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...

Descripción completa

Detalles Bibliográficos
Autores principales: Gong, A., Rode, S., Gompper, G., Kaupp, U. B., Elgeti, J., Friedrich, B. M., Alvarez, L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2021
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
_version_ 1783716885151350784
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
work_keys_str_mv AT gonga reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm
AT rodes reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm
AT gompperg reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm
AT kauppub reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm
AT elgetij reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm
AT friedrichbm reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm
AT alvarezl reconstructionofthethreedimensionalbeatpatternunderlyingswimmingbehaviorsofsperm