Flagellar hydrodynamics. A comparison between resistive-force theory and slender-body theory

Summary

This contribution reviews existing literature and some new own findings on teleost sperm motility and factors controlling it, emphasizing selected marine species. In marine teleosts with external fertilization (halibut, turbot, sea bass, hake, cod and tuna serving as examples), mainly the osmolality controls sperm motility: movement is activated by transfer from the seminal fluid into sea water, representing a large upward step in osmolality. The exception are flatfishes (such as halibut or turbot) where CO2 is responsible for flagellar immotility in seminal fluid. In all cases, the duration of motility is short and limited to minutes ranges due to partial exhaustion of the ATP energy and to increase of internal ionic concentration as suggested by studies with de-membranated/ATP reactivated flagellae. In this overview, we compare motility characteristics (percentage of active spermatozoa, velocity, linearity), flagellar waves parameters (wave length and amplitude, number of waves) and energy content (respiration and ATP concentration) within species where these data have been established. All parameters show a rapid decrease after activation; therefore progressive forward movement needed by the sperm to effectively reach the egg surface, is limited to a short initial period following activation. In two species (turbot and sea bass) the rapid decrease of sperm motility is reflected by a corresponding decrease of the fertilizing ability. Exposure to external environments (sea water) at activation also leads to local defects of the sperm flagella posing additional limitations on motility duration. However, minor flagellar damages as well as energetic exhaustion are reversible: after a resting period in a non-swimming solution at the end of the motility period, spermatozoa can be re-activated for a second motility period. From these results and from additional data obtained from de-membranated/ATP re-activated spermatozoa, a paradigm has been developed which establishes a link between external osmolality (sea water), internal ionic concentration and control of axonemal activity.

Studying sperm motility in marine fish: an overview on the state of the art

In the absence of glycolytic support, mammalian sperm derive their energy for motility from a densely packed array of mitochondria at the base of the flagellum known as the midpiece. Using data on the morphometric dimensions of over 200 mammalian species, we found that an allometric relationship exists between midpiece length (Lm) and flagellum length (Lf). Specifically, the length of the mid-piece varies approximately as the 3/2 power of the flagellar length although the proportionality constant is different for eutherian and marsupial sperm. In contrast, when we corrected for the fraction of the midpiece that was taken up by mitochondria, a single linear correlation between mitochondrial volume and flagellar length for all mammals was found. These allometric relationships were used along with basic flagellar hydrodynamic theories to establish a unifying equation that predicted flagellar frequencies for any mammalian sperm between 40 microns and 200 microns in length. These findings imply that, at least in mammals, the mechanisms for energy production and dissipation in sperm flagella are highly conserved.

Metabolic regulation in mammalian sperm: mitochondrial volume determines sperm length and flagellar beat frequency.

Bull sperm that had been extracted with 0.2% Triton X-100 could be reactivated with ATP, and their movement closely resembled the motion of intact live sperm. Their motility required the presence of ATP, magnesium, and a medium of suitable salt concentration and pH. When Triton-extracted bull sperm were digested briefly with trypsin at pH 9.0, they appeared to retain most of their normal structure, but subsequent exposure of the digested sperm to ATP caused a disintegration of the flagellar structure. Direct observation of this disintegration by light microscopy, using dark-field illumination, combined with an electron microscope study of preparations of the disintegrated sperm, demonstrated the presence of an active sliding mechanism of filament interaction in bull spermatozoa. Human sperm subjected to the same procedures showed similar patterns of reactivation and of

/pdf/adenosine-triphosphate-induced-motility-and-sliding-of-4augffb2b2.pdf

Adenosine triphosphate-induced motility and sliding of filaments in mammalian sperm extracted with Triton X-100.

on ejaculates from bullsdemonstratedthatspermatozoa in the presence of caffeine (6 mM) maintained the initial percentage of motility for at least 4 hr at 37C, whereas in the untreated sperm samples, 50% of sperm that were motile initially became immotile during 4 hr storage. Comparison of bulls yielding semen of original low motility with bulls yielding originally high motilityspermatozoa indicatedthatan immediate stimulation of sperm motilityby caffeine occurred inthelow motilityspecimens (32.2-49.3% motile) but not inthoseofhighmotility. Itispostulated that the effect of caffeine on spermatozoan motility and respiration is mediatedby one ofthecyclic nucleotides. This results in a somewhat unique effect, because sperm activity and sperm life, asjudgedby motility, areboth increasedwithcaffeineaddition.

Stimulation and Maintenance of Ejaculated Bovine Spermatozoan Respiration and Motility by Caffeine

The relation between oxygen consumption and motility of Ciona spermatozoa has been measured by using pH stats to measure the acid production of spermatozoa swimming in dilute suspensions where their motility can be analyzed accurately, and calibrating the acid production by measuring it simultaneously with measurements of oxygen consumption, using more concentrated sperm suspensions. When the motility of the spermatozoa is inhibited by thiourea or by increased viscosity, their oxygen consumption decreases in proportion to the decrease in beat frequency. 80–85 % of their oxygen consumption appears to be tightly coupled to motility. The amount of movement-coupled oxidative metabolism per beat remains nearly constant, even when there are significant changes in the energy required per beat for movement against the viscous resistance of the medium. This implies that under these conditions, where the radius of curvature of flagellar bending remains constant, the amount of ATP used is determined by a stoichiometric relation to bending rather than by the energy requirement. The movement-coupled oxidative metabolism appears to be sufficient to generate approximately two molecules of ATP per beat for each molecule of the flagellar ATPase, dynein.

/pdf/mechanochemical-coupling-in-flagella-ii-effects-of-viscosity-38kqocg8il.pdf

Mechanochemical coupling in flagella. II. Effects of viscosity and thiourea on metabolism and motility of Ciona spermatozoa.

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Mechanochemical coupling in flagella. II. Effects of viscosity and thiourea on metabolism and motility of Ciona spermatozoa.