Rolling controls sperm navigation in response to the dynamic rheological properties of the environment

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Abstract

Mammalian sperm rolling around their longitudinal axes is a long-observed component of motility, but its function in the fertilization process, and more specifically in sperm migration within the female reproductive tract, remains elusive. While investigating bovine sperm motion under simple shear flow and in a quiescent microfluidic reservoir and developing theoretical and computational models, we found that rolling regulates sperm navigation in response to the rheological properties of the sperm environment. In other words, rolling enables a sperm to swim progressively even if the flagellum beats asymmetrically. Therefore, a rolling sperm swims stably along the nearby walls (wall-dependent navigation) and efficiently upstream under an external fluid flow (rheotaxis). By contrast, an increase in ambient viscosity and viscoelasticity suppresses rolling, consequently, non-rolling sperm are less susceptible to nearby walls and external fluid flow and swim in two-dimensional diffusive circular paths (surface exploration). This surface exploration mode of swimming is caused by the intrinsic asymmetry in flagellar beating such that the curvature of a sperm’s circular path is proportional to the level of asymmetry. We found that the suppression of rolling is reversible and occurs in sperm with lower asymmetry in their beating pattern at higher ambient viscosity and viscoelasticity. Consequently, the rolling component of motility may function as a regulatory tool allowing sperm to navigate according to the rheological properties of the functional region within the female reproductive tract.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. All data related to this paper are deposited in https://doi.org/10.5061/dryad.ngf1vhhtd

The following data sets were generated

1. Abbaspourrad A
2. et al
(2021) Data from: Rolling controls sperm navigation in response to the dynamic rheological properties of the environment
Dryad Digital Repository, doi:10.5061/dryad.ngf1vhhtd.

https://doi.org/10.5061/dryad.ngf1vhhtd

Article and author information

Author details

Meisam Zaferani

Department of Food Science, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.
Farhad Javi

Food Science, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.
Amir Mokhtare

Department of Food Science, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.
Peilong Li

Food Science, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.
Alireza Abbaspourrad

Food Science, Cornell University, Ithaca, United States

For correspondence
alireza@cornell.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5617-9220

Funding

Cornell University

Alireza Abbaspourrad

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.