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Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration
Diatoms are unicellular algae characterized by silica cell walls. These silica elements are known to be formed intracellularly in membrane-bound silica deposition vesicles and exocytosed after completion. How diatoms maintain membrane homeostasis during the exocytosis of these large and rigid silica...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886994/ https://www.ncbi.nlm.nih.gov/pubmed/36717559 http://dx.doi.org/10.1038/s41467-023-36112-z |
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author | de Haan, Diede Aram, Lior Peled-Zehavi, Hadas Addadi, Yoseph Ben-Joseph, Oz Rotkopf, Ron Elad, Nadav Rechav, Katya Gal, Assaf |
author_facet | de Haan, Diede Aram, Lior Peled-Zehavi, Hadas Addadi, Yoseph Ben-Joseph, Oz Rotkopf, Ron Elad, Nadav Rechav, Katya Gal, Assaf |
author_sort | de Haan, Diede |
collection | PubMed |
description | Diatoms are unicellular algae characterized by silica cell walls. These silica elements are known to be formed intracellularly in membrane-bound silica deposition vesicles and exocytosed after completion. How diatoms maintain membrane homeostasis during the exocytosis of these large and rigid silica elements remains unknown. Here we study the membrane dynamics during cell wall formation and exocytosis in two model diatom species, using live-cell confocal microscopy, transmission electron microscopy and cryo-electron tomography. Our results show that during its formation, the mineral phase is in tight association with the silica deposition vesicle membranes, which form a precise mold of the delicate geometrical patterns. We find that during exocytosis, the distal silica deposition vesicle membrane and the plasma membrane gradually detach from the mineral and disintegrate in the extracellular space, without any noticeable endocytic retrieval or extracellular repurposing. We demonstrate that within the cell, the proximal silica deposition vesicle membrane becomes the new barrier between the cell and its environment, and assumes the role of a new plasma membrane. These results provide direct structural observations of diatom silica exocytosis, and point to an extraordinary mechanism in which membrane homeostasis is maintained by discarding, rather than recycling, significant membrane patches. |
format | Online Article Text |
id | pubmed-9886994 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-98869942023-02-01 Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration de Haan, Diede Aram, Lior Peled-Zehavi, Hadas Addadi, Yoseph Ben-Joseph, Oz Rotkopf, Ron Elad, Nadav Rechav, Katya Gal, Assaf Nat Commun Article Diatoms are unicellular algae characterized by silica cell walls. These silica elements are known to be formed intracellularly in membrane-bound silica deposition vesicles and exocytosed after completion. How diatoms maintain membrane homeostasis during the exocytosis of these large and rigid silica elements remains unknown. Here we study the membrane dynamics during cell wall formation and exocytosis in two model diatom species, using live-cell confocal microscopy, transmission electron microscopy and cryo-electron tomography. Our results show that during its formation, the mineral phase is in tight association with the silica deposition vesicle membranes, which form a precise mold of the delicate geometrical patterns. We find that during exocytosis, the distal silica deposition vesicle membrane and the plasma membrane gradually detach from the mineral and disintegrate in the extracellular space, without any noticeable endocytic retrieval or extracellular repurposing. We demonstrate that within the cell, the proximal silica deposition vesicle membrane becomes the new barrier between the cell and its environment, and assumes the role of a new plasma membrane. These results provide direct structural observations of diatom silica exocytosis, and point to an extraordinary mechanism in which membrane homeostasis is maintained by discarding, rather than recycling, significant membrane patches. Nature Publishing Group UK 2023-01-30 /pmc/articles/PMC9886994/ /pubmed/36717559 http://dx.doi.org/10.1038/s41467-023-36112-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article de Haan, Diede Aram, Lior Peled-Zehavi, Hadas Addadi, Yoseph Ben-Joseph, Oz Rotkopf, Ron Elad, Nadav Rechav, Katya Gal, Assaf Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
title | Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
title_full | Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
title_fullStr | Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
title_full_unstemmed | Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
title_short | Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
title_sort | exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886994/ https://www.ncbi.nlm.nih.gov/pubmed/36717559 http://dx.doi.org/10.1038/s41467-023-36112-z |
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