Autonomous changes in the swimming direction of sperm in the gastropodStrombus luhuanus

Abstract

The sperm of the gastropod Strombus luhuanus show dimorphism. The eusperm have a nucleus and fertilize the egg, whereas the other type of sperm, parasperm, are anucleate and are thought to assist fertilization. Here we report the autonomous changes in the swimming pattern of S. luhuanus eusperm. In artificial seawater, the eusperm collected from S. luhuanus sperm ducts formed sperm bundles and initially swam backward with asymmetric flagellar waveforms to detach from the bundles. One hour later, the sperm began to swim forward and in a circle. After an additional 1 h incubation, the sperm swam straight, with a change in the flagellar waveforms from asymmetric to symmetric. Spontaneous backward swimming with symmetric waveforms was also observed. The eusperm stored in the female seminal receptacle were motile and showed forward symmetric swimming with spontaneous backward swimming, which appeared necessary for detachment from the wall of receptacle. All of these motility changes were observed in the absence of parasperm, suggesting that these changes autonomously occur in eusperm. Our waveform analysis of these swimming patterns revealed that only the swimming with symmetric waveform showed reverse propagation of the flagellar waveforms. Both types of backward swimming were diminished in Ca INTRODUCTIONChanges in the swimming patterns of sperm are commonly seen in animals and plants and are considered to be necessary for efficient fertilization (Cosson, 2010;Inaba, 2003;Morisawa, 1994). Generally, spermatozoa are immotile in the testes and sperm ducts but become motile after spawning into an external or female environment. The factors that regulate the initiation and activation of sperm motility include both physical factors such as osmolality and temperature and chemical factors such as specific ions and egg-or genital tract-derived substances. These factors trigger ion influx/efflux and changes in the membrane potential and intracellular Ca 2+ concentration, leading to the activation of protein kinase and eventually to the modulation of axonemal dyneins (Darszon et al., 1999;Inaba, 2011). However, a transient increase of the intracellular Ca 2+ concentration induced by chemoattractants caused changes in flagellar asymmetry, resulting in chemotaxis toward the eggs (Kaupp et al., 2008;Shiba et al., 2008;Yoshida and Yoshida, 2011;Mizuno et al., 2012). Animals with internal fertilization exhibit a variety of changes in sperm motility. For example, the motility of mammalian spermatozoa is changed remarkably after a couple of hours of incubation with a solution containing calcium and bicarbonate. This state of motility is called hyperactivation, which is characterized by high amplitude and asymmetric flagellar waveforms, and is required for penetration of the zona pellucida (Suarez, 2008a;Yanagimachi, 1970). In contrast to motility activation, the suppression of sperm motility has also been shown during sperm storage in special female organs called spermatheca or seminal receptacles (Neubaum and Wolfner, 199...

From damage response to action potentials: early evolution of neural and contractile modules in stem eukaryotes

“…In animals, calcium usually inhibits flagellar or ciliary motility: calcium induces ciliary arrest in mussel gill cilia [101][102][103], in ascidian gill slits [104] and in embryonic epidermal cilia of sea urchins [105]. In sperm cells of ascidians [106], sea urchins [107,108], siphonophores [109] and snails [110], calcium bursts increase the asymmetry of flagellar beating and the swimming curvature, which serves to change direction during chemotaxis [111]; in Ciona sperm cells, the calcium sensor has been shown to be calaxin, a protein that directly inhibits outer-arm dyneins, thus triggering beating asymmetry [112]-showing that the response of sperm flagellar beating to calcium is inhibitory at the molecular level. Exceptions are known in vertebrates, such as the cilia of the vertebrate foregut (mammalian airways and frog oesophagus [98,113]) or the flagellum of mammalian spermatozoa [114], which respond to calcium by increasing beating frequency.…”

Axonemal Growth and Alignment During Paraspermatogenesis in the Marine Gastropod Strombus luhuanus

“…We previously reported that eusperm change motility in seawater autonomously, including backward asymmetric movement for detachment from the sperm bundle, circular and straight forward movement, and spontaneous backward swimming with symmetric flagellar waveforms ( Shiba et al, 2014 ). As Nishiwaki (1964) briefly mentioned, the Strombus parasperm also exhibited backward swimming.…”

Calcium sensors of ciliary outer arm dynein: functions and phylogenetic considerations for eukaryotic evolution

“…Sperm in some insects and snails reverse the direction of bend propagation in a Ca 2+ -dependent manner [ 26 - 30 ]. For example, in the sperm of the gastropod Strombus luhuanus , the reversal of bend propagation appears to be involved in sperm release from the sperm storage site in the female genital tract [ 30 ].…”