Hybrid Motility Mechanism of Sperm at the Viscoelastic Fluid-Solid Interface

Shobitha Unnikrishnan¹, Robert L. Scott¹, Emmanuel Ogundele¹, Mohammad A. Azad², Kenta Ishimoto³, Susan S. Suarez⁴, Chih K. Kuan Tung¹

Abstract Text:

Sperm motility is critical in assessing its fertilization potential, yet the precise mechanisms by which they propel themselves in the complex environment of the female reproductive tract remains incompletely understood. To reach the egg, mammalian sperm must move through the female reproductive tract, often encountering narrow passages generally filled with viscoelastic fluids such as cervical mucus and oviductal fluid that influence their motility. This study investigated the motility mechanism of bull sperm at the interface of viscoelastic fluid and a solid boundary, revealing how flagellum-surface interactions enhance propulsion in complex environments. We used a microfluidic device filled with a 1% methylcellulose solution dissolved in Tyrode's albumin lactate pyruvate (TALP) to simulate the fluid environment of the bovine female reproductive tract. Using high-speed imaging, we visualized the flagellum interaction with surfaces in the microfluidic device. The side-view visualization of sperm interacting with the solid surface revealed that the flagellum remained close to the surface, while the kinetic friction between the flagellum and the surface acted in the direction of sperm movement, providing thrust. The flagellar contact points exhibited backward sliding motion as the head progressed, suggesting that kinetic friction contributes to forward propulsion. The flagellar contacts with the walls moved backward at a significantly faster rate than the forward motion of the head (31 ± 2 μm/s vs. 28 ± 2 μm/s,p < 0.0001, paired t-test, n=21, notably, in every pair analyzed, the flagellar contact moved faster than the head). Measurements from side-view imaging showed that the flagellum consistently formed bends with an amplitude of around 2 µm at the surface (ANOVA comparing the three different bends showed no significant difference, p=0.195, n=18). The measured amplitude demonstrates that in confined spaces of similar dimensions (~2 µm, which is the thickness of the sperm head), such as the utero tubal junction filled with viscoelastic fluid, sperm may generate thrust via kinetic friction from both sidewalls. To understand the role of fluid in sperm propulsion, we measured the flow field around moving sperm in the same solution embedded with tracer particles. Our flow field generated by motile sperm shares features characteristic of an idealized pusher swimmer, but only when tracer particles come in contact with the sperm were included in our analysis. This observation suggests slippage between the viscoelastic fluid and the solid surface, deviating from the no-slip boundary typically used in standard fluid dynamics models. These observations point to hybrid motility mechanisms in sperm, where sperm gains additional thrust from flagellum-surface interaction while the flagellum pushes the fluid, as in conventional swimming. Our future work will investigate how this sperm-surface interaction, combined with a soft surface, affects sperm propulsion. Our ongoing studies also explore sperm motility across different species to understand different strategies sperm adopt to move through different reproductive environments. The insights from this study contribute to a broader understanding of the adaptive motility strategies mammalian sperm use to move through the confined, complex environment of the female reproductive tract. Understanding how sperm interact with their natural environment during their journey to the egg is critical to improving infertility assessments, developing novel treatment strategies, and new sperm selection methods for assisted reproduction.NIH 1R15HD095411-01 and NSF Grant DMR-2144064.