Evolution of heterotrophy in chrysophytes as reflected by comparative transcriptomics

Graupner, Nadine; Jensen, Manfred; Böck, Christina; Marks, Sabina; Rahmann, Sven; Beißer, Daniela; Boenigk, Jens

doi:10.1093/femsec/fiy039

Cited by 35 publications

(46 citation statements)

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“…Further, numerous authors stated and proved a correlation of cell volume and genome size (e.g., Bennett 1972). Additionally, heterotrophic chrysophytes are generally smaller than phototrophic ones, since they do only host remnants of a plastid (Škaloud et al 2014;Grossmann et al 2016;Graupner et al 2018). Following these, we hypothesize phototrophic taxa to have larger genomes than heterotrophic ones, due to the differences in cell sizes.…”

Section: Introductionmentioning

confidence: 55%

“…However, the heterotrophic Paraphysomonadida also branch basal indicating that the loss of phototrophy occurred early in some branches of Chrysophyceae . As the basal branching pattern is not yet sufficiently resolved, we cannot fully exclude the possibility of early heterotrophic ancestors within Chrysophyceae even though such a scenario appears highly unlikely as it would require secondary "revival" of the plastid and plastid metabolism (Graupner et al 2018).…”

Section: Discussionmentioning

confidence: 95%

“…The plastids of these heterotrophic chrysophytes are in different stages of reduction and may be involved in several metabolic pathways as well as contain numerous photopigments (Graupner et al 2018). However, the heterotrophic chrysophytes have in common the loss of chlorophyll and photosynthetic pathways as it had been demonstrated for several lineages so far (Graupner et al 2018). They rely on particulate food uptake and prey on bacteria and other bacteria-sized microorganisms to gain carbon (Boenigk et al 2005).…”

Section: Introductionmentioning

confidence: 98%

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Genome size of chrysophytes varies with cell size and nutritional mode

et al. 2018

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The cellular content of nuclear DNA varies up to 200,000-fold between eukaryotes. These differences can arise via different mechanisms. In particular, cell size and nutritional mode may influence evolution of the nuclear DNA content. Chrysophytes comprise organisms with different cell organizations and nutritional modes. Heterotrophic clades evolved independently several times from phototrophic or mixotrophic ancestors. Thus, chrysophytes are an ideal model taxon for investigating the effect of the nutritional mode on cellular DNA content. We investigated the genome size of heterotrophic, mixotrophic, and phototrophic chrysophytes. We demonstrate that cell sizes and genome sizes differ significantly between taxa with different nutritional modes. Phototrophic strains tend to have larger cell volumes and larger genomes than heterotrophic strains do. The investigated mixotrophic strains had intermediate cell volumes and small to intermediate genome sizes. Heterotrophic chrysophytes had the smallest genomes and cell volumes compared to other chrysophytes. In general, genome size increased with cell volume, but cell volume only partially explained the variation in genome size. In particular, genome sizes of mixotrophic strains were smaller than expected based on cell sizes.

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Section: Introductionmentioning

confidence: 55%

Section: Discussionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 98%

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Genome size of chrysophytes varies with cell size and nutritional mode

et al. 2018

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“…E. longa thus joins the group of recently discovered plastid-bearing eukaryotes lacking the MEP pathway, namely the colourless diatom Nitzschia sp. NIES-3581 (Kamikawa et al 2017) and various colourless chrysophytes (Graupner et al 2018; Dorrell et al 2019). In contrast, the plastid-localized MEP pathway in apicomplexans and related alveolates (i.e.…”

Section: Resultsmentioning

confidence: 99%

“…Many of them have a similar metabolic capacity as the apicoplast (Sanchez-Puerta et al 2007; Slamovits and Keeling 2008; Fernández Robledo et al 2011), and some house an even more complex metabolism that includes amino acid biosynthesis and carbohydrate metabolism pathways (Borza et al 2005; Pombert et al 2014; Smith and Lee 2014). Until recently, IPP synthesis seemed to be a process conserved even in the most reduced relic plastids, such as the genome-lacking plastids of certain alveolates (Matsuzaki et al 2008; Janouškovec et al 2015), but non-photosynthetic plastids lacking the characteristic plastidial (MEP or DOXP) pathway of IPP biosynthesis are now known (Kamikawa et al 2017; Graupner et al 2018; Dorrell et al 2019). Thus, there is generally a metabolic reason for a plastid retention, although the cases of plastid dependency differ between lineages.…”

Section: Introductionmentioning

confidence: 99%

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

Füssy

Záhonová

Tomčala

et al. 2019

Preprint

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AbstractMost secondarily non-photosynthetic eukaryotes have retained residual plastids whose physiological role is often still unknown. One such example is Euglena longa, a close non-photosynthetic relative of Euglena gracilis harbouring a plastid organelle of enigmatic function. By mining transcriptome data from E. longa 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 E. longa 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+ 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 E. longa cell. In effect, the pathway may function as a redox valve bypassing the glycolytic oxidation of glyceraldehyde-3-phosphate to 3-phosphoglycerate. Altogether, the E. longa plastid defines a new class of relic plastids that is drastically different from the best studied organelle of this category, the apicoplast.ImportanceColourless 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 Euglena longa, a non-photosynthetic cousin of the familiar green flagellate Euglena gracilis. We document an unprecedented combination of metabolic functions that the E. longa 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 CO2-fixing enzyme RuBisCO in E. longa. 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.

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Eukaryotic cellular intricacies shape mitochondrial proteomic complexity

et al. 2022

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Mitochondria have been fundamental to the eco‐physiological success of eukaryotes since the last eukaryotic common ancestor (LECA). They contribute essential functions to eukaryotic cells, above and beyond classical respiration. Mitochondria interact with, and complement, metabolic pathways occurring in other organelles, notably diversifying the chloroplast metabolism of photosynthetic organisms. Here, we integrate existing literature to investigate how mitochondrial metabolism varies across the landscape of eukaryotic evolution. We illustrate the mitochondrial remodelling and proteomic changes undergone in conjunction with major evolutionary transitions. We explore how the mitochondrial complexity of the LECA has been remodelled in specific groups to support subsequent evolutionary transitions, such as the acquisition of chloroplasts in photosynthetic species and the emergence of multicellularity. We highlight the versatile and crucial roles played by mitochondria during eukaryotic evolution, extending from its huge contribution to the development of the LECA itself to the dynamic evolution of individual eukaryote groups, reflecting both their current ecologies and evolutionary histories.

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Evolution of heterotrophy in chrysophytes as reflected by comparative transcriptomics

Cited by 35 publications

References 75 publications

Genome size of chrysophytes varies with cell size and nutritional mode

Genome size of chrysophytes varies with cell size and nutritional mode

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

Eukaryotic cellular intricacies shape mitochondrial proteomic complexity

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