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

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 Ṁ O 2 is used to support protein synthesis in mantle, while the cost of protein synthesis (50 μmol O 2 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.

The mechanical properties of the mantle muscle of European cuttlefish (Sepia officinalis)

“…The isometric tetanic stress of cuttlefish muscle (88 kN m −2 in juveniles and 144 kN m −2 in adults) is within the same range as previously reported values for this species (104±18 kN m −2 in juveniles: Lamarre et al, 2019 ; and 226±19 kN m −2 in adults: Milligan et al, 1997 ). Twitch stress (70 and 84 kN m −2 ) and tetanic stress were also similar to those of other species of mollusc; e.g.…”

“…Characterisation of the contractile properties of cephalopod muscle has been limited to measurements during isometric and isotonic contractions, in squid (longfin squid, Doryteuthis pealeii : Thompson et al, 2010 , 2008 ; European common squid, Alloteuthis subulata : Milligan et al, 1997 ; Rogers et al, 1997 ), and European common cuttlefish ( Sepia officinalis : Curtin et al, 2000 ; Milligan et al, 1997 ; Rogers et al, 1997 ), and has mostly focused upon mature animals (but see Thompson et al, 2010 ; Lamarre et al, 2019 ), with little work addressing whether changes occur throughout ontogeny ( Thompson et al, 2010 ). However, during jet propulsion swimming, the mantle muscle contracts intermittently, undergoing a cyclical length change during which power is generated, which is rather different to muscle behaviour during isometric and isotonic contractions ( Caiozzo, 2002 ; Josephson, 1993 ).…”

Food availability modulates the combined effects of ocean acidification and warming on fish growth

“…Trypsin is necessary for protein hydrolysis but the production of this enzyme requires the activation of machinery for cellular protein production. This activation represents another energetic demand 70 in addition to the energy already invested to exchange ions and release bicarbonate. This additional energetic cost may be difficult to cover for fish persistently experiencing restricted feeding conditions.…”