Flagellar ultrastructure suppresses buckling instabilities and enables mammalian sperm navigation in high-viscosity media

Abstract

<jats:p>Eukaryotic flagellar swimming is driven by a slender motile unit, the axoneme, which possesses an internal structure that is essentially conserved in a tremendous diversity of sperm. Mammalian sperm, however, which are internal fertilizers, also exhibit distinctive accessory structures that further dress the axoneme and alter its mechanical response. This raises the following two fundamental questions. What is the functional significance of these structures? How do they affect the flagellar waveform and ultimately cell swimming? Hence we build on previous work to develop a mathematical mechanical model of a virtual human sperm to examine the impact of mammalian sperm accessory structures on flagellar dynamics and motility. Our findings demonstrate that the accessory structures reinforce the flagellum, preventing waveform compression and symmetry-breaking buckling instabilities when the viscosity of the surrounding medium is increased. This is in agreement with previous observations of internal and external fertilizers, such as human and sea urchin spermatozoa. In turn, possession of accessory structures entails that the progressive motion during a flagellar beat cycle can be enhanced as viscosity is increased within physiological bounds. Hence the flagella of internal fertilizers, complete with accessory structures, are predicted to be advantageous in viscous physiological media compared with watery media for the fundamental role of delivering a genetic payload to the egg.</jats:p>

Human sperm uses asymmetric and anisotropic flagellar controls to regulate swimming symmetry and cell steering

“…The postulation of symmetric beating is, however, in contrast with the abundance of observations showing structural asymmetries within the flagellar scaffold (2,10,20,23,(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36). Asymmetric waves have been reported in murine spermatozoa (37,38), while a one-sided stroke is commonly observed in Chlamydomonas (23,(27)(28)(29).…”

The steering gaits of sperm

“…By contrast, males from internal fertilizers, such as mammals, deposit sperm in the complex female reproductive tract, where sperm interact with the boundary walls and must progress through the highly viscous mucus that lines the reproductive tract tissue [5]. It has been proposed that to deal with such high viscosities, human sperm, for instance, have developed additional structures that render their flagellum more stable to buckling [6]. Furthermore, progression through mucus, detachment from the epithelia and penetration of egg vestments are supported by hyperactive sperm motility, a transient vigorous motility pattern commonly observed across mammals [7].…”

The human sperm beats anisotropically and asymmetrically in 3D

“…8(a). This may find its origin on the ultrastructural complex reinforcing the axoneme in human sperm [10,12], represented in Fig. 8(b).…”

“…Asymmetric waveforms have also been reported in mammalian sperm, such as murine spermatozoa [3,4], while an asymmetric beating mode is a typical feature in the Chlamydomonas flagellum [5][6][7][8][9]. Whilst structural anisotropies are inherent to the mammalian sperm architecture [10][11][12], other sources of asymmetry are equally present at the molecular level, from asymmetric dynein activity [1,2,[13][14][15], to an ever growing number of asymmetric regulatory complexes [6,8,[16][17][18][19][20], including anisotropically localised membrane ion channel along the flagellum [17]. This is further augmented by external sources of asymmetry, such as the hydrodynamic influence of solid surfaces during for sperm boundary accumulation near to the coverslip [21][22][23].…”

“…As such, beating symmetry is the cornerstone of any comparative study on flagellar undulation [24,29,32], especially so while assessing symmetry-breaking events, such as in sperm capacitation, hyperactivation and buckling phenomena [18,19,[32][33][34]. Theoretical and computational models equally, and ubiquitously, invoke symmetry, ranging from flagellar kinematic models to structural mechanics and even motor control hypothesis [5,10,12,26,[35][36][37][38][39].…”