Abstract
Cnidaria is an animal phylum, whose members probably have the most ancestral musculature. We prepared and characterized, for the first time to our knowledge, native actomyosin from the striated myoepithelium of the adult moon jelly Aurelia sp. The actomyosin contained myosin, paramyosin-like protein, Ser/Thr-kinase, actin, and two isoforms of tropomyosin, but not troponin, which is known to activate contraction dependent on intracellular Ca2+ signaling in almost all striated muscles of bilaterians. Notably, the myosin comprised striated muscle-type heavy chain and smooth muscle-type regulatory light chains. In the presence of Ca2+, the Mg-ATPase activity of actomyosin was stimulated and Ser21 of the regulatory light chain was concomitantly phosphorylated by the addition of calmodulin and myosin light chain kinase prepared from chicken smooth muscle. Collectively, these results suggest that, similar to smooth muscle, the contraction of jellyfish striated muscle is regulated by Ca2+-dependent phosphorylation of the myosin light chain.
Highlights
The contraction and relaxation of musculature are regulated by cytosolic Ca2+ concentrations
The sessile polyp of the moon jelly Aurelia shows transverse segmentation, termed strobilation, which gives rise to many free-swimming larvae called ephyrae. The ephyrae develop both radial and circular striated muscles for swimming11,12. -Each ephyra grows into a mature medusa, which has smooth muscles in its tentacles, oral arms, and the marginal region of the subumbrella, as well as striated myofibrils that are arranged concentrically and form a muscular sheet in the subumbrella, the rhythmic contraction of which generates pulsation for swimming[10,13,14]
The striated myofibrils structurally resemble those of vertebrate skeletal muscles; that is, the sarcomere, which comprises interdigitating thick and thin filaments sandwiched between Z-discs, is longitudinally repeated[11,15,16,17]
Summary
The absence of troponin indicates that there is likely to be another machinery for the Ca2+-dependent regulation of contraction in jellyfish striated muscle. It is important to elucidate the ancestral regulatory mechanisms of cnidarian muscle contraction in order to understand the evolution of muscles in the animal kingdom. There have been no reports about the biochemical properties of muscular proteins from jellyfish, probably because both the large amount of gelatinous components and the protease released from the animal’s gastric cavity into its whole body interfere with purification of these proteins. We prepared and characterized for the first time the native actomyosin from jellyfish striated muscle to investigate the Ca2+-dependent regulation of muscular contraction in this species
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