Evolutionary History of the Enzymes Involved in the Calvin–Benson Cycle in Euglenids

Published on May 1, 2016in Journal of Eukaryotic Microbiology 2.54
· DOI :10.1111/jeu.12282
Chelsea M. Markunas1
Estimated H-index: 1
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
Abstract
Euglenids are an ancient lineage that may have existed as early as 2 billion years ago. A mere 65 years ago, Melvin Calvin and Andrew A. Benson performed experiments on Euglena gracilis and elucidated the series of reactions by which carbon was fixed and reduced during photosynthesis. However, the evolutionary history of this pathway (Calvin-Benson cycle) in euglenids was more complex than Calvin and Benson could have imagined. The chloroplast present today in euglenophytes arose from a secondary endosymbiosis between a phagotrophic euglenid and a prasinophyte green alga. A long period of evolutionary time existed before this secondary endosymbiotic event took place, which allowed for other endosymbiotic events or gene transfers to occur prior to the establishment of the green chloroplast. This research revealed the evolutionary history of the major enzymes of the Calvin-Benson cycle throughout the euglenid lineage and showed that the majority of genes for Calvin-Benson cycle enzymes shared an ancestry with red algae and/or chromophytes suggesting they may have been transferred to the nucleus prior to the acquisition of the green chloroplast.
  • References (43)
  • Citations (7)
Cite
References43
Published on Jan 1, 1959in Journal of Bacteriology 3.22
O. Holm-Hansen1
Estimated H-index: 1
,
V. Moses1
Estimated H-index: 1
,
Melvin Calvin64
Estimated H-index: 64
Studies by Lynch and Calvin (1952,1953) have established the nature of the compounds incorporating C{sup 14} nonphotosynthetically from C{sup 14}O{sub 2} in thirteen microorganisms: a yeast, a protozoan, two water moulds, one slime mould, three algae, three bacteria, and the green flagellate Euglena Gracilis. With the exception of H. gracilis, and of Lactobacillus cassi which fixed no detectable amounts of carbon dioxide, all these organisms fixed carbon dioxide into amino and organic acids deri...
22 Citations Source Cite
Published on Nov 1, 2015in Journal of Eukaryotic Microbiology 2.54
Matthew S. Bennett11
Estimated H-index: 11
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
Over the last few years multiple studies have been published outlining chloroplast genomes that represent many of the photosynthetic euglenid genera. However, these genomes were scattered throughout the euglenophyceaean phylogenetic tree, and focused on comparisons with Euglena gracilis. Here, we present a study exclusively on taxa within the Euglenaceae. Six new chloroplast genomes were characterized, those of Cryptoglena skujai, E. gracilis var. bacillaris, Euglena viridis, Euglenaria anabaena...
22 Citations Source Cite
Published on Feb 1, 2012in PLOS ONE 2.77
Ravi Patel8
Estimated H-index: 8
,
Mukesh K. Jain64
Estimated H-index: 64
Next generation sequencing (NGS) technologies provide a high-throughput means to generate large amount of sequence data. However, quality control (QC) of sequence data generated from these technologies is extremely important for meaningful downstream analysis. Further, highly efficient and fast processing tools are required to handle the large volume of datasets. Here, we have developed an application, NGS QC Toolkit, for quality check and filtering of high-quality data. This toolkit is a standa...
957 Citations Source Cite
Published on Mar 1, 2009in Molecular Biology and Evolution 10.22
Monique Turmel41
Estimated H-index: 41
(Laval University),
Marie-Christine Gagnon1
Estimated H-index: 1
(Laval University)
+ 2 AuthorsClaude Lemieux45
Estimated H-index: 45
(Laval University)
Because they represent the earliest divergences of the Chlorophyta and include the smallest known eukaryotes (e.g., the coccoid Ostreococcus), the morphologically diverse unicellular green algae making up the Prasinophyceae are central to our understanding of the evolutionary patterns that accompanied the radiation of chlorophytes and the reduction of cell size in some lineages. Seven prasinophyte lineages, four of which exhibit a coccoid cell organization (no flagella nor scales), were uncovere...
142 Citations Source Cite
Published on Mar 20, 2012in PLOS ONE 2.77
Štěpánka Hrdá4
Estimated H-index: 4
(Charles University in Prague),
Jan Fousek6
Estimated H-index: 6
(Academy of Sciences of the Czech Republic)
+ 2 AuthorsCestmir Vlcek30
Estimated H-index: 30
(Academy of Sciences of the Czech Republic)
Euglenids are a group of protists that comprises species with diverse feeding modes. One distinct and diversified clade of euglenids is photoautotrophic, and its members bear green secondary plastids. In this paper we present the plastid genome of the euglenid Eutreptiella, which we assembled from 454 sequencing of Eutreptiella gDNA. Comparison of this genome and the only other available plastid genomes of photosynthetic euglenid, Euglena gracilis, revealed that they contain a virtually identica...
36 Citations Source Cite
Published on Apr 1, 1995in Biochimica et Biophysica Acta 3.44
Matthias Schmidt10
Estimated H-index: 10
(Goethe University Frankfurt),
Ib Svendsen43
Estimated H-index: 43
(Carlsberg Laboratory),
Jürgen Feierabend23
Estimated H-index: 23
(Goethe University Frankfurt)
Abstract The primary structure of the chloroplast isozyme of triosephosphate isomerase from rye leaves was identified by protein and cDNA sequencing and compared to the deduced amino acid sequence of a cDNA for the cytosolic isozyme. The mature cytosolic and chloroplast isozyme proteins share 64% amino acid sequence identity. The cDNA for the chloroplast isozyme codes for a precursor protein consisting of an N-terminal transit peptide of M r 4351 and a mature subunit of M r 27282. Southern blot ...
