title: 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.
authors.affiliation: Department of Ocean Sciences, Memorial University of Newfoundland, St. John's, NL, A1C 5S7, Canada. bspeersr@gmail.com.
authors.forename: Ben
authors.initials: B
authors.lastname: Speers-Roesch
authors.affiliation: Department of Biology, Mount Allison University, Sackville, NB, Canada.
authors.forename: Neal I
authors.initials: NI
authors.lastname: Callaghan
authors.affiliation: Department of Biology, Mount Allison University, Sackville, NB, Canada.
authors.forename: Tyson J
authors.initials: TJ
authors.lastname: MacCormack
authors.affiliation: Département de Biologie, Université de Moncton, Moncton, NB, Canada.
authors.forename: Simon G
authors.initials: SG
authors.lastname: Lamarre
authors.affiliation: CCMAR, Centro de Ciências do Mar do Algarve, Campus de Gambelas, Universidade do Algarve, Faro, Portugal.
authors.forename: Antonio V
authors.initials: AV
authors.lastname: Sykes
authors.affiliation: Department of Ocean Sciences, Memorial University of Newfoundland, St. John's, NL, A1C 5S7, Canada.
authors.forename: William R
authors.initials: WR
authors.lastname: Driedzic
mesh_terms: D000596:Amino Acids / Q000378:metabolism; D000818:Animals; D001219:Aspartate Aminotransferases / Q000378:metabolism; D002950:Citrate (si)-Synthase / Q000378:metabolism; D049832:Decapodiformes / Q000378:metabolism*; D004734:Energy Metabolism; D005227:Fatty Acids / Q000378:metabolism; D006597:Fructose-Bisphosphatase / Q000378:metabolism; D041981:Gastrointestinal Tract / Q000378:metabolism; D005943:Gluconeogenesis; D005947:Glucose / Q000378:metabolism; D005952:Glucose-6-Phosphatase / Q000378:metabolism; D006019:Glycolysis; D007657:Ketone Bodies / Q000378:metabolism; D019764:Phosphoenolpyruvate Carboxykinase (ATP) / Q000378:metabolism; D013217:Starvation / Q000378:metabolism; D014280:Triglycerides / Q000378:metabolism
chemical_list: D000596:Amino Acids; D005227:Fatty Acids; D007657:Ketone Bodies; D014280:Triglycerides; D002950:Citrate (si)-Synthase; D001219:Aspartate Aminotransferases; D006597:Fructose-Bisphosphatase; D005952:Glucose-6-Phosphatase; D019764:Phosphoenolpyruvate Carboxykinase (ATP); D005947:Glucose
keywords: Amino acid; Cephalopod; Digestive gland; Energy metabolism; Enzyme activity; Fasting; Gluconeogenesis; Glucose; Glycolysis; Ketone body; Lipid; Metabolic fuel preference; Starvation