Most cited article - PubMed ID 27391690
RuBisCO in Non-Photosynthetic Alga Euglena longa: Divergent Features, Transcriptomic Analysis and Regulation of Complex Formation
Complete plastid loss seems to be very rare among secondarily non-photosynthetic eukaryotes. Leukarachnion sp. PRA-24, an amoeboid colourless protist related to the photosynthetic algal class Synchromophyceae (Ochrophyta), is a candidate for such a case based on a previous investigation by transmission electron microscopy. Here, we characterize this organism in further detail and describe it as Leucomyxa plasmidifera gen. et sp. nov., additionally demonstrating it is the first known representative of a broader clade of non-photosynthetic ochrophytes. We recovered its complete plastid genome, exhibiting a reduced gene set similar to plastomes of other non-photosynthetic ochrophytes, yet being even more extreme in sequence divergence. Identification of components of the plastid protein import machinery in the L. plasmidifera transcriptome assembly corroborated that the organism possesses a cryptic plastid organelle. According to our bioinformatic reconstruction, the plastid contains a unique combination of biosynthetic pathways producing haem, a folate precursor and tocotrienols. As another twist to its organellar biology, L. plasmidifera turned out to contain an unusual long insertion in its mitogenome related to a newly discovered mitochondrial plasmid exhibiting unprecedented features in terms of its size and coding capacity. Combined, our work uncovered further striking outcomes of the evolutionary course of semiautonomous organelles in protists.
- Keywords
- Leukarachnion, mitochondrial plasmids, non-photosynthetic plastid, plastid evolution, plastid genome, stramenopiles,
- MeSH
- Phylogeny * MeSH
- Genome, Mitochondrial MeSH
- Genome, Plastid * MeSH
- Mitochondria genetics metabolism MeSH
- Evolution, Molecular MeSH
- Plastids * genetics metabolism MeSH
- Plasmids * genetics MeSH
- Publication type
- Journal Article MeSH
A considerable part of the diversity of eukaryotic phototrophs consists of algae with plastids that evolved from endosymbioses between two eukaryotes. These complex plastids are characterized by a high number of envelope membranes (more than two) and some of them contain a residual nucleus of the endosymbiotic alga called a nucleomorph. Complex plastid-bearing algae are thus chimeric cell assemblies, eukaryotic symbionts living in a eukaryotic host. In contrast, the primary plastids of the Archaeplastida (plants, green algae, red algae, and glaucophytes) possibly evolved from a single endosymbiosis with a cyanobacterium and are surrounded by two membranes. Complex plastids have been acquired several times by unrelated groups of eukaryotic heterotrophic hosts, suggesting that complex plastids are somewhat easier to obtain than primary plastids. Evidence suggests that complex plastids arose twice independently in the green lineage (euglenophytes and chlorarachniophytes) through secondary endosymbiosis, and four times in the red lineage, first through secondary endosymbiosis in cryptophytes, then by higher-order events in stramenopiles, alveolates, and haptophytes. Engulfment of primary and complex plastid-containing algae by eukaryotic hosts (secondary, tertiary, and higher-order endosymbioses) is also responsible for numerous plastid replacements in dinoflagellates. Plastid endosymbiosis is accompanied by massive gene transfer from the endosymbiont to the host nucleus and cell adaptation of both endosymbiotic partners, which is related to the trophic switch to phototrophy and loss of autonomy of the endosymbiont. Such a process is essential for the metabolic integration and division control of the endosymbiont in the host. Although photosynthesis is the main advantage of acquiring plastids, loss of photosynthesis often occurs in algae with complex plastids. This chapter summarizes the essential knowledge of the acquisition, evolution, and function of complex plastids.
