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

Lior Aram; Diede de Haan; Neta Varsano; James B. Gilchrist; Christoph Heintze; Ron Rotkopf; Katya Rechav; Nadav Elad; Nils Kröger; Assaf Gal

doi:10.1038/s41467-024-52211-x

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

Lior Aram, Diede de Haan, Neta Varsano, James B. Gilchrist, Christoph Heintze, Ron Rotkopf, Katya Rechav, Nadav Elad, Nils Kröger, Assaf Gal^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

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.

Original language	English
Article number	7888
Journal	Nature Communications
Volume	15
DOIs	https://doi.org/10.1038/s41467-024-52211-x
Publication status	Published - 10 Sept 2024

Funding

We are grateful to Yael Shilderman for the image analysis work, as well as Tobias Fürstenhaupt (MPI-CBG Dresden, Germany) for help with cryoTEM analysis of extracted valve SDV. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No. 848339). We acknowledge Diamond for access and support of the cryo-EM facilities at the UK National Electron Bio-Imaging Center (eBIC), proposal BI29609, funded by the Wellcome Trust, MRC, and BBSRC. The work was supported by the Deutsche Forschungsgemeinschaft (DFG) through grants KR1853/8-2 (to N.K.) in the framework of Research Unit 2038 (NANOMEE). This research received support from the Irving and Cherna Moskowitz Center for Nano and Bio-Imaging. D.dH. was supported by the Sustainability and Energy Research Initiative (SAERI) of Weizmann Institute of Science. Publisher Copyright: © The Author(s) 2024.

All Science Journal Classification (ASJC) codes

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/s41467-024-52211-xLicence: CC BY

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title = "Intracellular morphogenesis of diatom silica is guided by local variations in membrane curvature",

abstract = "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.",

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AU - Varsano, Neta

AU - Gilchrist, James B.

AU - Heintze, Christoph

AU - Rotkopf, Ron

AU - Rechav, Katya

AU - Elad, Nadav

AU - Kröger, Nils

AU - Gal, Assaf

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AB - 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.

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

Abstract

Funding

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