Uniaxial orientation of β-chitin nanofibres used as an organic framework in the scales of a hot vent snail

Author:

Isobe Noriyuki1ORCID,Chen Chong2ORCID,Daicho Kazuho3ORCID,Saito Tsuguyuki3ORCID,Bissessur Dass4,Takai Ken2ORCID,Okada Satoshi2ORCID

Affiliation:

1. Biogeochemistry Research Center, Research Institute for Marine Resources Utilization (MRU), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan

2. Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-STAR), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan

3. Department of Biomaterial Sciences, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan

4. Department for Continental Shelf, Maritime Zones Administration and Exploration, Prime Minister's Office, 2nd Floor, Belmont House, 12 Intendance Street, Port Louis 11328, Mauritius

Abstract

Organisms use various forms and orientations of chitin nanofibres to make structures with a wide range of functions, from insect wings to mussel shells. Lophotrochozoan animals such as snails and annelid worms possess an ancient ‘biomineralization toolkit’, enabling them to flexibly and rapidly evolve unique hard parts. The scaly-foot snail is a gastropod endemic to deep-sea hydrothermal vents, unique in producing dermal sclerites used as sites of sulfur detoxification. Once considered to be strictly proteinaceous, recent data pointed to the presence of chitin in these sclerites, but direct evidence is still lacking. Here, we show that β-chitin fibres (approx. 5% of native weight) are indeed the building framework, through a combination of solid-state nuclear magnetic resonance spectroscopy, wide-angle X-ray diffraction, and electron microscopy. The fibres are uniaxially oriented, likely forming a structural basis for column-like channels into which the scaly-foot snail is known to actively secrete sulfur waste—expanding the known function of chitinous hard parts in animals. Our results add to the existing evidence that animals are capable of modifying and co-opting chitin synthesis pathways flexibly and rapidly, in order to serve novel functions during their evolution.

Funder

Japan Society for the Promotion of Science

Publisher

The Royal Society

Subject

Biomedical Engineering,Biochemistry,Biomaterials,Bioengineering,Biophysics,Biotechnology

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