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

Published on May 1, 2016in Journal of Eukaryotic Microbiology 2.36
· DOI :10.1111/jeu.12282
Chelsea M. Markunas1
Estimated H-index: 1
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
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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)
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References43
Newest
Published on Nov 1, 2015in Journal of Eukaryotic Microbiology 2.36
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: 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 Jun 1, 2014in Journal of Phycology 2.83
John W. Stiller24
Estimated H-index: 24
(ECU: East Carolina University)
The idea that evolutionary models should minimize plastid endosymbioses has dominated thinking about the history of eukaryotic photosynthesis. Although a reasonable starting point, this framework has not gained support from observed patterns of algal and plant evolution, and can be an obstacle to fully understanding the modern distribution of plastids. Empirical data indicate that plastid losses are extremely uncommon, that major changes in plastid biochemistry/architecture are evidence of an en...
22 Citations Source Cite
Published on Jan 1, 2014in Phycologia 1.98
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Krystle E. Wiegert5
Estimated H-index: 5
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
Euglena proxima is a common, globally dispersed, and easily identified photosynthetic euglenoid. Previous phylogenetic analyses using nuclear-encoded small subunit (SSU) and large subunit (LSU) rRNA genes revealed that this taxon was paraphyletic with other Euglena species and was positioned as sister to all Euglenaceae. Despite this, authors were reluctant to remove this taxon from Euglena until additional data, or taxa pairing with E. proxima, were obtained because it created a monotypic genus...
20 Citations Source Cite
Published on Mar 1, 2013in Journal of Eukaryotic Microbiology 2.36
Krystle E. Wiegert5
Estimated H-index: 5
(MSU: Michigan State University),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: 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 Nov 1, 2012in Phycologia 1.98
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Krystle E. Wiegert5
Estimated H-index: 5
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
Bennett M.S., Wiegert K.E. and Triemer R.E. 2012. Comparative chloroplast genomics between Euglena viridis and Euglena gracilis (Euglenophyta). Phycologia 51: 711–718. DOI: 10.2216/12-017.1 The chloroplast genomes of Euglena gracilis, Eutreptia viridis, Eutreptiella gymnastica, Colacium vesiculosum, Strombomonas acuminata and the colourless Euglena (Astasia) longa, which had secondarily lost the ability to photosynthesize, were previously reported. These studies had shown that there was a great ...
16 Citations Source Cite
Published on Nov 1, 2012in Protist 3.00
Krystle E. Wiegert5
Estimated H-index: 5
(MSU: Michigan State University),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: 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
Published on Mar 20, 2012in PLOS ONE 2.78
Štěpánka Hrdá4
Estimated H-index: 4
(Charles University in Prague),
Jan Fousek6
Estimated H-index: 6
(CAS: Academy of Sciences of the Czech Republic)
+ 2 AuthorsCestmir Vlcek30
Estimated H-index: 30
(CAS: 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 Feb 1, 2012in PLOS ONE 2.78
Ravi K. Patel7
Estimated H-index: 7
,
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...
1,020 Citations Source Cite
Published on Jan 1, 2012in Integrative Biology 2.77
Laura Barsanti20
Estimated H-index: 20
,
Valtere Evangelista10
Estimated H-index: 10
+ 2 AuthorsPaolo Gualtieri19
Estimated H-index: 19
The ability to sense light can be considered the most fundamental and presumably the most ancient property of visual systems. This ability is the basis of phototaxis, one of the most striking behavioral responses of motile photosynthetic microorganisms (i.e. microalgae) to light stimuli, which allows them to move toward or away directional light. In order to fully exploit the information content of light (intensity, direction, distribution) microorganisms need proper perceiving devices, termed p...
9 Citations Source Cite
Published on Dec 1, 2011in BMC Evolutionary Biology 3.04
Shinichiro Maruyama16
Estimated H-index: 16
(UTokyo: University of Tokyo),
Toshinobu Suzaki4
Estimated H-index: 4
(Kobe University)
+ 2 AuthorsHisayoshi Nozaki35
Estimated H-index: 35
(UTokyo: University of Tokyo)
Background Euglenophytes are a group of photosynthetic flagellates possessing a plastid derived from a green algal endosymbiont, which was incorporated into an ancestral host cell via secondary endosymbiosis. However, the impact of endosymbiosis on the euglenophyte nuclear genome is not fully understood due to its complex nature as a 'hybrid' of a non-photosynthetic host cell and a secondary endosymbiont.
35 Citations Source Cite
Cited By7
Newest
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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Published on Sep 1, 2018in Molecular Biology and Evolution 14.80
Rafael I Ponce-Toledo1
Estimated H-index: 1
(Université Paris-Saclay),
David Moreira54
Estimated H-index: 54
(Université Paris-Saclay)
+ 1 AuthorsPhilippe Deschamps2
Estimated H-index: 2
(Université Paris-Saclay)
3 Citations Source Cite
Published on Aug 14, 2017in Advances in Botanical Research 2.29
Anna M. G. Novák 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 Feb 1, 2017in Journal of Phycology 2.83
Bryan Lakey1
Estimated H-index: 1
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: 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 Jan 1, 2017
Bożena Zakryś11
Estimated H-index: 11
(University of Warsaw),
Rafał Milanowski11
Estimated H-index: 11
(University of Warsaw),
Anna Karnkowska6
Estimated H-index: 6
(University of Warsaw)
Euglenids (Excavata, Discoba, Euglenozoa, Euglenida) is a group of free-living, single-celled flagellates living in the aquatic environments. The uniting and unique morphological feature of euglenids is the presence of a cell covering called the pellicle. The morphology and organization of the pellicle correlate well with the mode of nutrition and cell movement. Euglenids exhibit diverse modes of nutrition, including phagotrophy and photosynthesis. Photosynthetic species (Euglenophyceae) constit...
6 Citations Source Cite
Published on Mar 16, 2016in Frontiers in Ecology and Evolution
Carlos Eduardo de Mattos Bicudo14
Estimated H-index: 14
,
Mariângela Menezes8
Estimated H-index: 8
(UFRJ: 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