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, necessi-tates 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 trans-port 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 -shut-tling 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.

Automated summary

This study investigates the absorption and transport of nutrients, especially lipids, in the oocytes of the cnidarian Nematostella vectensis. The researchers found that an extracellular matrix-based lipid transport system plays a crucial role in this process, suggesting its existence before the divergence of cnidarians and bilaterians and providing a foundation for the evolution of bilaterian circulatory systems.