27 Citations Source Cite
Published on Mar 1, 2013in Journal of Eukaryotic Microbiology 2.54
Krystle E. Wiegert5
Estimated H-index: 5
(Michigan State University),
Matthew S. Bennett11
Estimated H-index: 11
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
The chloroplast genomes of two photosynthetic euglenoids, Colacium vesiculosum Ehrenberg (128,889 bp), and Strombomonas acuminata (Schmarda) Deflandre (144,167 bp) have been sequenced. These chloroplast genomes in combination with those of Euglena gracilis, Eutreptia viridis, and Eutreptiella gymnastica provide a snapshot of euglenoid chloroplast evolution allowing comparisons of gene content, arrangement, and expansion. The gene content of the five chloroplast genomes is very similar varying on...
18 Citations Source Cite
Published on Jul 1, 2011in Journal of Bacteriology 3.22
Di Wang2
Estimated H-index: 2
(University of Minnesota),
Yaoping Zhang20
Estimated H-index: 20
(University of Minnesota)
+ 2 AuthorsGary P. Roberts42
Estimated H-index: 42
(University of Wisconsin-Madison)
Ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) catalyzes the first step of CO2 fixation in the Calvin-Benson-Bassham (CBB) cycle. Besides its function in fixing CO2 to support photoautotrophic growth, the CBB cycle is also important under photoheterotrophic growth conditions in purple nonsulfur photosynthetic bacteria. It has been assumed that the poor photoheterotrophic growth of RubisCO-deficient strains was due to the accumulation of excess intracellular reductant, which implied th...
21 Citations Source Cite
Published on Nov 1, 2012in Protist 2.70
Krystle E. Wiegert5
Estimated H-index: 5
(Michigan State University),
Matthew S. Bennett11
Estimated H-index: 11
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
The chloroplast genome of Eutreptia viridis Perty, a basal taxon in the photosynthetic euglenoid lineage, was sequenced and compared with that of Euglena gracilis Ehrenberg, a crown species. Several common gene clusters were identified and gene order, conservation, and sequence similarity was assessed through comparisons with Euglena gracilis . Significant gene rearrangements were present between Eutreptia viridis and Euglena gracilis chloroplast genomes. In addition, major expansion has occurre...
26 Citations Source Cite
Cited By7
Published on Mar 16, 2016in Frontiers in Ecology and Evolution
Carlos Eduardo de Mattos Bicudo2
Estimated H-index: 2
,
Mariângela Menezes7
Estimated H-index: 7
(Federal University of Rio de Janeiro)
Euglenophyceae (phototrophic euglenids) are an important lineage within the Euglenida, Euglenozoa. Most of the approximately 3,000 described species are free-living, phototrophic, unicellular flagellates with one to several plastids of secondary origin, three bounding membranes and chlorophylls a and b; but, the lineage also includes colorless species that lost their photosynthesizing capability. They show a typical cell membrane consisting of parallel proteinaceous strips and microtubules locat...
5 Citations Source Cite
Published on Feb 1, 2017in Journal of Phycology 3.00
Bryan Lakey1
Estimated H-index: 1
(Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(Michigan State University)
The history of euglenoids may have begun as early as ~2 bya. These early phagotrophs ate cyanobacteria, archaea, and eubacteria, and the subsequent appearance of red algae and chromalveolates provided euglenoids with additional food sources. Following the appearance of green algae, euglenoids acquired a chloroplast via a secondary endosymbiotic event with a green algal ancestor. This endosymbiosis also involved a massive transfer of nuclear-encoded genes from the symbiont nucleus to the host. Ex...
4 Citations Source Cite
Published on Aug 14, 2017in Advances in Botanical Research 1.39
Anna M.G. Vanclová2
Estimated H-index: 2
(Charles University in Prague),
Lucia Hadariová2
Estimated H-index: 2
(Charles University in Prague)
+ 1 AuthorsVladimír Hampl21
Estimated H-index: 21
(Charles University in Prague)
Abstract Euglenophytes obtained their plastids from a primary green alga related to extant genus Pyramimonas . The relatively recent establishment of this new organelle is an intriguing evolutionary phenomenon worth studying and comparing with other secondary plastids with a regard to their similarities and differences. A remarkably fast evolution driven by rapid intron gain and diversification is observed in euglenid plastid genomes which often tend to swell in size and rearrange while keeping ...
2 Citations Source Cite
Published on Sep 1, 2018in Molecular Biology and Evolution 10.22
Rafael I Ponce-Toledo1
Estimated H-index: 1
(Université Paris-Saclay),
David Moreira52
Estimated H-index: 52
(Université Paris-Saclay)
+ 1 AuthorsPhilippe Deschamps1
Estimated H-index: 1
(Université Paris-Saclay)
1 Citations Source Cite
Published on Dec 1, 2018in Scientific Reports 4.12
Kristína Záhonová4
Estimated H-index: 4
(University of Ostrava),
Zoltán Füssy6
Estimated H-index: 6
+ 6 AuthorsMarek Eliáš27
Estimated H-index: 27
(University of Ostrava)
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 characteris...
3 Citations Source Cite
Published on Mar 11, 2019in bioRxiv
A. M. Novak Vanclova , Martin Zoltner8
Estimated H-index: 8
+ 9 AuthorsJulius Lukeš50
Estimated H-index: 50
Euglena gracilis is a well-studied biotechnologically exploitable phototrophic flagellate harbouring secondary green plastids. Here we describe its plastid proteome obtained by high-resolution proteomics. We identified 1,345 candidate plastid proteins and assigned functional annotations to 774 of them. More than 120 proteins are affiliated neither to the host lineage nor the plastid ancestor and may represent horizontal acquisitions from various algal and prokaryotic groups. Reconstruction of pl...
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