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The New Red Algal Subphylum Proteorhodophytina Comprises the Largest and Most Divergent Plastid Genomes Known

Published on Jun 1, 2017in Current Biology 9.25
· DOI :10.1016/j.cub.2017.04.054
Sergio A. Muñoz-Gómez6
Estimated H-index: 6
(Dalhousie University),
Fabian G. Mejía-Franco1
Estimated H-index: 1
+ 4 AuthorsClaudio H. Slamovits26
Estimated H-index: 26
(Canadian Institute for Advanced Research)
Abstract
Summary Red algal plastid genomes are often considered ancestral and evolutionarily stable, and thus more closely resembling the last common ancestral plastid genome of all photosynthetic eukaryotes [1, 2]. However, sampling of red algal diversity is still quite limited (e.g., [2–5]). We aimed to remedy this problem. To this end, we sequenced six new plastid genomes from four undersampled and phylogenetically disparate red algal classes (Porphyridiophyceae, Stylonematophyceae, Compsopogonophyceae, and Rhodellophyceae) and discovered an unprecedented degree of genomic diversity among them. These genomes are rich in introns, enlarged intergenic regions, and transposable elements (in the rhodellophycean Bulboplastis apyrenoidosa ), and include the largest and most intron-rich plastid genomes ever sequenced (that of the rhodellophycean Corynoplastis japonica ; 1.13 Mbp). Sophisticated phylogenetic analyses accounting for compositional heterogeneity show that these four "basal" red algal classes form a larger monophyletic group, Proteorhodophytina subphylum nov., and confidently resolve the large-scale relationships in the Rhodophyta. Our analyses also suggest that secondary red plastids originated before the diversification of all mesophilic red algae. Our genomic survey has challenged the current paradigmatic view of red algal plastid genomes as "living fossils" [1, 2, 6] by revealing an astonishing degree of divergence in size, organization, and non-coding DNA content. A closer look at red algae shows that they comprise the most ancestral (e.g., [2, 7, 8]) as well as some of the most divergent plastid genomes known.
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  • Citations (30)
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References70
Published on Jun 18, 2015in PeerJ 2.12
Marie-Mathilde Perrineau9
Estimated H-index: 9
(Rutgers University),
Dana C. Price19
Estimated H-index: 19
(Rutgers University)
+ 1 AuthorsDebashish Bhattacharya64
Estimated H-index: 64
(Rutgers University)
Group II introns are closely linked to eukaryote evolution because nuclear spliceosomal introns and the small RNAs associated with the spliceosome are thought to trace their ancient origins to these mobile elements. Therefore, elucidating how group II introns move, and how they lose mobility can potentially shed light on fundamental aspects of eukaryote biology. To this end, we studied five strains of the unicellular red alga Porphyridium purpureum that surprisingly contain 42 group II introns i...
9 Citations Source Cite
Published on Apr 1, 2012in Phycological Research 1.27
Asuka Kushibiki1
Estimated H-index: 1
(Yamagata University),
Akiko Yokoyama10
Estimated H-index: 10
(University of Tsukuba)
+ 3 AuthorsYoshiaki Hara19
Estimated H-index: 19
(Yamagata University)
SUMMARY A novel unicellular red alga collected from a mangrove area on Iriomote Island in southwest Japan is described as Bulboplastis apyrenoidosa gen. et sp. nov. The cells are spherical, mean 11.2 µm in diameter, and surrounded by a thick mucilaginous sheath. The grayish-green chloroplast has many lobes extending throughout the cell and lacks a pyrenoid. This chloroplast type is similar to Glaucosphaera vacuolata, but differs from other unicellular red algae. Plastoglobuli clusters occur bene...
6 Citations Source Cite
Hwan Su Yoon24
Estimated H-index: 24
(University of Iowa),
Jeremiah D. Hackett24
Estimated H-index: 24
(University of Iowa)
+ 1 AuthorsDebashish Bhattacharya64
Estimated H-index: 64
(University of Iowa)
Abstract Algae include a diverse array of photosynthetic eukaryotes excluding land plants. Explaining the origin of algal plastids continues to be a major challenge in evolutionary biology. Current knowledge suggests that plastid primary endosymbiosis, in which a single-celled protist engulfs and “enslaves” a cyanobacterium, likely occurred once and resulted in the primordial alga. This eukaryote then gave rise through vertical evolution to the red, green, and glaucophyte algae. However, some mo...
281 Citations Source Cite
Published on Aug 1, 2001in Genome Biology 13.21
Natalia Volfovsky15
Estimated H-index: 15
,
Brian J. Haas45
Estimated H-index: 45
,
Steven L. Salzberg118
Estimated H-index: 118
Background A computational system for analysis of the repetitive structure of genomic sequences is described. The method uses suffix trees to organize and search the input sequences; this data structure has been used previously for efficient computation of exact and degenerate repeats.
118 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
C Bernard1
Estimated H-index: 1
(Centre national de la recherche scientifique),
Jean-Claude Thomas20
Estimated H-index: 20
(Centre national de la recherche scientifique)
+ 4 AuthorsJ P Dubacq1
Estimated H-index: 1
(Centre national de la recherche scientifique)
Abstract The phycobilisome of the eukaryotic unicellular red alga Rhodella violacea presents in some respects an organization that is intermediate between those of the homologous counterparts found in cyanobacteria (the putative chloroplast progenitor) and more advanced, pluricellular red algae. This suggests evolutionary relationships that we investigated at the genome level. The present work describes the sequences of two rhodophytan phycobilisome genes, rpeA and rpeB. These chloroplast genes ...
