Abstract

Apicomplexa are protist parasites that include Plasmodium spp., the causative agents of malaria, and Toxoplasma gondii, responsible for toxoplasmosis. Most Apicomplexa possess a relict plastid, the apicoplast, which was acquired by secondary endosymbiosis of a red alga. Despite being nonphotosynthetic, the apicoplast is otherwise metabolically similar to algal and plant plastids and is essential for parasite survival. Previous studies of Toxoplasma gondii identified membrane lipids with some structural features of plastid galactolipids, the major plastid lipid class. However, direct evidence for the plant-like enzymes responsible for galactolipid synthesis in Apicomplexan parasites has not been obtained. Chromera velia is an Apicomplexan relative recently discovered in Australian corals. C. velia retains a photosynthetic plastid, providing a unique model to study the evolution of the apicoplast. Here, we report the unambiguous presence of plant-like monogalactosyldiacylglycerol and digalactosyldiacylglycerol in C. velia and localize digalactosyldiacylglycerol to the plastid. We also provide evidence for a plant-like biosynthesis pathway and identify candidate galactosyltranferases responsible for galactolipid synthesis. Our study provides new insights in the evolution of these important enzymes in plastid-containing eukaryotes and will help reconstruct the evolution of glycerolipid metabolism in important parasites such as Plasmodium and Toxoplasma.

Highlights

  • Galactolipids in the Plastid of Chromera tions of membrane biogenesis and homeostasis, as well as developmental and physiological processes in autotrophic organisms

  • C. velia Contains MGDG and DGDG Enriched in Long Polyunsaturated Fatty Acid Chains—To assess the presence of plant/plastid-like galactolipids in C. velia, total lipids were analyzed by HPTLC

  • C. velia, and their apparent absence in apicoplasts of Apicomplexan parasites, supports the notion that an abundance of MGDG and DGDG correlates with photosynthesis

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Summary

Introduction

Galactolipids in the Plastid of Chromera tions of membrane biogenesis and homeostasis, as well as developmental and physiological processes in autotrophic organisms. A digalactolipid reacting against an anti-DGDG antibody was localized within the pellicle membranes of T. gondii, but not in the apicoplast [20] This plantlike digalactolipid was proposed to be the same as those detected in previous labeling experiments. Lipidomic analysis performed in T. gondii showed the presence of two types of hexosyl(galacto) lipid classes as minor membrane components as follows: (i) plant-like hexosylglycerolipids and (ii) hexosylceramides [20, 21]. These data are suggestive of a pathway of galactolipid biosynthesis in some Apicomplexan parasites, many questions remain. We identify the candidate genes encoding galactosyltransferases responsible for galactolipid synthesis in C. velia and discuss their importance for the evolution of this pathway in photosynthetic eukaryotes

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