Intracellular morphogenesis of diatom silica is guided by local variations in membrane curvature

• Published in: Nature communications Vol. 15; no. 1; pp. 7888 - 11
• Main Authors: Aram, Lior, de Haan, Diede, Varsano, Neta, Gilchrist, James B., Heintze, Christoph, Rotkopf, Ron, Rechav, Katya, Elad, Nadav, Kröger, Nils, Gal, Assaf
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 10.09.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 101/28; 147/143; 631/535/1258/1260; 631/57/2270; 639/301/54/991; 704/829/826; Algae; Biological effects; Biological properties; Cell Membrane - metabolism; Cell Wall - metabolism; Cell Wall - ultrastructure; Cell walls; Cryoelectron Microscopy; Curvature; Diatoms - growth & development; Diatoms - metabolism; Diatoms - ultrastructure; Electron Microscope Tomography; Humanities and Social Sciences; Intracellular; Marine microorganisms; Membranes; Mineralization; Morphogenesis; multidisciplinary; Plasma membranes; Science; Science (multidisciplinary); Self-assembly; Silica; Silicon dioxide; Silicon Dioxide - chemistry; Silicon Dioxide - metabolism; Tethering
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-52211-x

Silica cell-wall formation in diatoms is a showcase for the ability of organisms to control inorganic mineralization. The process of silicification by these unicellular algae is tightly regulated within a membrane-bound organelle, the silica deposition vesicle (SDV). Two opposing scenarios were proposed to explain the tight regulation of this intracellular process: a template-mediated process that relies on preformed scaffolds, or a template-independent self-assembly process. The present work points to a third scenario, where the SDV membrane is a dynamic mold that shapes the forming silica. We use in-cell cryo-electron tomography to visualize the silicification process in situ, in its native-state, and with a nanometer-scale resolution. This reveals that the plasma membrane interacts with the SDV membrane via physical tethering at membrane contact sites, where the curvature of the tethered side of the SDV membrane mirrors the intricate silica topography. We propose that silica growth and morphogenesis result from the biophysical properties of the SDV and plasma membranes. The silica cell wall of unicellular algae has intricate architecture unattainable by current technology. In this work it is shown that membrane contact sites are the biological morphogenesis handles to shape such intracellular mineralization.