- Keywords
- Complex endosymbiosis, Plastid replacement, Reductive evolution,
- MeSH
- Biological Evolution * MeSH
- Phylogeny MeSH
- Plastids genetics metabolism MeSH
- Rhodophyta * genetics MeSH
- Plants genetics MeSH
- Symbiosis MeSH
- Publication type
- Journal Article MeSH
Catalase is one of the most abundant enzymes on Earth. It decomposes hydrogen peroxide, thus protecting cells from dangerous reactive oxygen species. The catalase-encoding gene is conspicuously absent from the genome of most representatives of the family Trypanosomatidae. Here, we expressed this protein from the Leishmania mexicana Β-TUBULIN locus using a novel bicistronic expression system, which relies on the 2A peptide of Teschovirus A. We demonstrated that catalase-expressing parasites are severely compromised in their ability to develop in insects, to be transmitted and to infect mice, and to cause clinical manifestation in their mammalian host. Taken together, our data support the hypothesis that the presence of catalase is not compatible with the dixenous life cycle of Leishmania, resulting in loss of this gene from the genome during the evolution of these parasites.
- Keywords
- Leishmania, catalase, dixeny, evolution, virulence,
- MeSH
- Virulence Factors genetics metabolism MeSH
- Catalase genetics metabolism MeSH
- Cells, Cultured MeSH
- Leishmania mexicana genetics growth & development pathogenicity MeSH
- Mice, Inbred BALB C MeSH
- Mice MeSH
- Protozoan Proteins genetics MeSH
- Psychodidae parasitology MeSH
- Life Cycle Stages genetics MeSH
- Teschovirus genetics MeSH
- Virulence MeSH
- Animals MeSH
- Check Tag
- Mice MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Virulence Factors MeSH
- Catalase MeSH
- Protozoan Proteins MeSH
Most secondary nonphotosynthetic eukaryotes have retained residual plastids whose physiological role is often still unknown. One such example is Euglena longa, a close nonphotosynthetic relative of Euglena gracilis harboring 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 the 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 catalyzed by the SqdX form of an 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 nonphotosynthetic plastids studied so far. The most striking attribute of the organelle could be 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 system. We hypothesize that the ferredoxin/thioredoxin system activates the linear CB pathway in response to the redox status of the E. longa cell and speculate on the role of the pathway in keeping the redox balance of the cell. 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.IMPORTANCE Colorless 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 nonphotosynthetic 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 nonphotosynthetic 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 nonphotosynthetic 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 nonphotosynthetic plastids.
- Keywords
- Calvin-Benson cycle, Euglena longa, Euglenophyceae, evolution, nonphotosynthetic plastids, phylloquinone, redox balance, sulfoquinovosyldiacylglycerol, tocopherol,
- MeSH
- Euglena longa cytology genetics physiology MeSH
- Photosynthesis MeSH
- Phylogeny MeSH
- Evolution, Molecular MeSH
- Plastids classification genetics MeSH
- Transcriptome MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
In this work, we studied the biochemical properties and evolutionary histories of catalase (CAT) and ascorbate peroxidase (APX), two central enzymes of reactive oxygen species detoxification, across the highly diverse clade Eugenozoa. This clade encompasses free-living phototrophic and heterotrophic flagellates, as well as obligate parasites of insects, vertebrates, and plants. We present evidence of several independent acquisitions of CAT by horizontal gene transfers and evolutionary novelties associated with the APX presence. We posit that Euglenozoa recruit these detoxifying enzymes for specific molecular tasks, such as photosynthesis in euglenids and membrane-bound peroxidase activity in kinetoplastids and some diplonemids.
- Keywords
- Euglenozoa, ascorbate peroxidase, catalase, enzymatic activity, phylogeny,
- Publication type
- Journal Article MeSH
Euglenophytes are a familiar algal group with green alga-derived secondary plastids, but the knowledge of euglenophyte plastid function and evolution is still highly incomplete. With this in mind we sequenced and analysed the transcriptome of the non-photosynthetic species Euglena longa. The transcriptomic data confirmed the absence of genes for the photosynthetic machinery, but provided candidate plastid-localised proteins bearing N-terminal bipartite topogenic signals (BTSs) of the characteristic euglenophyte type. Further comparative analyses including transcriptome assemblies available for photosynthetic euglenophytes enabled us to unveil salient aspects of the basic euglenophyte plastid infrastructure, such as plastidial targeting of several proteins as C-terminal translational fusions with other BTS-bearing proteins or replacement of the conventional eubacteria-derived plastidial ribosomal protein L24 by homologs of archaeo-eukaryotic origin. Strikingly, no homologs of any key component of the TOC/TIC system and the plastid division apparatus are discernible in euglenophytes, and the machinery for intraplastidial protein targeting has been simplified by the loss of the cpSRP/cpFtsY system and the SEC2 translocon. Lastly, euglenophytes proved to encode a plastid-targeted homolog of the termination factor Rho horizontally acquired from a Lambdaproteobacteria-related donor. Our study thus further documents a substantial remodelling of the euglenophyte plastid compared to its green algal progenitor.
