First evidence of sperm motility inhibition by the diatom aldehyde 2E,4E-decadienal

Abstract

Diatoms synthesise bioactive unsaturated short-chain aldehydes (SCAs) in response to wound-activation. The defensive SCAs are toxic to developmental stages of a range of invertebrate species including copepods, sea urchins, polychaetes and ascidians. Embryotoxicity is dose-dependent, with inhibition of cleavage, a reduction in hatching success, and teratogenic effects in neonates symptomatic. Bioactivity is directed at cellular and molecular targets. Diatom extracts and the SCA 2E,4E-decadienal (DD) affect microtubule and microfilament stability. Bioactivity is not restricted to embryogenesis, but has also been demonstrated to affect fertilization success in broadcast-spawning macroinvertebrates. This study has sought to further identify the responses of marine invertebrate gametes and the process of fertilization to DD exposure with particular reference to sperm motility. Incubation of gametes with the saturated aldehydes decanal and undecanal and the fatty acid 5, 8,11,14,17-eicosapentaenoic acid (EPA) did not affect fertilization success. Exposure of gametes to DD inhibits fertilization success in a dose-dependent manner. Fertilization rate declined to 50% of control values at concentrations of 1.55 µg ml -1 for Arenicola marina, 3.98 µg ml -1 for Nereis virens, 7.94 µg ml -1 for Psammechinus miliaris and 10 µg ml -1 for Asterias rubens. Pre-incubation of oocytes in DD affected fertilization success to a limited degree; however pre-incubation of sperm in DD caused a pronounced dose-and time-dependent decline. DD exposure inhibits sperm migration rates and flagellar beating at concentrations as low as 0.05 µg ml -1 . The sperm remained alive, as evidenced by oscillation of the sperm head; however, flagellar beating was inhibited. The negative effect of DD exposure was further enhanced as sperm density was reduced. Analysis by general linear model revealed a significant interaction between DD concentration, period of sperm exposure and fertilizing sperm density (F = 6.7, p = 0.01). We suggest that diatom-derived SCAs can significantly impact fertilization success in broadcast-spawning invertebrates. The identification of sperm motility inhibition as a symptom of DD exposure offers a potentially useful cellular model to further study the effects of novel diatom-derived bioactive molecules.

Toxigenic effects of diatoms on grazers, phytoplankton and other microbes: a review

“…For example, exposure of gametes to decadienal inhibited fertilization success which declined to 50% of control values at concentrations of 1.55 lg ml -1 in Arenicola marina, 3.98 lg ml -1 in Nereis virens, 7.94 lg ml -1 in Psammechinus miliaris and 10 lg ml -1 in Asterias rubens (Caldwell et al 2004a). The cause of reduced fertilization success was shown to depend on sperm motility, as demonstrated by pre-incubation of sperm in decadienal which caused a pronounced dosedependent decline in sperm migration rates.…”

Sex-specific biochemical and histological differences in gonads of sea urchins (Psammechinus miliaris) and their response to phenanthrene exposure

“…In the sea urchin, Anthocidaris crassipina, a higher sensitivity of males, assessed by reduced sperm motility and fertilization success of offspring was found after chronic Cd 2þ exposure (Au et al, 2001). In different invertebrate species, Caldwell et al (2004) observed a reduced fertilization success after preincubation of sperm with the diatom-derived aldehyde 2E,4E-decadienal, whereas the effect was negligible after preincubation of eggs. Another example is the blue mussel Mytilus trossulus with significantly reduced fertilization rates after exposure of sperm to 100 mg L À1 copper but not after exposure of eggs (Fitzpatrick et al, 2008).…”

“…Examples are seen in female flounder (Platichthys flesus L.), where higher incidence of liver cancer is associated with sex-specific differences in NADPH metabolism important for xenobiotic biotransformation (Köhler and Van Noorden, 2003). Interestingly, in invertebrates male gametes often appear more susceptible to chemical stress than eggs (Au et al, 2001;Caldwell et al, 2004;Fitzpatrick et al, 2008). In the sea urchin, Anthocidaris crassipina, a higher sensitivity of males, assessed by reduced sperm motility and fertilization success of offspring was found after chronic Cd 2þ exposure (Au et al, 2001).…”

Long-lived sperm in the geothermal bryophyte Pohlia nutans

“…Turner 2006;Stewart et al 2007) and marine invertebrates (e.g. Caldwell et al 2004;Johnson & Yund 2004), very little is known about this important life-history stage in algae and non-vascular plants (Rice & Laetsch 1967;Paolillo 1981). As taxa with bryophyte-type morphology were probably the first land plants (Kenrick & Crane 1997;Nickrent et al 2000), reliance on motile sperm is theorized to have limited their ability to spread in the terrestrial environment, particularly in comparison with seed plants that disperse gametes as pollen (Shaw & Renzaglia 2004).…”