Interrelationship Between Contractility, Protein Synthesis and Metabolism in Mantle of Juvenile Cuttlefish (Sepia officinalis).

Simon G Lamarre,José P Andrade,Émilie Bourloutski,Neal I Callaghan,Tyson J Maccormack,William R Driedzic,Vanessa D Pinto,Antonio V Sykes

doi:10.3389/fphys.2019.01051

Abstract

Young juvenile cuttlefish (Sepia officinalis) can grow at rates as high as 12% body weight per day. How the metabolic demands of such a massive growth rate impacts muscle performance that competes for ATP is unknown. Here, we integrate aspects of contractility, protein synthesis, and energy metabolism in mantle of specimens weighing 1.1 g to lend insight into the processes. Isolated mantle muscle preparations were electrically stimulated and isometric force development monitored. Preparations were forced to contract at 3 Hz for 30 s to simulate a jetting event. We then measured oxygen consumption, glucose uptake and protein synthesis in the hour following the stimulation. Protein synthesis was inhibited with cycloheximide and glycolysis was inhibited with iodoacetic acid in a subset of samples. Inhibition of protein synthesis impaired contractility and decreased oxygen consumption. An intact protein synthesis is required to maintain contractility possibly due to rapidly turning over proteins. At least, 41% of whole animal ṀO2 is used to support protein synthesis in mantle, while the cost of protein synthesis (50 μmol O2 mg protein–1) in mantle was in the range reported for other aquatic ectotherms. A single jetting challenge stimulated protein synthesis by approximately 25% (2.51–3.12% day–1) over a 1 h post contractile period, a similar response to that which occurs in mammalian skeletal muscle. Aerobic metabolism was not supported by extracellular glucose leading to the contention that at this life stage either glycogen or amino acids are catabolized. Regardless, an intact glycolysis is required to support contractile performance and protein synthesis in resting muscle. It is proposed that glycolysis is needed to maintain intracellular ionic gradients. Intracellular glucose at approximately 3 mmol L–1 was higher than the 1 mmol L–1 glucose in the bathing medium suggesting an active glucose transport mechanism. Octopine did not accumulate during a single physiologically relevant jetting challenge; however, octopine accumulation increased following a stress that is sufficient to lower Arg-P and increase free arginine.

Highlights

Cephalopods have a short life span and a semelparous reproductive pattern which gives them the reputation of living in the “fast lane.” Early juvenile cuttlefish (Sepia officinalis) grow at a rate of up to 12% body mass per day (Sykes et al, 2006, 2014)
Force development during the initial hallmark challenge averaged a stress of 104 mN mm−2, in keeping with a previous study that reported peak contractile stress during tetanus of 226 mN mm−2 in similar preparations from S. officinalis of unknown but likely larger body mass, as animals were trawled off Plymouth, United Kingdom (Milligan et al, 1997)
The current experiments were terminated after approximately 70 min but in parallel experiments force development could be sustained for at least a further hour

Summary

Introduction

Cephalopods have a short life span and a semelparous reproductive pattern which gives them the reputation of living in the “fast lane.” Early juvenile cuttlefish (Sepia officinalis) grow at a rate of up to 12% body mass per day (Sykes et al, 2006, 2014). Jet propulsion is energetically inefficient relative to the undulatory swimming used by fish and perhaps the best demonstration of this is provided by O’Dor and Webber (1986), who determined that the net cost of transport (J Kg−1 m−1) is 3–4.5 times higher in squids compared to trout This means that in order to travel the same distance, cephalopod mantle muscles have to work much harder than fish swimming muscles. If rates of protein synthesis are already maximized to support growth in juvenile cuttlefish, frequent jetting events may require a redistribution of resources away from growth and toward recovery, prolonging the time to maturity If they do maintain scope to further increase rates of protein synthesis in the mantle muscle following a jetting event, it may impose yet another energetic demand on their already highly solicited aerobic metabolism

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Results

Conclusion