de Gambelas, Universidade do Algarve, Faro, Portugal

    Antonio V. Sykes

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  1. Ben Speers-Roesch
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  2. Neal I. Callaghan
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  4. Simon G. Lamarre
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  6. William R. Driedzic
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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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