Mechanism of branching morphogenesis inspired by diatom silica formation

Abstract

The silica-based cell walls of diatoms are prime examples of genetically controlled, species-specific mineral architectures. The physical principles underlying morphogenesis of their hierarchically structured silica patterns are not understood, yet such insight could indicate novel routes towards synthesizing functional inorganic materials. Recent advances in imaging nascent diatom silica allow rationalizing possible mechanisms of their pattern formation. Here, we combine theory and experiments on the model diatom Thalassiosira pseudonana to put forward a minimal model of branched rib patterns - a fundamental feature of the silica cell wall. We quantitatively recapitulate the time-course of rib pattern morphogenesis by accounting for silica biochemistry with autocatalytic formation of diffusible silica precursors followed by conversion into solid silica. We propose that silica deposition releases an inhibitor that slows down up-stream precursor conversion, thereby implementing a self-replicating reaction-diffusion system featuring a non-classical Turing mechanism. The proposed mechanism highlights the role of geometrical cues for guided self-organization, rationalizing the instructive role for the single initial pattern seed known as primary silicification site. The mechanism of branching morphogenesis that we characterize here is possibly generic and may apply also in other biological systems. Significance statementThe formation of minerals by living organisms is a widespread biological phenomenon occurring throughout the evolutionary tree-of-life. The silica-based cell walls of diatom microalgae are impressive examples featuring intricate architectures and outstanding materials properties that still defy their reconstitution in vitro. Here, we developed a minimal mathematical model that explains the formation of branched patterns of silica ribs, providing unprecedented understanding of basic physico-chemical processes capable of guiding silica morphogenesis in diatoms. The generic mechanism of branching morphogenesis identified here could provide recipes for bottom-up synthesis of mineral-nanowire networks for technological applications. Moreover, similar mechanisms may apply in the biological morphogenesis of other branched structures, like corals, bacterial colonies, tracheal networks, fungal plexuses, or the vascular system.