Biogenic Crystallographically Continuous Aragonite Helices: The Microstructure of the Planktonic Gastropod Cuvierina

Abstract

The pteropod Cuvierina constructs very lightweight, thin, flexible, and resistant shells with the most unusual microstructure: densely packed, continuous crystalline aragonite fibers that coil helically around axes perpendicular to the shell surface. The high degree of fiber intergrowth results in a particular interlocking structure. The shell is constructed by guided self‐assembly, outside the animal's soft body. A prerequisite to understand its formation is to resolve the underlying crystallographic building principle. This is basic in order to use this hierarchically structured and highly functional biomaterial as inspiration for the production of new materials. It teaches us about the optimization of structures over millions of years of evolution under strict consideration of energetic costs and efficient use of available resources and materials. We have described how helical coiling proceeds by using a combination of diffraction and imaging techniques, which complement at different levels of resolution. Despite their curling, the fibers are continuously crystalline and show a preferred crystallographic growth direction. When the latter can no more be maintained due to the imposed curving, abrupt changes across twins permit to continue growth in the desired direction. This is a nice example of how crystallographically continuous fibers can grow helically.

Biological strategy for the fabrication of highly ordered aragonite helices: the microstructure of the cavolinioidean gastropods

“…In general, the helix angle is noticeably smaller for the first turn (12–15°) and later increases (to 25°–30°) towards the shell interior 1 13 ( Fig. 1a , Supplementary Figs S2 and S7 ).…”

“…Little can be added to the detailed descriptions of Bé et al 1 and subsequent authors 2 6 11 12 13 about the general morphology of the fibres. In all the species examined, the fibres invariably coil dextrally.…”

“…1a , Supplementary Fig. S2 ) 1 12 13 . When the fibres can be seen curving in fractures parallel to the shell surface ( Fig.…”

“…Previous crystallographic studies 6 11 12 have shown that the c -axes of the aragonite crystals are strictly aligned with the coiling axes of the evenly aligned helical fibres. Recently, it has been shown that the crystals in Cuvierina are also relatively well aligned in the a - b plane and that they tend to grow preferentially along the projection of the b -axis on the fibre axis 13 . When this preferential crystallographic growth direction substantially departs from the actual growth direction of the fibre due to the permanent curling, abrupt changes in the orientation of the a - and b -axes across {110} twins permit growth to continue in the desired direction 13 .…”

“…Recently, it has been shown that the crystals in Cuvierina are also relatively well aligned in the a - b plane and that they tend to grow preferentially along the projection of the b -axis on the fibre axis 13 . When this preferential crystallographic growth direction substantially departs from the actual growth direction of the fibre due to the permanent curling, abrupt changes in the orientation of the a - and b -axes across {110} twins permit growth to continue in the desired direction 13 . This study evidences that this is the mechanism by which fibres adapt their crystallography to helical growth and not vice-versa, i.e.…”