Effect of flagellar beating pattern on sperm rheotaxis and boundary-dependent navigation

Abstract

7The study of navigational mechanisms used by mammalian sperm inside a microenvironment 8 yields better understanding of sperm locomotion during the insemination process, which aids in 9 the design of tools for overcoming infertility. Near-and far-field hydrodynamic interactions with 10 nearby boundaries and rheotaxis are known to be some of the steering strategies that keep sperm 11 on the correct path toward the egg. However, it is not known how the beating patterns of sperm 12 may influence these navigational strategies. In this study, we investigate the effect of flagellar 13 beating pattern on navigation of sperm cells both theoretically and experimentally using a two-14 step approach. We first isolate bovine sperm based on their rheotactic behavior in a zone with 15 quiescent medium using a microfluidic system. This step ensures that the swimmers are able to 16 navigate upstream and have motilities higher than a selected value, even though they feature 17 various flagellar beating patterns. We then explore the flagellar beating pattern of these isolated 18 sperm and their subsequent influence on boundary-dependent navigation. Our findings indicate 19 that rheotaxis enables sperm to navigate upstream even in the presence of circular motion in their 20 motility, whereas boundary-dependent navigation is more sensitive to the circular motion and 21 selects for progressive motility. This finding may explain the clinical importance of progressive 23 the sperm cells throughout the process of insemination. 24 Keywords: Mammalian sperm | Navigation | Rheotaxis | Boundary-dependent navigation | 25 Progressive motility 26 Significance 27Finding the egg and moving toward it while traversing the complex structure of the female 28 reproductive tract is necessary for mammalian sperm. Previous studies have shown how sperm use 29 navigational steering mechanisms that are based on swimming upstream (i.e. rheotaxis) and along 30 the boundaries of the female reproductive tract. We demonstrate that the performance of theses 31 navigational mechanisms is associated with the primary characteristics of sperm motility. In fact, 32 sperm rheotaxis is more sensitive to the motility and thus average velocity of sperm while 33 navigation via rigid boundaries is more sensitive to the flagellar beating pattern and selects for 34 symmetric beating. Our results can be expanded to other autonomous microswimmers and their 35 subsequent navigation mechanisms. 36 37 38 39 40 41 42 43 48which vary among different species. For instance, marine plants and animals (10, 11) release their 49 gametes into the sea, where chemotactic behavior is observed (4,(11)(12)(13). Strikingly, the role of 50 this chemical communication observed in marine invertebrate sperm (which is reminiscent of 51 bacterial chemotaxis (14)) is uncertain in the navigation of mammalian sperm (13,(15)(16)(17)(18)(19). In 52 contrast, in vitro/vivo evidence suggests that the navigation of mammalian sperm within the female 53 reproductive tract depends more on fluid mechanical c...

Phenotyping single-cell motility in microfluidic confinement

“…This provides a distinct route towards a chiral nonequilibrium steady-state that has not been reported previously, since CR-like swimmers roaming inside circular traps with constant curvature were suggested to be incapable of producing flux loops on average [25]. This discrepancy highlights the importance of further particulars of cell shape and/or swimming mechanism [29,54,55,56]. Further experimental and modelling e↵orts are currently underway to resolve these microswimmer-boundary interactions [57], including the role of cilia mechanosensitivity [14].…”

Phenotyping single-cell motility in microfluidic confinement

“…This provides a distinct route towards a chiral nonequilibrium steady-state that has not been reported previously, since CR-like swimmers roaming inside circular traps with constant curvature were suggested to be incapable of producing flux loops on average [25]. This discrepancy highlights the importance of further particulars of cell shape and/or swimming mechanism [29, 54, 55, 56]. Further experimental and modelling efforts are currently underway to resolve these microswimmer-boundary interactions [57], including the role of cilia mechanosensitivity [14].…”