The argonaut constructs its shell via physical self-organization and coordinated cell sensorial activity

Abstract

Summary The shell of the cephalopod Argonauta consists of two layers of fibers that elongate perpendicular to the shell surfaces. Fibers have a high-Mg calcitic core sheathed by thin organic membranes (>100 nm) and configurate a polygonal network in cross section. Their evolution has been studied by serial sectioning with electron microscopy-associated techniques. During growth, fibers with small cross-sectional areas shrink, whereas those with large sections widen. It is proposed that fibers evolve as an emulsion between the fluid precursors of both the mineral and organic phases. When polygons reach big cross-sectional areas, they become subdivided by new membranes. To explain both the continuation of the pattern and the subdivision process, the living cells from the mineralizing tissue must perform contact recognition of the previously formed pattern and subsequent secretion at sub-micron scale. Accordingly, the fabrication of the argonaut shell proceeds by physical self-organization together with direct cellular activity.

The unique fibrilar to platy nano- and microstructure of twinned rotaliid foraminiferal shell calcite

“…Shell formation through growth competition is not only observed for Rotaliida. It has been reported for the columnar layer of brachiopod shells 37 , for cephalopod shells 42 , 43 and for prismatic layers of euheterodont bivalves 44 . Structural characteristics for shell growth through growth competition are well observable for the calcite of P. obliquiloculata , for the shell layer between the POS and the outer shell surface.…”

Wet shells and dry tales: the evolutionary ‘Just-So’ stories behind the structure–function of biominerals

“…Interface 19: 20220336 the shell thickness begin as spherulites within the organicsrich layer (figure 1g) that grow outwards in conical clusters. Though the ultrastructure, crystallography and geochemistry of the shell have been previously investigated [40][41][42][43][44][45][46], the mechanics of the shell are, to our knowledge, unexplored beyond notes of the shell being fairly flexible when wet [38]. The unique construction of the argonaut shell, with a large central organics-rich layer, and the relative simplicity of the organization of the mineral structure compared to Nautilus make for an interesting comparison between the two architectures.…”

“…While nacre has a number of features that limit inter-tablet movement, such as nanoasperities, mineral bridges and dove tailing [ 60 , 61 ], these reinforcing mechanisms were not observed in the prismatic ultrastructure nor the argonaut ultrastructure. Furthermore, the organic phase in the nautilid shell is largely spread throughout thin lamellae in nacre, whereas in the argonaut shell, it is concentrated in relatively large volumes, both in between crystal units [ 45 ] and at the centre of the shell ( figure 1 g ). These characteristics likely permit a relatively large deformability of the argonaut shell at the macro-scale compared to nacre that has a fairly limited range of motion regardless of the properties of the organic phase.…”

The unique nano- and microstructure of twinned foraminiferal shell calcite

“…For other shelled organisms shell fabrication through growth competition is not as dominant as it is for rotaliid shells. It is, however, reported for the columnar layer of brachiopod shells 26 , for the formation of cephalopod shells 53,23 and for prismatic layers of euheterodont bivalves 54 .…”