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Phylogenetic Relationships and Morphological Character Evolution of Photosynthetic Euglenids (Excavata) Inferred from Taxon-rich Analyses of Five Genes

Published on May 1, 2015in Journal of Eukaryotic Microbiology 2.36
· DOI :10.1111/jeu.12192
Anna Karnkowska6
Estimated H-index: 6
(University of Warsaw),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University)
+ 3 AuthorsRichard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
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Abstract
Photosynthetic euglenids acquired chloroplasts by secondary endosymbiosis, which resulted in changes to their mode of nutrition and affected the evolution of their morphological characters. Mapping morphological characters onto a reliable molecular tree could elucidate major trends of those changes. We analyzed nucleotide sequence data from regions of three nuclear-encoded genes (nSSU, nLSU, hsp90), one chloroplast-encoded gene (cpSSU) and one nuclear-encoded chloroplast gene (psbO) to estimate phylogenetic relationships among 59 photosynthetic euglenid species. Our results were consistent with previous works; most genera were monophyletic, except for the polyphyletic genus Euglena, and the paraphyletic genus Phacus. We also analyzed character evolution in photosynthetic euglenids using our phylogenetic tree and eight morphological traits commonly used for generic and species diagnoses, including: characters corresponding to well-defined clades, apomorphies like presence of lorica and mucilaginous stalks, and homoplastic characters like rigid cells and presence of large paramylon grains. This research indicated that pyrenoids were lost twice during the evolution of phototrophic euglenids, and that mucocysts, which only occur in the genus Euglena, evolved independently at least twice. In contrast, the evolution of cell shape and chloroplast morphology was difficult to elucidate, and could not be unambiguously reconstructed in our analyses.
  • References (70)
  • Citations (17)
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References70
Newest
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 Nov 1, 2013in Journal of Eukaryotic Microbiology 2.36
Gordon Lax3
Estimated H-index: 3
(TUK: Kaiserslautern University of Technology),
Alastair G. B. Simpson39
Estimated H-index: 39
(CIFAR: Canadian Institute for Advanced Research)
Phagotrophic euglenids are one of the most diverse and important forms of heterotrophic flagellates in sediment systems, and are key to understanding the evolution of photosynthetic euglenids and ‘primary osmotrophs’, yet relatively little is known about their biodiversity and phylogenetic relationships. A wealth of light microscopy-based information is available, but little progress has been made in associating this with molecular sequence data. We established a protocol to obtain light microsc...
16 Citations Source Cite
Published on Jun 1, 2013in Journal of Phycology 2.83
Anna Karnkowska-Ishikawa8
Estimated H-index: 8
(University of Warsaw),
Rafał Milanowski11
Estimated H-index: 11
(University of Warsaw)
+ 1 AuthorsBożena Zakryś11
Estimated H-index: 11
(University of Warsaw)
Euglena sanguinea (Ehrenberg 1831) was one of the first green euglenoid species described in the literature. At first, the species aroused the interest of researchers mainly due to the blood-red color of its cells, which, as it later turned out, is not a constant feature. Complicated chloroplast morphology, labeled by Pringsheim as the "peculiar chromatophore system", made the correct identification of the species difficult, which is the reason why, throughout the 20th century, new species resem...
9 Citations Source Cite
Published on Jun 1, 2012in Journal of Phycology 2.83
Anna Karnkowska-Ishikawa8
Estimated H-index: 8
(University of Warsaw),
Rafał Milanowski11
Estimated H-index: 11
(University of Warsaw)
+ 1 AuthorsBożena Zakryś11
Estimated H-index: 11
(University of Warsaw)
The establishment of epitypes (together with the emended diagnoses) for three species of Euglenaria Karnkowska, E. W. Linton et Kwiatowski [Eu. anabaena (Mainx) Karnkowska et E. W. Linton; Eu. caudata (Hubner) Karnkowska et E. W. Linton; and Eu. clavata (Skuja) Karnkowska et E. W. Linton] and two species of Euglena Ehrenberg [E. granulata (Klebs) Schmitz and E. velata Klebs] was achieved due to literature studies, verification of morphological diagnostic features (cell size, cell shape, number o...
