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Basal Sliding and the Mechanics of Oscillation in a Mammalian Sperm Flagellum

Department of Physiology, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, United Kingdom

Correspondence: Address reprint requests to David M. Woolley, E-mail: d.m.woolley{at}bristol.ac.uk.

The mechanism of oscillation in cilia and flagella has been a long-standing mystery. This article raises the possibility of a mechanical explanation based on new findings relating to where in the flagellum microtubule sliding can occur—and where it cannot occur. All theoretical analyses of flagellar bending have until now made the assumption that sliding displacements at the base of the flagellum cannot occur. One consequence of this has been the need to accept that sliding must be transmitted through propagating bends, an idea that has been tolerated even though it becomes paradoxical if bends are the result of resistance to sliding. Our observations, of spermatozoa from the chinchilla, have led us to a contradictory view. We have shown directly, by light microscopy and by two methods of electron microscopy, that basal sliding does occur. Also, evidence from video microscopy indicates that a propagating bend cannot transmit sliding through it. We have analyzed a movement pattern in which the beat frequency increases fourfold in a phasic manner. Our analysis of this suggests that new bends terminate when no further sliding is possible. At this point the bend direction immediately reverses. That is, the flagellar beat frequency increases when there is a limitation to sliding. One can see directly the alternation in basal sliding direction under these circumstances. This suggests a mechanism for the initiation of a new bend in the opposite direction to the bend just completed: we propose that the initiating trigger is the reversal of elastic deformations at the base, which reverses the direction of interdoublet sliding.

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