Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgate 55, 5008 Bergen, Norway.
Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgate 55, 5008 Bergen, Norway.
Curr Biol. 2022 Nov 7;32(21):4620-4630.e5. doi: 10.1016/j.cub.2022.08.039. Epub 2022 Sep 8.
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.
动物进化过程中面临的一个关键挑战是系统营养物质运输的出现，但人们对此知之甚少。循环系统在许多两侧对称动物（如脊椎动物和节肢动物）中分布营养物质，但在非两侧对称动物（如刺胞动物和海绵动物）中则不存在，在这些动物中，分子和细胞水平上的营养吸收和运输仍鲜有研究。卵黄的积累——卵黄发生，需要大量营养物质流入卵母细胞，并且存在于所有动物门中，因此是研究营养物质运输进化的一个很好的范例。有鉴于此，我们研究了刺胞动物 Nematostella vectensis（珊瑚纲）中卵母细胞的饮食营养物质运输。我们结合使用荧光珠标记和标记基因表达，发现吞噬作用、微胞饮作用和食物成分的细胞内消化发生在性腺上皮内。脉冲追踪实验进一步表明，标记的脂肪酸迅速从性腺上皮通过细胞外基质（ECM）转运到卵母细胞中。保守的脂质转运蛋白卵黄蛋白原（vtg）和载脂蛋白-B（apoB）的表达以及标记脂肪酸与荧光标记的 ApoB 蛋白的共定位进一步支持了性腺上皮的脂质转运作用。互补的卵母细胞表达极低密度脂蛋白受体（vldlr）的同源物，该同源物介导了两侧对称动物 apoB 和 vtg 脂蛋白的内吞作用，这支持了这个进化上保守的配体/受体对在海葵卵黄发生过程中脂质运输的基础作用。此外，我们还在 ECM 中发现了具有潜在脂质运输作用的富含脂质和 ApoB 的细胞。总之，我们的工作支持了一个长期存在的假说，即基于 ECM 的脂质运输系统先于刺胞动物与两侧对称动物的分化出现，并为两侧对称动物循环系统的进化提供了基础。
