The cuttlefish Sepia officinalis (Sepiidae, Cephalopoda) constructs cuttlebone from a liquid-crystal precursor

TL;DR

This study reveals that cuttlebone formation in Sepia officinalis involves a liquid-crystal precursor and self-organizing principles, providing insights into its complex structure and evolutionary homology.

Contribution

It demonstrates that the cuttlebone is assembled from a liquid-crystal precursor and viscous fingering, offering a new understanding of its biomineralization process.

Findings

Cuttlebone membranes are formed from nanofibre layers with a helical arrangement.

The organism secretes a chitin-protein complex that self-organizes as a cholesteric liquid crystal.

Pillars are formed by viscous fingering, linking structure to physical self-organization.

Abstract

Cuttlebone, the sophisticated buoyancy device of cuttlefish, is made of extensive superposed chambers that have a complex internal arrangement of calcified pillars and organic membranes. It has not been clear how this structure is assembled. We find that the membranes result from a myriad of minor membranes initially filling the whole chamber, made of nanofibres evenly oriented within each membrane and slightly rotated with respect to those of adjacent membranes, producing a helical arrangement. We propose that the organism secretes a chitin-protein complex, which self-organizes layer-by-layer as a cholesteric liquid crystal, whereas the pillars are made by viscous fingering. The liquid crystallization mechanism permits us to homologize the elements of the cuttlebone with those of other coleoids and with the nacreous septa and the shells of nautiloids. These results challenge our view of this ultra-light natural material possessing desirable mechanical, structural and biological properties, suggesting that two self-organizing physical principles suffice to understand its formation.