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The growth cycle in nutrient-rich, aquatic environments starts with a diatom bloom that ends in mass sinking of ungrazed cells and phytodetritus. The low grazing pressure on these blooms has been attributed to the inability of overwintering copepod populations to track them temporally. We tested an alternative explanation: that dominant diatom species impair the reproductive success of their grazers. We compared larval development of a common overwintering copepod fed on a ubiquitous, early-blooming diatom species with its development when fed on a typical post-bloom dinoflagellate. Development was arrested in all larvae in which both mothers and their larvae were fed the diatom diet. Mortality remained high even if larvae were switched to the dinoflagellate diet. Aldehydes, cleaved from a fatty acid precursor by enzymes activated within seconds after crushing of the cell, elicit the teratogenic effect. This insidious mechanism, which does not deter the herbivore from feeding but impairs its recruitment, will restrain the cohort size of the next generation of early-rising overwinterers. Such a transgenerational plant-herbivore interaction could explain the recurringly inefficient use of a predictable, potentially valuable food resource--the spring diatom bloom--by marine zooplankton.

SUMMARY The diatom-derived aldehyde 2-trans-4-trans-decadienal(DD) was tested as an apoptogenic inducer in both copepod and sea urchin embryos, using terminal-deoxynucleotidyl-transferase-mediated dUTP nick-end labelling (TUNEL), DNA fragmentation profiling (laddering) and an assay for caspase-3 activity. DD induced TUNEL positivity and DNA laddering, but not caspase-like activation, in copepod embryos spawned by females fed for 10-15 days the diatom diet Thalassiosira rotula Meunier (in vivo),or when newly spawned eggs were exposed for 1 h to 5 μg ml-1 DD(in vitro). To our knowledge, this is the first time that evidence for an apoptotic process in copepods has been obtained by cytochemical (TUNEL)and biochemical (DNA fragmentation) approaches. The absence of caspase-like activity in copepod embryos suggests that caspase-independent programmed cell death occurs in these organisms. In sea urchin embryos, DD induced apoptosis and also activated a caspase-3-like protease. The saturated aldehyde decanal induced apoptosis at higher concentrations and after a longer incubation period than DD, indicating that α,β-unsaturation of the molecule,coupled with the aldehyde group, is responsible for the greater biological activity of DD. Since diatoms are an important food source for marine herbivores such as copepods and sea urchins, these findings may help explain why unsaturated aldehydes often induce reproductive failure, with important ecological consequences at the population level.

No abstract

The effects of bioactive aldehydes from diatoms, unicellular algae at the base of the marine food web, were studied on fertilization and early development processes of the ascidian Ciona intestinalis. Using whole-cell voltage clamp techniques, we show that 2-trans-4-trans-decadienal (DD) and 2-trans-4-cis-7-cis-decatrienal (DT) inhibited the fertilization current which is generated in oocytes upon interaction with the spermatozoon. This inhibition was dose-dependent and was accompanied by inhibition of the voltage-gated calcium current activity of the plasma membrane. DD and DT did not inhibit the subsequent contraction of the cortex. Moreover, DD specifically acted as a fertilization channel inhibitor since it did not affect the steady state conductance of the plasma membrane or gap junctional (GJ) communication within blastomeres of the embryo. On the other hand, DD did affect actin reorganization even though the mechanism of action on actin filaments differed from that of other actin blockers. Possibly this effect on actin reorganization was responsible for the subsequent teratogenic action on larval development. The effect of DD was reversible if oocytes were washed soon after fertilization indicating that DD may specifically target certain fertilization mechanisms. Thus, diatom reactive aldehydes such as DD may have a dual effect on reproductive processes, influencing primary fertilization events such as gating of fertilization channels and secondary processes such as actin reorganization which is responsible for the segregation of cell lineages. These findings add to a growing body of evidence on the antiproliferative effects of diatom-derived aldehydes. Our results also report, for the first time, on the action of a fertilization channel blocker in marine invertebrates.