Characterization of paramyosin and thin filaments in the smooth muscle of acorn worm, a member of hemichordates

Abstract

Paramyosin is a myosin-binding protein characteristic of invertebrate animals, while troponin is a Ca-dependent regulator of muscle contraction. Both proteins are widely distributed in protostomes, while in deuterostomes, their distribution is limited; namely, presence of paramyosin and absence of troponin are common features in echinoderm muscles, while muscles of chordates contain troponin but lack paramyosin. In this study, we examined the muscle of a hemichordate, acorn worm, to clarify whether this animal is like echinoderms or like the other deuterostome animals. We found a 100-kDa protein in the smooth muscle of acorn worm. This protein was identified with paramyosin, since the purified protein formed paracrystals with a constant axial periodicity in the presence of divalent cations as paramyosin of other animals, showed ability to interact with myosin and shared common antigenicity with echinoderm paramyosin. On the other hand, troponin band was not detected in isolated thin filaments, and the filaments increased myosin-ATPase activity in a Ca-independent manner. The results indicate that troponin is lacking in thin filaments of acorn worm muscle just as in those of echinoderms. The muscle of hemichordate acorn worm is quite similar to echinoderm muscles, but different from chordate muscles.

Deuterostome Genomics: Lineage-Specific Protein Expansions That Enabled Chordate Muscle Evolution

“…Biochemical analyses suggest the existence of tropomyosin in muscles of a sea lily (Echinodermata) ( Obinata et al. 2014 ) and an acorn worm (Hemichordata) ( Sonobe et al. 2016 ).…”

“…2017 ) genes was observed in circumesophageal muscle of sea urchin, and the function of tropomyosin gene (Sakowv30041361 in supplementary fig. S2 C , Supplementary Material online) is suggested in acorn worm muscle via biochemical analysis ( Sonobe et al. 2016 ).…”

Troponin-I is present as an essential component of muscles in echinoderm larvae

“…Like echinoderms, hemichordates have been reported to have no troponin complex 6 . However, TnT and TnC are computationally predicted in the genome of Saccoglossus kowalevskii .…”

“…Ca 2+ signaling, troponin regulation and actomyosin contraction—the input, the mediator, and the output, respectively—are well conserved in almost all bilaterians 3 . However, it has been reported that echinoderms and hemichordates, collectively termed Ambulacraria, lack all components of the troponin complex, which is composed of Troponin-I (TnI), Troponin-T (TnT), and Troponin-C (TnC), thus raising the question of how the troponin systems emerged in the ancestors of bilaterians and how they evolved in the deuterostomes 4 5 6 . One possibility that has been suggested is that Ambulacraria has simply lost the troponin complex and uses another regulatory system, such as direct Ca 2+ binding to myosin 6 7 .…”

“…However, it has been reported that echinoderms and hemichordates, collectively termed Ambulacraria, lack all components of the troponin complex, which is composed of Troponin-I (TnI), Troponin-T (TnT), and Troponin-C (TnC), thus raising the question of how the troponin systems emerged in the ancestors of bilaterians and how they evolved in the deuterostomes 4 5 6 . One possibility that has been suggested is that Ambulacraria has simply lost the troponin complex and uses another regulatory system, such as direct Ca 2+ binding to myosin 6 7 . However, the genomic sequencing of Strongylocentrotus purpuratus has revealed incomplete troponin candidate genes 8 9 , thus leading us to reconsider whether echinoderms have the troponin complex.…”