13 Citations Source Cite
Published on May 1, 2012in Systematic Biology 10.27
Fredrik Ronquist45
Estimated H-index: 45
(Swedish Museum of Natural History),
Maxim Teslenko2
Estimated H-index: 2
(Swedish Museum of Natural History)
+ 7 AuthorsJohn P. Huelsenbeck58
Estimated H-index: 58
(University of California, Berkeley)
Since its introduction in 2001, MrBayes has grown in popularity as a software package for Bayesian phylogenetic inference using Markov chain Monte Carlo (MCMC) methods. With this note, we announce the release of version 3.2, a major upgrade to the latest official release presented in 2003. The new version provides convergence diagnostics and allows multiple analyses to be run in parallel with convergence progress monitored on the fly. The introduction of new proposals and automatic optimization ...
7,600 Citations Source Cite
Published on Feb 1, 2012in Journal of Phycology 2.83
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
One of the foremost issues in the field of algal taxonomy is the inability to acquire, grow, and sequence new taxa. This problem is particularly true in the study of photosynthetic euglenoids where most of the distinct taxa in culture collections have been sequenced, and many other taxa of interest have been resistant to culturing, and thus, sequencing. In an effort to address this problem, we have utilized a new technique, novel to the field of taxonomy, which allows for the sequencing of nucle...
15 Citations Source Cite
Published on Jan 1, 2012in BMC Evolutionary Biology 3.04
Aika Yamaguchi12
Estimated H-index: 12
(UBC: University of British Columbia),
Naoji Yubuki15
Estimated H-index: 15
(UBC: University of British Columbia),
Brian S. Leander35
Estimated H-index: 35
(UBC: University of British Columbia)
Background Morphostasis of traits in different species is necessary for reconstructing the evolutionary history of complex characters. Studies that place these species into a molecular phylogenetic context test hypotheses about the transitional stages that link divergent character states. For instance, the transition from a phagotrophic mode of nutrition to a phototrophic lifestyle has occurred several times independently across the tree of eukaryotes; one of these events took place within the E...
40 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
Published on Jun 1, 2011in Journal of Phycology 2.83
Anna Karnkowska-Ishikawa8
Estimated H-index: 8
(University of Warsaw),
Rafał Milanowski11
Estimated H-index: 11
(University of Warsaw),
Bożena Zakryś11
Estimated H-index: 11
(University of Warsaw)
For this study, we have examined the literature and the morphological diversity, as well as analyzed the nuclear SSU rDNA sequences of two very common and cosmopolitan species formerly known as Euglena deses Ehrenb. and Euglena intermedia (G. A. Klebs) F. Schmitz. Our studies have shown that there is evidence for distinguishing only one species (E. deses). Here, we define new diagnostic features for E. deses, namely, periplast ornamentation (the presence of small papillae—discovered for the firs...
8 Citations Source Cite
Cited By17
Newest
Published on May 16, 2019in Biological Reviews 10.29
Matej Vesteg9
Estimated H-index: 9
,
Lucia Hadariová2
Estimated H-index: 2
(Charles University in Prague)
+ 3 AuthorsJuraj Krajčovič17
Estimated H-index: 17
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Published on May 1, 2019in Nature Physics 20.11
Giovanni Noselli12
Estimated H-index: 12
(SISSA: International School for Advanced Studies),
Alfred Beran1
Estimated H-index: 1
+ 1 AuthorsAntonio DeSimone35
Estimated H-index: 35
(SISSA: International School for Advanced Studies)
Some euglenids, a family of aquatic unicellular organisms, can develop highly concerted, large-amplitude peristaltic body deformations. This remarkable behaviour has been known for centuries. Yet, its function remains controversial, and is even viewed as a functionless ancestral vestige. Here, by examining swimming Euglena gracilis in environments of controlled crowding and geometry, we show that this behaviour is triggered by confinement. Under these conditions, it allows cells to switch from u...
