Algorithmic construction of topologically complex biomineral lattices via cellular syncytia

Abstract

Biomineralization is ubiquitous in both unicellular and multicellular living systems [1, 2] and has remained elusive due to a limited understanding of physicochemical and biomolecular processes [3]. Echinoderms, identified with diverse architectures of calcite-based structures in the dermis[4], present an enigma of how cellular processes control shape and form of individual structures. Specifically, in holothurians (sea cucumbers), multi-cellular clusters construct discrete single-crystal calcite ossicles ([~] 100 {micro}m length scale), with diverse morphologies both across species and even within an individual animal [5]. The local rules that might encode these unique morphologies in calcite ossicles in holothurians remain largely unknown. Here we show how transport processes in a cellular syncytium impart a top-down control on ossicle geometry via symmetry breaking, branching, and fusion in finite cellular clusters. As a unique example of cellular masonary, we show how coordination within a small cluster of cells builds calcite structures about an order of magnitude larger than any individual participating cell. We establish live imaging of ossicle growth in Apostichopus parvimensis juveniles revealing how individual crystalline seeds ([~] 1 - 2 {micro}m) grow inside a multi-cellular syncytial complex with the biomineral completely wrapped within a membrane-bound cytoplasmic sheath. Constructing a topological description of ossicle geometries from 3D micro-CT (computational tomography) data reveals the hidden growth history and conserved patterns across ossicle types. We further demonstrate vesicle transport on the surface of the ossicle, rather than cell motility, regulates material transport to the ossicle tips via a unique cytoskeletal architecture. Finally, using reduced order models of conserved transport on self-closing active branching networks, we highlight the hidden universality in the growth process of distinct ossicles. The system presented here serves as a unique playground merging top-down cellular physiology and classical branching morphogenesis [6] with bottom-up non-equilibrium mineralization [7] processes at the interface of living and non-living matter [8].