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

2019 ◽  
Author(s):  
Zoltán Füssy ◽  
Kristína Záhonová ◽  
Aleš Tomčala ◽  
Juraj Krajčovič ◽  
Vyacheslav Yurchenko ◽  
...  
Keyword(s):  
Euglena Gracilis ◽  
Physiological Role ◽  
Redox Status ◽  
Secondary Endosymbiosis ◽  
Metabolic Functions ◽  
Green Algal ◽  
Photosynthetic Eukaryotes ◽  
Algal Groups ◽  
New Type ◽  
Green Flagellate

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.

scholarly journals The Cryptic Plastid of Euglena longa Defines a New Type of Nonphotosynthetic Plastid Organelle

mSphere ◽  
2020 ◽  
Vol 5 (5) ◽  
Author(s):  
Zoltán Füssy ◽  
Kristína Záhonová ◽  
Aleš Tomčala ◽  
Juraj Krajčovič ◽  
Vyacheslav Yurchenko ◽  
...  
Keyword(s):  
Euglena Gracilis ◽  
Physiological Role ◽  
Redox Balance ◽  
Redox Status ◽  
Secondary Endosymbiosis ◽  
Content Type ◽  
Metabolic Functions ◽  
Green Algal ◽  
Thioredoxin System ◽  
Algal Groups

ABSTRACT 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.

scholarly journals Purification and some properties of cytosolic cobalamin-binding protein in Euglena gracilis

1987 ◽  
Vol 247 (3) ◽  
pp. 679-685 ◽  
Author(s):  
F Watanabe ◽  
Y Nakano ◽  
S Kitaoka
Keyword(s):  
Euglena Gracilis ◽  
Binding Proteins ◽  
Microsomal Fraction ◽  
Binding Protein ◽  
Physiological Role ◽  
Binding Activity ◽  
Thiol Groups ◽  
Double Immunodiffusion ◽  
Ph Dependency ◽  
Ks Values

In Euglena gracilis SM-ZK, a bleached mutant of E. gracilis z, the cobalamin- (Cbl-)binding activity was distributed in cytosol (49.2%), mitochondria (20.3%) and microsomal fraction (20.4%). The cytosolic Cbl-binding activity gave two major peaks in isoelectric focusing. The Cbl-binding protein with pI 3.2 was purified 6500-fold in a yield of 19.9%, and that with pI 4.7 5800-fold in a yield of 11.9%. The monomeric Mr values of both Cbl-binding proteins were about 66,000. The Cbl-binding activity of both proteins showed a very low pH-dependency, and thiol groups and metal ions were not concerned with the Cbl-binding activities. The Ks values of the Cbl-binding proteins with pI 3.8 and 4.7 for CN-Cbl were 1.0 and 2.0 nM respectively. The Cbl-binding protein with pI 3.8 was shown to be immunologically identical with the protein with pI 4.7 by double-immunodiffusion experiments against antibody to the protein with pI 3.8. The two cytosolic Cbl-binding proteins did not show the activities of Cbl-dependent enzymes in E. gracilis, N5-methyltetrahydrofolate:homocysteine methyltransferase, methylmalonyl-CoA mutase and ribonucleotide reductase, suggesting that the two cytosolic Cbl-binding proteins play a physiological role as intracellular Cbl carriers.

scholarly journals Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis

2020 ◽  
Vol 117 (10) ◽  
pp. 5364-5375 ◽  
Author(s):  
Chihiro Sarai ◽  
Goro Tanifuji ◽  
Takuro Nakayama ◽  
Ryoma Kamikawa ◽  
Kazuya Takahashi ◽  
...  
Keyword(s):  
Phylogenetic Analyses ◽  
Evolutionary Process ◽  
Dna Transfer ◽  
Free Living ◽  
Genus Level ◽  
Green Algal ◽  
Endosymbiotic Alga ◽  
Two Systems ◽  
Algal Groups ◽  
Genetic Level

Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which endosymbiont-to-host DNA transfer is on-going and for which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. With the combined evidence, we conclude that the host–endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.

The complexity and evolution of the plastid-division machinery

2010 ◽  
Vol 38 (3) ◽  
pp. 783-788 ◽  
Author(s):  
Jodi Maple ◽  
Simon Geir Møller
Keyword(s):  
Molecular Mechanisms ◽  
Environmental Changes ◽  
Cell Types ◽  
Cellular Level ◽  
Plastid Division ◽  
Bacterial Cell Division ◽  
Metabolic Functions ◽  
Photosynthetic Eukaryotes ◽  
Metabolic Output ◽  
Host Nucleus

Plastids are vital organelles, fulfilling important metabolic functions that greatly influence plant growth and productivity. In order to both regulate and harness the metabolic output of plastids, it is vital that the process of plastid division is carefully controlled. This is essential, not only to ensure persistence in dividing plant cells and that optimal numbers of plastids are obtained in specialized cell types, but also to allow the cell to act in response to developmental signals and environmental changes. How this control is exerted by the host nucleus has remained elusive. Plastids evolved by endosymbiosis and during the establishment of a permanent endosymbiosis they retained elements of the bacterial cell-division machinery. Through evolution the photosynthetic eukaryotes have increased dramatically in complexity, from single-cell green algae to multicellular non-vascular and vascular plants. Reflected with this is an increasing complexity of the division machinery and recent findings also suggest increasing complexity in the molecular mechanisms used by the host cell to control the process of plastid division. In the present paper, we explore the current understanding of the process of plastid division at the molecular and cellular level, with particular respect to the evolution of the division machinery and levels of control exerted on the process.

scholarly journals The endosymbiotic origin, diversification and fate of plastids

2010 ◽  
Vol 365 (1541) ◽  
pp. 729-748 ◽  
Author(s):  
Patrick J. Keeling
Keyword(s):  
Green Algae ◽  
Red Algae ◽  
Protein Trafficking ◽  
Molecular Data ◽  
Secondary Endosymbiosis ◽  
Plastid Evolution ◽  
Evolutionary Transitions ◽  
Green Algal ◽  
Endosymbiotic Event ◽  
Plastid Loss

Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.

scholarly journals Physiological role of rhodoquinone in Euglena gracilis mitochondria

2005 ◽  
Vol 1710 (2-3) ◽  
pp. 113-121 ◽  
Author(s):  
Norma A. Castro-Guerrero ◽  
Ricardo Jasso-Chávez ◽  
Rafael Moreno-Sánchez
Keyword(s):  
Euglena Gracilis ◽  
Physiological Role
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