3 Citations Source Cite
Published on Apr 1, 2019in Protist 3.00
Gordon Lax3
Estimated H-index: 3
(Dal: Dalhousie University),
Won Je Lee6
Estimated H-index: 6
(Kyungnam University)
+ 1 AuthorsAlastair G. B. Simpson39
Estimated H-index: 39
(Dal: Dalhousie University)
Ploeotids are an assemblage of rigid phagotrophic euglenids that have 10–12 pellicular strips and glide on their posterior flagellum. Molecular phylogenies place them as a poorly resolved, likely paraphyletic assemblage outside the Spirocuta clade of flexible euglenids, which includes the well-known phototrophs and primary osmotrophs. Here, we report SSU rRNA gene sequences from 38 ploeotids, using both single-cell and culture-based methods. Several contain group I or non-canonical introns. Our ...
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Published on Dec 1, 2018in Journal of Applied Phycology 2.63
Madhavi Ellala Hewadikaramge (CMU: Central Michigan University), Eric W. Linton10
Estimated H-index: 10
(CMU: Central Michigan University)
The genus Euglena is composed of six subclades with a diversity of chloroplast morphologies, unlike that found in the other genera of Euglenaceae. This genus contains five published chloroplast genomes (cpGenome) and the colorless plastid genome (ptGenome) of the non-photosynthetic euglenoid Euglena longa within the same subclade as Euglena gracilis. Previous studies of cpGenomes revealed that Euglena viridis and E. gracilis, although in separate subclades, had few cpGenome differences, while Eu...
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Published on Dec 1, 2018in Scientific Reports 4.01
Anna Karnkowska6
Estimated H-index: 6
(University of Warsaw),
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
Photosynthetic euglenids (Euglenophyta) are a monophyletic group of unicellular eukaryotes characterized by the presence of plastids, which arose as the result of the secondary endosymbiosis. Many Euglenophyta plastid (pt) genomes have been characterized recently, but they represented mainly one family – Euglenaceae. Here, we report a comparative analysis of plastid genomes from eight representatives of the family Phacaceae. Newly sequenced plastid genomes share a number of features including sy...
1 Citations Source Cite
Published on Mar 1, 2018in Harmful Algae 5.01
Yeong Du Yoo26
Estimated H-index: 26
(Kunsan National University),
Kyeong Ah Seong19
Estimated H-index: 19
(Kunsan National University)
+ 6 AuthorsBrian Palenik42
Estimated H-index: 42
(UCSD: University of California, San Diego)
Abstract The phototrophic euglenophyte Eutreptiella eupharyngea often causes blooms in the coastal waters of many countries, but its mode of nutrition has not been assessed. This species has previously been considered as exclusively auxotrophic. To explore whether E. eupharyngea is a mixotrophic species, the protoplasm of E. eupharyngea cells were examined using light, epifluorescence, and transmission electron microscopy after eubacteria, the cyanobacterium Synechococcus sp., and diverse algal ...
1 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 Jun 1, 2017in Journal of Phycology 2.83
Matthew S. Bennett11
Estimated H-index: 11
(MSU: Michigan State University),
Shin Han Shiu43
Estimated H-index: 43
(MSU: Michigan State University),
Richard E. Triemer25
Estimated H-index: 25
(MSU: Michigan State University)
4 Citations Source Cite
Published on May 1, 2017in Current Genetics 3.46
Lucia Hadariová2
Estimated H-index: 2
(Comenius University in Bratislava),
Matej Vesteg9
Estimated H-index: 9
(Matej Bel University)
+ 2 AuthorsJuraj Krajčovič17
Estimated H-index: 17
(Comenius University in Bratislava)
Euglena gracilis growth with antibacterial agents leads to bleaching, permanent plastid gene loss. Colorless Euglena (Astasia) longa resembles a bleached E. gracilis. To evaluate the role of bleaching in E. longa evolution, the effect of streptomycin, a plastid protein synthesis inhibitor, and ofloxacin, a plastid DNA gyrase inhibitor, on E. gracilis and E. longa growth and plastid DNA content were compared. E. gracilis growth was unaffected by streptomycin and ofloxacin. Quantitative PCR analys...
4 Citations Source Cite