Morphogenesis of the diamond-type stereom microlattice and the origin of saddle-shaped minimal surfaces in the echinoderm skeleton
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Echinoderm endoskeleton has a unique trabecular microstructure known as stereom, which can exhibit highly ordered geometries. A particularly striking example of these geometries is the recently discovered “diamond-type” stereom, characterized by a diamond triply periodic minimal surface (D-TPMS) geometry and distinguished by its exceptional mechanical and structural properties. Despite its promising features for engineering applications, the morphogenesis of this microarchitecture remains poorly understood, notably due to its uniqueness in the natural world. Here, we applied a multimodal imaging and labeling approach to investigate the developmental processes underlying the formation of the diamond-type stereom in adults of a starfish species Protoreaster nodosus . We showed that this stereom type develops through two principal marginal growth patterns: trabecular trifurcation, which generates successive, horizontally spreading layers and occurs on flat external plate surfaces oriented approximately along the crystallographic {111} planes of the D-TPMS; and trabecular bifurcation, typically occurring along the edges of external plates and in the regions between trifurcating zones, aligned with the crystallographic {100} planes of the D-TPMS lattice. Although these growth patterns may proceed at different rates, they are tightly coordinated, resulting in the coherent D-TPMS microarchitecture. Furthermore, we demonstrated that F-actin cytoskeletal activity is consistently associated with active biomineralization fronts (trabecular tips), regardless of whether the stereom is of the diamond-type or of a less ordered, galleried form. Notably, we also observed that the formation of lateral bridges between adjacent stereom trabeculae is often preceded by the appearance of catenoid-like F-actin structures, suggesting a guiding and templating role for the cytoskeleton in building trabecular connectivity and shaping its peculiar curvature profile. Given the structural conservation of saddle-like features across multiple stereom types, we hypothesize that such minimal surface geometries may emerge as a result of tension-driven cytoskeletal dynamics acting as a physical template during biomineralization. Our observations underscore the critical involvement of the cytoskeleton in adult echinoderm biomineralization, implying that cytoskeletal patterning may actively contribute to complex adult skeletal microarchitecture.
Statement of Significance
Triple periodic minimal surfaces (TPMS) are geometrically regular surfaces that extend periodically in three dimensions and locally minimize surface area by maintaining zero mean curvature. Among different TPMS structures, the diamond-type (D-TPMS) is particularly notable for its exceptional mechanical stability, uniform porosity, and minimal surface area-to-volume ratio. Although TPMS-like microarchitectures are not uncommon in nature, D-TPMS structures, with such exceptionally large lattice parameters (>10 µm), are exceedingly rare. One notable natural example of these is the stereom of certain echinoderms. However, the fundamental question of what governs the formation of such highly ordered microstructures remains unresolved. To investigate this, we applied a multi-modal labeling and imaging approach to elucidate the general principles of diamond-type stereom morphogenesis. This study not only provides the first insights into the growth dynamics of this unique microarchitecture, but also highlights the essential role of the cytoskeleton, particularly F-actin, in guiding trabecular connectivity and the emergence of minimal surface geometry, regardless of whether the stereom is regular (periodic in three dimensions) or not (non-periodic, with a more irregular arrangement of trabeculae).
