Bilaterally Asymmetric Helical Myofibrils in Ascidian Tadpole Larvae

Koichi Matsuo; Ryota Tamura; Kohji Hotta; Mayu Okada; Akihisa Takeuchi; Yanlin Wu; Koh Hashimoto; Hidekazu Takano; Atsushi Momose; Atsuo Nishino

doi:10.3389/fcell.2021.800455

Bilaterally Asymmetric Helical Myofibrils in Ascidian Tadpole Larvae

Front Cell Dev Biol. 2021 Dec 7:9:800455. doi: 10.3389/fcell.2021.800455. eCollection 2021.

Authors

Koichi Matsuo¹, Ryota Tamura², Kohji Hotta³, Mayu Okada¹, Akihisa Takeuchi⁴, Yanlin Wu⁵, Koh Hashimoto⁵, Hidekazu Takano⁵, Atsushi Momose⁵, Atsuo Nishino⁶

Affiliations

¹ Laboratory of Cell and Tissue Biology, Keio University School of Medicine, Tokyo, Japan.
² Department of Neurosurgery, Keio University School of Medicine, Tokyo, Japan.
³ Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Yokohama, Japan.
⁴ Japan Synchrotron Radiation Research Institute (JASRI), Sayo, Japan.
⁵ Institute of Multidisciplinary Research for Advanced Materials, Tohoku University, Sendai, Japan.
⁶ Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan.

Abstract

The locomotor system is highly bilateral at the macroscopic level. Homochirality of biological molecules is fully compatible with the bilateral body. However, whether and how single-handed cells contribute to the bilateral locomotor system is obscure. Here, exploiting the small number of cells in the swimming tadpole larva of the ascidian Ciona, we analyzed morphology of the tail at cellular and subcellular scales. Quantitative phase-contrast X-ray tomographic microscopy revealed a high-density midline structure ventral to the notochord in the tail. Muscle cell nuclei on each side of the notochord were roughly bilaterally aligned. However, fluorescence microscopy detected left-right asymmetry of myofibril inclination relative to the longitudinal axis of the tail. Zernike phase-contrast X-ray tomographic microscopy revealed the presence of left-handed helices of myofibrils in muscle cells on both sides. Therefore, the locomotor system of ascidian larvae harbors symmetry-breaking left-handed helical cells, while maintaining bilaterally symmetrical cell alignment. These results suggest that bilateral animals can override cellular homochirality to generate the bilateral locomotor systems at the supracellular scale.

Keywords: Ciona robusta; bilateral symmetry; cellular homochirality; left-handed helix; left-right asymmetry; muscle cell; myofibrils; synchrotron radiation.