- MeSH
- Euglena longa classification cytology genetics MeSH
- Photosynthesis * MeSH
- Phylogeny MeSH
- Evolution, Molecular * MeSH
- Plastids genetics MeSH
- Chloroplast Proteins genetics MeSH
- Base Sequence MeSH
- Sequence Homology MeSH
- Gene Expression Profiling MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Chloroplast Proteins MeSH
Chloroplasts are generally known as eukaryotic organelles whose main function is photosynthesis. They perform other functions, however, such as synthesizing isoprenoids, fatty acids, heme, iron sulphur clusters and other essential compounds. In non-photosynthetic lineages that possess plastids, the chloroplast genomes have been reduced and most (or all) photosynthetic genes have been lost. Consequently, non-photosynthetic plastids have also been reduced structurally. Some of these non-photosynthetic or "cryptic" plastids were overlooked or unrecognized for decades. The number of complete plastid genome sequences and/or transcriptomes from non-photosynthetic taxa possessing plastids is rapidly increasing, thus allowing prediction of the functions of non-photosynthetic plastids in various eukaryotic lineages. In some non-photosynthetic eukaryotes with photosynthetic ancestors, no traces of plastid genomes or of plastids have been found, suggesting that they have lost the genomes or plastids completely. This review summarizes current knowledge of non-photosynthetic plastids, their genomes, structures and potential functions in free-living and parasitic plants, algae and protists. We introduce a model for the order of plastid gene losses which combines models proposed earlier for land plants with the patterns of gene retention and loss observed in protists. The rare cases of plastid genome loss and complete plastid loss are also discussed.
- Keywords
- Essential metabolic pathways, Non-photosynthetic plastids, Parasitism, Plastid genome, Plastid loss,
- MeSH
- Biological Evolution MeSH
- Chloroplasts genetics MeSH
- Photosynthesis genetics MeSH
- Phylogeny MeSH
- Genome genetics MeSH
- Plastids genetics MeSH
- Plants genetics MeSH
- Cyanobacteria genetics growth & development MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
Rheb is a conserved and widespread Ras-like GTPase involved in cell growth regulation mediated by the (m)TORC1 kinase complex and implicated in tumourigenesis in humans. Rheb function depends on its association with membranes via prenylated C-terminus, a mechanism shared with many other eukaryotic GTPases. Strikingly, our analysis of a phylogenetically rich sample of Rheb sequences revealed that in multiple lineages this canonical and ancestral membrane attachment mode has been variously altered. The modifications include: (1) accretion to the N-terminus of two different phosphatidylinositol 3-phosphate-binding domains, PX in Cryptista (the fusion being the first proposed synapomorphy of this clade), and FYVE in Euglenozoa and the related undescribed flagellate SRT308; (2) acquisition of lipidic modifications of the N-terminal region, namely myristoylation and/or S-palmitoylation in seven different protist lineages; (3) acquisition of S-palmitoylation in the hypervariable C-terminal region of Rheb in apusomonads, convergently to some other Ras family proteins; (4) replacement of the C-terminal prenylation motif with four transmembrane segments in a novel Rheb paralog in the SAR clade; (5) loss of an evident C-terminal membrane attachment mechanism in Tremellomycetes and some Rheb paralogs of Euglenozoa. Rheb evolution is thus surprisingly dynamic and presents a spectacular example of molecular tinkering.
- MeSH
- Cell Membrane metabolism MeSH
- Euglenozoa genetics metabolism MeSH
- Phylogeny * MeSH
- Euglenozoa Infections parasitology MeSH
- Carcinogenesis genetics metabolism MeSH
- Humans MeSH
- Evolution, Molecular MeSH
- Ras Homolog Enriched in Brain Protein chemistry genetics metabolism MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Ras Homolog Enriched in Brain Protein MeSH
- RHEB protein, human MeSH Browser