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Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora

Unicellular euglyphid testate amoeba Paulinella micropora with filose pseudopodia secrete approximately 50 siliceous scales into the extracellular template-free space to construct a shell isomorphic to that of its mother cell. This shell-constructing behavior is analogous to building a house with br...

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Autores principales: Nomura, Mami, Ohta, Keisuke, Nishigami, Yukinori, Nakayama, Takuro, Nakamura, Kei-Ichiro, Tadakuma, Kenjiro, Galipon, Josephine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507277/
https://www.ncbi.nlm.nih.gov/pubmed/37731817
http://dx.doi.org/10.3389/fcell.2023.1232685
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author Nomura, Mami
Ohta, Keisuke
Nishigami, Yukinori
Nakayama, Takuro
Nakamura, Kei-Ichiro
Tadakuma, Kenjiro
Galipon, Josephine
author_facet Nomura, Mami
Ohta, Keisuke
Nishigami, Yukinori
Nakayama, Takuro
Nakamura, Kei-Ichiro
Tadakuma, Kenjiro
Galipon, Josephine
author_sort Nomura, Mami
collection PubMed
description Unicellular euglyphid testate amoeba Paulinella micropora with filose pseudopodia secrete approximately 50 siliceous scales into the extracellular template-free space to construct a shell isomorphic to that of its mother cell. This shell-constructing behavior is analogous to building a house with bricks, and a complex mechanism is expected to be involved for a single-celled amoeba to achieve such a phenomenon; however, the three-dimensional (3D) structure of the shell and its assembly in P. micropora are still unknown. In this study, we aimed to clarify the positional relationship between the cytoplasmic and extracellular scales and the structure of the egg-shaped shell in P. micropora during shell construction using focused ion beam scanning electron microscopy (FIB-SEM). 3D reconstruction revealed an extensive invasion of the electron-dense cytoplasm between the long sides of the positioned and stacked scales, which was predicted to be mediated by actin filament extension. To investigate the architecture of the shell of P. micropora, each scale was individually segmented, and the position of its centroid was plotted. The scales were arranged in a left-handed, single-circular ellipse in a twisted arrangement. In addition, we 3D printed individual scales and assembled them, revealing new features of the shell assembly mechanism of P. micropora. Our results indicate that the shell of P. micropora forms an egg shape by the regular stacking of precisely designed scales, and that the cytoskeleton is involved in the construction process.
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spelling pubmed-105072772023-09-20 Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora Nomura, Mami Ohta, Keisuke Nishigami, Yukinori Nakayama, Takuro Nakamura, Kei-Ichiro Tadakuma, Kenjiro Galipon, Josephine Front Cell Dev Biol Cell and Developmental Biology Unicellular euglyphid testate amoeba Paulinella micropora with filose pseudopodia secrete approximately 50 siliceous scales into the extracellular template-free space to construct a shell isomorphic to that of its mother cell. This shell-constructing behavior is analogous to building a house with bricks, and a complex mechanism is expected to be involved for a single-celled amoeba to achieve such a phenomenon; however, the three-dimensional (3D) structure of the shell and its assembly in P. micropora are still unknown. In this study, we aimed to clarify the positional relationship between the cytoplasmic and extracellular scales and the structure of the egg-shaped shell in P. micropora during shell construction using focused ion beam scanning electron microscopy (FIB-SEM). 3D reconstruction revealed an extensive invasion of the electron-dense cytoplasm between the long sides of the positioned and stacked scales, which was predicted to be mediated by actin filament extension. To investigate the architecture of the shell of P. micropora, each scale was individually segmented, and the position of its centroid was plotted. The scales were arranged in a left-handed, single-circular ellipse in a twisted arrangement. In addition, we 3D printed individual scales and assembled them, revealing new features of the shell assembly mechanism of P. micropora. Our results indicate that the shell of P. micropora forms an egg shape by the regular stacking of precisely designed scales, and that the cytoskeleton is involved in the construction process. Frontiers Media S.A. 2023-09-04 /pmc/articles/PMC10507277/ /pubmed/37731817 http://dx.doi.org/10.3389/fcell.2023.1232685 Text en Copyright © 2023 Nomura, Ohta, Nishigami, Nakayama, Nakamura, Tadakuma and Galipon. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Nomura, Mami
Ohta, Keisuke
Nishigami, Yukinori
Nakayama, Takuro
Nakamura, Kei-Ichiro
Tadakuma, Kenjiro
Galipon, Josephine
Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora
title Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora
title_full Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora
title_fullStr Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora
title_full_unstemmed Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora
title_short Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora
title_sort three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba paulinella micropora
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507277/
https://www.ncbi.nlm.nih.gov/pubmed/37731817
http://dx.doi.org/10.3389/fcell.2023.1232685
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