Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm
ABSTRACT: The eukaryotic flagellum propels sperm cells and simultaneously detects physical and chemical cues that modulate the waveform of the flagellar beat. Most previous studies have characterized the flagellar beat and swimming trajectories in two space dimensions (2D) at a water/glass interfac...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer Berlin Heidelberg
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8249298/ https://www.ncbi.nlm.nih.gov/pubmed/34196906 http://dx.doi.org/10.1140/epje/s10189-021-00076-z |
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author | Gong, A. Rode, S. Gompper, G. Kaupp, U. B. Elgeti, J. Friedrich, B. M. Alvarez, L. |
author_facet | Gong, A. Rode, S. Gompper, G. Kaupp, U. B. Elgeti, J. Friedrich, B. M. Alvarez, L. |
author_sort | Gong, A. |
collection | PubMed |
description | ABSTRACT: The eukaryotic flagellum propels sperm cells and simultaneously detects physical and chemical cues that modulate the waveform of the flagellar beat. Most previous studies have characterized the flagellar beat and swimming trajectories in two space dimensions (2D) at a water/glass interface. Here, using refined holographic imaging methods, we report high-quality recordings of three-dimensional (3D) flagellar bending waves. As predicted by theory, we observed that an asymmetric and planar flagellar beat results in a circular swimming path, whereas a symmetric and non-planar flagellar beat results in a twisted-ribbon swimming path. During swimming in 3D, human sperm flagella exhibit torsion waves characterized by maxima at the low curvature regions of the flagellar wave. We suggest that these torsion waves are common in nature and that they are an intrinsic property of beating axonemes. We discuss how 3D beat patterns result in twisted-ribbon swimming paths. This study provides new insight into the axoneme dynamics, the 3D flagellar beat, and the resulting swimming behavior. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version supplementary material available at 10.1140/epje/s10189-021-00076-z. |
format | Online Article Text |
id | pubmed-8249298 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Springer Berlin Heidelberg |
record_format | MEDLINE/PubMed |
spelling | pubmed-82492982021-07-20 Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm Gong, A. Rode, S. Gompper, G. Kaupp, U. B. Elgeti, J. Friedrich, B. M. Alvarez, L. Eur Phys J E Soft Matter Regular Article - Living Systems ABSTRACT: The eukaryotic flagellum propels sperm cells and simultaneously detects physical and chemical cues that modulate the waveform of the flagellar beat. Most previous studies have characterized the flagellar beat and swimming trajectories in two space dimensions (2D) at a water/glass interface. Here, using refined holographic imaging methods, we report high-quality recordings of three-dimensional (3D) flagellar bending waves. As predicted by theory, we observed that an asymmetric and planar flagellar beat results in a circular swimming path, whereas a symmetric and non-planar flagellar beat results in a twisted-ribbon swimming path. During swimming in 3D, human sperm flagella exhibit torsion waves characterized by maxima at the low curvature regions of the flagellar wave. We suggest that these torsion waves are common in nature and that they are an intrinsic property of beating axonemes. We discuss how 3D beat patterns result in twisted-ribbon swimming paths. This study provides new insight into the axoneme dynamics, the 3D flagellar beat, and the resulting swimming behavior. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version supplementary material available at 10.1140/epje/s10189-021-00076-z. Springer Berlin Heidelberg 2021-07-01 2021 /pmc/articles/PMC8249298/ /pubmed/34196906 http://dx.doi.org/10.1140/epje/s10189-021-00076-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Regular Article - Living Systems Gong, A. Rode, S. Gompper, G. Kaupp, U. B. Elgeti, J. Friedrich, B. M. Alvarez, L. Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
title | Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
title_full | Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
title_fullStr | Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
title_full_unstemmed | Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
title_short | Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
title_sort | reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm |
topic | Regular Article - Living Systems |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8249298/ https://www.ncbi.nlm.nih.gov/pubmed/34196906 http://dx.doi.org/10.1140/epje/s10189-021-00076-z |
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