Evolutionarily conserved aspects of animal nutrient uptake and transport in sea anemone vitellogenesis.

The emergence of systemic nutrient transport was a key challenge during animal evolution, yet it is poorly understood. Circulatory systems distribute nutrients in many bilaterians (e.g., vertebrates and arthropods) but are absent in non-bilaterians (e.g., cnidarians and sponges), where nutrient absorption and transport remain little explored at molecular and cellular levels. Vitellogenesis, the accumulation of egg yolk, necessitates high nutrient influx into oocytes and is present throughout animal phyla and therefore represents a well-suited paradigm to study nutrient transport evolution. With that aim, we investigated dietary nutrient transport to the oocytes in the cnidarian Nematostella vectensis (Anthozoa). Using a combination of fluorescent bead labeling and marker gene expression, we found that phagocytosis, micropinocytosis, and intracellular digestion of food components occur within the gonad epithelium. Pulse-chase experiments further show that labelled fatty acids rapidly translocate from the gonad epithelium through the extracellular matrix (ECM) into oocytes. Expression of conserved lipid transport proteins vitellogenin (vtg) and apolipoprotein-B (apoB) and colocalization of labeled fatty acids with a fluorescently tagged ApoB protein further support the lipid-shuttling role of the gonad epithelium. Complementary oocyte expression of very low-density lipoprotein receptor (vldlr) orthologs, which mediate endocytosis of bilaterian ApoB- and Vtg-lipoproteins, supports that this evolutionarily conserved ligand/receptor pair underlies lipid transport during sea anemone vitellogenesis. In addition, we identified lipid- and ApoB-rich cells with potential lipid transport roles in the ECM. Altogether, our work supports a long-standing hypothesis that an ECM-based lipid transport system predated the cnidarian-bilaterian split and provided a basis for the evolution of bilaterian circulatory systems.

Functional Role of Native and Invasive Filter-Feeders, and the Effect of Parasites: Learning from Hypersaline Ecosystems.

Filter-feeding organisms are often keystone species with a major influence on the dynamics of aquatic ecosystems. Studies of filtering rates in such taxa are therefore vital in order to understand ecosystem functioning and the impact of natural and anthropogenic stressors such as parasites, climate warming and invasive species. Brine shrimps Artemia spp. are the dominant grazers in hypersaline systems and are a good example of such keystone taxa. Hypersaline ecosystems are relatively simplified environments compared with much more complex freshwater and marine ecosystems, making them suitable model systems to address these questions. The aim of this study was to compare feeding rates at different salinities and temperatures between clonal A. parthenogenetica (native to Eurasia and Africa) and the invasive American brine shrimp A. franciscana, which is excluding native Artemia from many localities. We considered how differences observed in laboratory experiments upscale at the ecosystem level across both spatial and temporal scales (as indicated by chlorophyll-a concentration and turbidity). In laboratory experiments, feeding rates increased at higher temperatures and salinities in both Artemia species and sexes, whilst A. franciscana consistently fed at higher rates. A field study of temporal dynamics revealed significantly higher concentrations of chlorophyll-a in sites occupied by A. parthenogenetica, supporting our experimental findings. Artemia parthenogenetica density and biomass were negatively correlated with chlorophyll-a concentration at the spatial scale. We also tested the effect of cestode parasites, which are highly prevalent in native Artemia but much rarer in the invasive species. The cestodes Flamingolepis liguloides and Anomotaenia tringae decreased feeding rates in native Artemia, whilst Confluaria podicipina had no significant effect. Total parasite prevalence was positively correlated with turbidity. Overall, parasites are likely to reduce feeding rates in the field, and their negative impact on host fecundity is likely to exacerbate the difference between grazing rates of native and alien Artemia populations at the ecosystem level. The results of this study provide evidence for the first time that the replacement of native Artemia by A. franciscana may have major consequences for the functioning of hypersaline ecosystems. The strong effect of parasites on feeding rate underlines the importance of taking parasites into account in order to improve our understanding of the functioning of aquatic ecosystems.

Mating in the box jellyfish Copula sivickisi--Novel function of cnidocytes.

Within cubozoans, a few species have developed a sexual reproduction system including mating and internal fertilization. One species, Copula sivickisi, is found in a large area of the indo pacific. They have separate sexes and when mature males and females meet they entangle their tentacles and the males transfer a sperm package, a spermatozeugmata, which is ingested by the female fertilizing her eggs internally. After 2-3 days, the females lay an embryo strand that sticks to the substrate and after another 2-3 days, the fully developed larvae leave the strand. We have examined the ultrastructure of the gonads and spermatozeugmata to look for structural adaptations to this specialized way of reproduction and understand how the fertilization takes place. Surprisingly, we discovered that the male gonads were heavily packed with cnidocytes of the isorhiza type and that they are transferred to the spermatozeugmata. The spermatozeugmata does not dissolve in the female gastrovascular cavity but is attached to the female gonad probably using the isorhizas. Here, the sperm cells are partly digested and the nuclei are released. The actual fertilization seems to happen through phagocytosis of the released nuclei by the epithelial cells. The female gonads are likewise packed with cnidocytes but of the eurytele type. They do not mature inside the female and putatively serve to protect the developing larvae once the embryo strand is laid. This specialized way of fertilization is to our knowledge novel and so is this first account of cnidocytes being directly involved in cnidarian reproduction.