The cryptic plastid of Euglena longa defines a new type of non-photosynthetic plastid organelles

Abstract

<jats:title>Abstract</jats:title><jats:p>Most secondarily non-photosynthetic eukaryotes have retained residual plastids whose physiological role is often still unknown. One such example is <jats:italic>Euglena longa,</jats:italic> a close non-photosynthetic relative of <jats:italic>Euglena gracilis</jats:italic> harbouring a plastid organelle of enigmatic function. By mining transcriptome data from <jats:italic>E. longa</jats:italic> we finally provide an overview of metabolic processes localized to its elusive plastid. The organelle plays no role in biosynthesis of isoprenoid precursors and fatty acids, and has a very limited repertoire of pathways concerning nitrogen-containing metabolites. In contrast, the synthesis of phospholipids and glycolipids has been preserved, curiously with the last step of sulfoquinovosyldiacylglycerol synthesis being catalysed by the SqdX form of the enzyme so far known only from bacteria. Notably, we show that the <jats:italic>E. longa</jats:italic> plastid synthesizes tocopherols and a phylloquinone derivative, the first such report for non-photosynthetic plastids studied so far. The most striking attribute of the organelle is the presence of a linearized Calvin-Benson (CB) pathway including RuBisCO yet lacking the gluconeogenetic part of the standard cycle, together with ferredoxin-NADP<jats:sup>+</jats:sup> reductase (FNR) and the ferredoxin/thioredoxin systems. We hypothesize that FNR passes electrons to the ferredoxin/thioredoxin systems from NADPH to activate the linear CB pathway in response to the redox status of the <jats:italic>E. longa</jats:italic> cell. In effect, the pathway may function as a redox valve bypassing the glycolytic oxidation of glyceraldehyde-3-phosphate to 3-phosphoglycerate. Altogether, the <jats:italic>E. longa</jats:italic> plastid defines a new class of relic plastids that is drastically different from the best studied organelle of this category, the apicoplast.</jats:p><jats:sec><jats:title>Importance</jats:title><jats:p>Colourless plastids incapable of photosynthesis evolved in many plant and algal groups, but what functions they perform is still unknown in many cases. Here we study the elusive plastid of <jats:italic>Euglena longa,</jats:italic> a non-photosynthetic cousin of the familiar green flagellate <jats:italic>Euglena gracilis.</jats:italic> We document an unprecedented combination of metabolic functions that the <jats:italic>E. longa</jats:italic> plastid exhibits in comparison with previously characterized non-photosynthetic plastids. For example, and truly surprisingly, it has retained the synthesis of tocopherols (vitamin E) and a phylloquinone (vitamin K) derivative. In addition, we offer a possible solution of the long-standing conundrum of the presence of the CO<jats:sub>2</jats:sub>-fixing enzyme RuBisCO in <jats:italic>E. longa.</jats:italic> Our work provides a detailed account on a unique variant of relic plastids, the first among non-photosynthetic plastids that evolved by secondary endosymbiosis from a green algal ancestor, and suggests that it has persisted for reasons not previously considered in relation to non-photosynthetic plastids.</jats:p></jats:sec>