Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Abstract

To determine the metabolic response to food deprivation, cuttlefish (Sepia officinalis) juveniles were either fed, fasted (3 to 5 days food deprivation), or starved (12 days food deprivation). Fasting resulted in a decrease in triglyceride levels in the digestive gland, and after 12 days, these lipid reserves were essentially depleted. Oxygen consumption was decreased to 53% and NH4 excretion to 36% of the fed group following 3-5 days of food deprivation. Oxygen consumption remained low in the starved group, but NH4 excretion returned to the level recorded for fed animals during starvation. The fractional rate of protein synthesis of fasting animals decreased to 25% in both mantle and gill compared with fed animals and remained low in the mantle with the onset of starvation. In gill, however, protein synthesis rate increased to a level that was 45% of the fed group during starvation. In mantle, starvation led to an increase in cathepsin A-, B-, H-, and L-like enzyme activity and a 2.3-fold increase in polyubiquitin mRNA that suggested an increase in ubiquitin-proteasome activity. In gill, there was a transient increase in the polyubiquitin transcript levels in the transition from fed through fasted to the starved state and cathepsin A-, B-, H-, and L-like activity was lower in starved compared with fed animals. The response in gill appears more complex, as they better maintain rates of protein synthesis and show no evidence of enhanced protein breakdown through recognized catabolic processes.

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

“…In systemic heart, HK activity was maintained at fed Data are mean ± SEM, n = 7-8. These data were previously published in Lamarre et al (2016) levels following short-starvation (two-way ANOVA, p > 0.05), but decreased by 28 % following longstarvation (two-way ANOVA, p < 0.05). HK activity in branchial heart was not measured in short-starved individuals, but following long-starvation levels were decreased by 21 % compared with fed controls (t test, p < 0.01).…”

“…This general response is consistent with radiolabel and other studies in cephalopods that have suggested that a mix of metabolic fuels is used during early starvation, followed by a greater reliance upon lipids and amino acids in order to conserve carbohydrate stores (digestive gland glycogen is limited; mantle glycogen is reserved for fueling locomotion), and finally a large reliance upon amino acids once lipid stores are exhausted (O'Dor et al 1984;Castro et al 1992;Lamarre et al 2012). In fact, the responses of the ammonia quotient of our study animals suggested a transitory shift to lipid catabolism during short starvation and then to protein catabolism after long starvation, when triacylglycerol became depleted (Lamarre et al 2016). Layered upon the general response in cuttlefish was a tissue-specific response in which metabolic capacity in digestive gland and mantle appeared to be shut down more than in gill or systemic heart.…”

“…Mantle, the largest tissue in cephalopods (~30-40 % of body mass in cuttlefish; Gabr et al 1999), showed decreases in many enzyme activities after long starvation (e.g. CPT, CS, G3PDH, HK, PFK, ODH), possibly resulting from starvation-induced decreases in protein synthesis (Lamarre et al 2016). Conversely, enzymatic capacities in gill and systemic heart were largely unaffected even after long-starvation, aside from the decreased glycolytic capacity, suggesting a greater conservation of metabolism, sustained primarily by lipidbased and amino acid fuels.…”

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

“…This suggests that the higher mitochondrial density in the livers of fasted trout may be an adaptive component of the metabolic response to food deprivation (Secor & Carey, 2016). However, our results clearly show that the reduction in the total "number" of hepatic mitochondria drives a decrease in liver total oxygen requirements, and presumably partly explains the reduction of whole-body metabolism that occurs in response to food shortage Lamarre et al, 2016;Monternier et al, 2014).…”

Reversion to developmental pathways underlies rapid arm regeneration in juvenile European cuttlefish, Sepia officinalis (Linnaeus 1758)

“…Animals were then incubated for 1.5 hr in darkened containers bubbled with air. These conditions were shown to respect the assumptions of the flooding dose assay in this species (Lamarre et al, 2016). After this incorporation period, the animals were killed as previously described, and the treatment and reference arms from each animal were excised and flash-frozen in liquid nitrogen for further analysis.…”