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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2023.1232685/full |
| _version_ | 1827825373457416192 |
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| author | Mami Nomura Keisuke Ohta Keisuke Ohta Yukinori Nishigami Yukinori Nishigami Takuro Nakayama Kei-Ichiro Nakamura Kei-Ichiro Nakamura Kenjiro Tadakuma Kenjiro Tadakuma Josephine Galipon Josephine Galipon Josephine Galipon Josephine Galipon |
| author_facet | Mami Nomura Keisuke Ohta Keisuke Ohta Yukinori Nishigami Yukinori Nishigami Takuro Nakayama Kei-Ichiro Nakamura Kei-Ichiro Nakamura Kenjiro Tadakuma Kenjiro Tadakuma Josephine Galipon Josephine Galipon Josephine Galipon Josephine Galipon |
| author_sort | Mami Nomura |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-12T02:49:08Z |
| format | Article |
| id | doaj.art-61aa460a045e4a6c82bc3287438be3d1 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-03-12T02:49:08Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-61aa460a045e4a6c82bc3287438be3d12023-09-04T06:01:52ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2023-09-011110.3389/fcell.2023.12326851232685Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella microporaMami Nomura0Keisuke Ohta1Keisuke Ohta2Yukinori Nishigami3Yukinori Nishigami4Takuro Nakayama5Kei-Ichiro Nakamura6Kei-Ichiro Nakamura7Kenjiro Tadakuma8Kenjiro Tadakuma9Josephine Galipon10Josephine Galipon11Josephine Galipon12Josephine Galipon13Faculty of Science, Yamagata University, Yamagata, JapanDivision of Microscopic and Developmental Anatomy, Department of Anatomy, Kurume University School of Medicine, Kurume, JapanAdvanced Imaging Research Center, Kurume University School of Medicine, Kurume, JapanGraduate School of Life Science, Hokkaido University, Sapporo, JapanResearch Institute for Electronic Science, Hokkaido University, Sapporo, JapanCenter for Computational Sciences, University of Tsukuba, Tsukuba, JapanDivision of Microscopic and Developmental Anatomy, Department of Anatomy, Kurume University School of Medicine, Kurume, JapanAdvanced Imaging Research Center, Kurume University School of Medicine, Kurume, JapanGraduate School of Information Sciences, Tohoku University, Sendai, JapanTough Cyberphysical AI Research Center, Tohoku University, Sendai, JapanGraduate School of Information Sciences, Tohoku University, Sendai, JapanInstitute for Advanced Sciences, Keio University, Tsuruoka, Japan0Graduate School of Media and Governance, Keio University, Fujisawa, Japan1Graduate School of Science and Engineering, Yamagata University, Yonezawa, JapanUnicellular 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.https://www.frontiersin.org/articles/10.3389/fcell.2023.1232685/fulltestate amoebashell formationFIB-SEM3D reconstruction3D printerPaulinella |
| spellingShingle | Mami Nomura Keisuke Ohta Keisuke Ohta Yukinori Nishigami Yukinori Nishigami Takuro Nakayama Kei-Ichiro Nakamura Kei-Ichiro Nakamura Kenjiro Tadakuma Kenjiro Tadakuma Josephine Galipon Josephine Galipon Josephine Galipon Josephine Galipon Three-dimensional architecture and assembly mechanism of the egg-shaped shell in testate amoeba Paulinella micropora Frontiers in Cell and Developmental Biology testate amoeba shell formation FIB-SEM 3D reconstruction 3D printer Paulinella |
| 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 | testate amoeba shell formation FIB-SEM 3D reconstruction 3D printer Paulinella |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2023.1232685/full |
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