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

Abstract

Vitellogenesis, the accumulation of egg yolk, relies on the transport of dietary nutrients from the gut to the ovary through the circulatory system in many bilaterians (e.g. vertebrates, arthropods). How these dietary nutrients and yolk precursors are absorbed and transported in cnidarians (e.g. corals, sea anemones, jellyfish), which are bi-layered and lack a circulatory system, is however only poorly understood. Here, we studied the tissues and molecules that facilitate the uptake and transport of dietary nutrients, especially lipids, towards the oocytes in the sea anemone Nematostella vectensis to better understand the evolution of systemic nutrient transport in animals. We identified the somatic gonad epithelium as one of several gastrodermal tissues specialized in phagocytosis, micropinocytosis and intracellular digestion. We showed more specifically that dietary fatty acids are absorbed by the ApolipoproteinB- and Vitellogenin-expressing somatic gonad epithelium. Their subsequent, rapid transport into the extracellular matrix (ECM) and endocytosis into oocytes is likely mediated by an evolutionary conserved Vitellogenin (Vtg)-Very Low-Density Lipoprotein Receptor (VLDLR) ligand/receptor pair. We propose that ECM-based, Vtg/VLDLR-mediated lipoprotein transport during vitellogenesis predates the cnidarian-bilaterian split and provided a mechanistic basis to evolve sophisticated circulatory systems in bilaterians.