The highly efficient holding function of the mollusc ‘catch’ muscle is not based on decelerated myosin head cross-bridge cycles

Abstract

Certain smooth muscles are able to reduce energy consumption greatly when holding without shortening. For instance, this is the case with muscles surrounding blood vessels used for regulating blood flow and pressure. The phenomenon is most conspicuous in 'catch' muscles of molluscs, which have been used as models for investigating this important physiological property of smooth muscle. When the shells of mussels are held closed, the responsible muscles enter the highly energy-efficient state of catch. According to the traditional view, the state of catch is caused by the slowing down of the force-generating cycles of the molecular motors, the myosin heads. Here, we show that catch can still be induced and maintained when the myosin heads are prevented from generating force. This new evidence proves that the long-held explanation of the state of catch being due to the slowing down of force producing myosin head cycles is not valid and that the highly economic holding state is caused by the formation of a rigid network of inter-myofilament connections based on passive molecular structures.

Plasticity of foot muscle and cardiac thermal limits in the limpet Lottia limatula from locations with differing temperatures

“…The limpet foot is a complicated muscular structure which is not as functionally reliant on aerobic metabolism as cardiac muscle. The limpet foot mechanism uses energetically economic smooth muscles to lock into the 'catch' state, which clamps the foot into suction with the substrate (Frescura & Hodgson 1990, Smith 1991, Galler et al 2010. Compared to cardiac tissue, limpet foot muscles have low mitochondrial density and high anaerobic capacities (Marshall & McQuaid 1989, Morley et al 2009, Suda et al 2015).…”

The antipredator benefits of postural camouflage in peppered moth caterpillars

“…While these postures may at first appear associated with energetically-costly muscular activity, it is also possible that in some species they consume little if any extra energy. Certain smooth muscles, known as catch muscles, are able to reduce energy consumptions when holding fixed postures 28 . Catch muscles have not, to our knowledge, been found in lepidopteran larvae, and little is known about their use in maintaining defensive postures.…”

“…While there is only limited empirical evidence that postural camouflage has an antipredator benefit, intraspecific variation in this behavior has received even less attention. If postural camouflage is associated with energetic costs (which is not necessarily the case 28 , but seems to be true of other forms of defensive posture 29 ), then we might expect posture to be influenced by environmental conditions that impact an individual’s state. Here we exploit natural variation in the tendency of American peppered moth larvae to utilize twig-like postures (see SI experiment 2 ) to test whether naïve avian predators take longer to find and attack larvae when they are in these postures than when they are not (i.e., whether they benefit from postural camouflage).…”

Effect of Oxygen-Limiting Tidal Conditions on Muscle Metabolism and Structure in the Giant Acorn Barnacle, Balanus nubilus

“…Ultrastructural evidence that muscles from barnacles share these catch-like properties has been documented previously (Hoyle, 1987). If this is also true for (Cohen, 1982;Galler et al, 2010). The giant muscle cells of B. nubilus may therefore represent a highly functional, primeval mash-up of both striated and smooth muscle, which may confer their impressive contractile abilities in the face of low oxygen availability.…”

“…All of these characteristics suggest that contraction in these fibers is powered aerobically, which is paradoxical given the fact that they remain contracted for long-periods of time while the scutal and tergal plates are closed, and oxygen levels are presumably low. This sustained opercular closure ability under potential hypoxia may be explained by the use of a 'catch' state in giant barnacle fibers, similar to that seen in molluscan muscles and to a lesser extent in vertebrate smooth muscle (Southwood, 1983;Galler et al, 2010).…”