29 Citations Source Cite
Published on May 1, 2013in Molecular Biology and Evolution 10.22
Bui Quang Minh14
Estimated H-index: 14
(Medical University of Vienna),
Minh Anh Thi Nguyen3
Estimated H-index: 3
(University of Groningen),
Arndt von Haeseler47
Estimated H-index: 47
(Medical University of Vienna)
Nonparametric bootstrap has been a widely used tool in phylogenetic analysis to assess the clade support of phylogenetic trees. However, with the rapidly growing amount of data, this task remains a computational bottleneck. Recently, approximation methods such as the RAxML rapid bootstrap (RBS) and the Shimodaira–Hasegawa-like approximate likelihood ratio test have been introduced to speed up the bootstrap. Here, we suggest an ultrafast bootstrap approximation approach (UFBoot) to compute the su...
484 Citations Source Cite
Published on May 18, 2010in Genome Biology and Evolution 3.94
Jean-Simon Brouard6
Estimated H-index: 6
(Laval University),
Christian Otis34
Estimated H-index: 34
(Laval University)
+ 1 AuthorsMonique Turmel41
Estimated H-index: 41
(Laval University)
The Chlorophyceae, an advanced class of chlorophyte green algae, comprises five lineages that form two major clades (Chlamydomonadales + Sphaeropleales and Oedogoniales + Chaetopeltidales + Chaetophorales). The four complete chloroplast DNA (cpDNA) sequences currently available for chlorophyceans uncovered an extraordinarily fluid genome architecture as well as many structural features distinguishing this group from other green algae. We report here the 521,168-bp cpDNA sequence from a member of...
65 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 May 29, 2013in PLOS ONE 2.77
Li Wang5
Estimated H-index: 5
(Ocean University of China),
Yunxiang Mao10
Estimated H-index: 10
(Ocean University of China)
+ 8 AuthorsHongfan Xue2
Estimated H-index: 2
(Ocean University of China)
Background Pyropia haitanensis and P. yezoensis are two economically important marine crops that are also considered to be research models to study the physiological ecology of intertidal seaweed communities, evolutionary biology of plastids, and the origins of sexual reproduction. This plastid genome information will facilitate study of breeding, population genetics and phylogenetics.
45 Citations Source Cite
Cited By30
Published on May 12, 2017in eLife 7.62
Richard G. Dorrell10
Estimated H-index: 10
(École Normale Supérieure),
Gillian H. Gile15
Estimated H-index: 15
(Arizona State University)
+ 7 AuthorsChris Bowler70
Estimated H-index: 70
(École Normale Supérieure)
The cells of most plants and algae contain compartments called chloroplasts that enable them to capture energy from sunlight in a process known as photosynthesis. Chloroplasts are the remnants of photosynthetic bacteria that used to live freely in the environment until they were consumed by a larger cell. “Complex” chloroplasts can form if a cell that already has a chloroplast is swallowed by another cell. The most abundant algae in the oceans are known as diatoms. These algae belong to a group ...
21 Citations Source Cite
Published on Jul 1, 2017in Genome Biology and Evolution 3.94
Jong Im Kim10
Estimated H-index: 10
(Chungnam National University),
Christa E. Moore4
Estimated H-index: 4
(Dalhousie University)
+ 4 AuthorsWoongghi Shin14
Estimated H-index: 14
(Chungnam National University)
7 Citations Source Cite
Published on Jul 1, 2017in Current Biology 9.25
David Moreira52
Estimated H-index: 52
(Université Paris-Saclay),
Purificación López-García21
Estimated H-index: 21
(Université Paris-Saclay)
Summary Plastids, the photosynthetic organelles of eukaryotes, exhibit remarkably stable genome architecture. However, a recent study of microscopic red algae has found new record-sized plastid genomes with unusual architectures. These species form a new branch in the tree of red algae.
2 Citations Source Cite
Louise A. Lewis24
Estimated H-index: 24
(University of Connecticut)
The evolution of oxygenic photosynthesis by cyanobacteria was arguably one of the most significant biological events in Earth’s history, shaping the atmosphere and subsequently leading to diverse ecosystems (1). The permanent endosymbiotic merger between a cyanobacterium and a unicellular heterotrophic eukaryote in deep evolutionary time set the stage for the stunning diversity of photosynthetic eukaryotes and ecosystems seen today, giving rise to the supergroup Archaeplastida, the red, glaucoph...
3 Citations Source Cite
Published on Apr 1, 2018in Current Genetics 3.57
Lucia Hadariová2
Estimated H-index: 2
(Charles University in Prague),
Matej Vesteg8
Estimated H-index: 8
(Matej Bel University)
+ 1 AuthorsJuraj Krajčovič17
Estimated H-index: 17
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-photosynth...
4 Citations Source Cite
Published on Feb 1, 2018in Journal of Phycology 3.00
Monica O. Paiano2
Estimated H-index: 2
(Sao Paulo State University),
A. Del Cortona2
Estimated H-index: 2
(Ghent University)
+ 4 AuthorsOrlando Necchi18
Estimated H-index: 18
(Sao Paulo State University)
Little is known about genome organization in members of the order Batrachospermales, and the infra-ordinal relationship remains unresolved. Plastid (cp) genomes of seven members of the freshwater red algal order Batrachospermales were sequenced, with the following aims: 1) to describe the characteristics of cp genomes and compare these with other red algal groups; 2) to infer the phylogenetic relationships among these members to better understand the infra-ordinal classification. Cp genomes of B...
4 Citations Source Cite
Published on Dec 14, 2017in Frontiers in Plant Science 3.68
David Roy Smith26
Estimated H-index: 26
(University of Western Ontario)
There is a strong positive relationship between nuclear genome size and cell size across the eukaryotic domain, but the cause and effect of this relationship is unclear. A positive coupling of cell size and DNA content has also been recorded for various bacteria, suggesting that, with some exceptions, this association might be universal throughout the tree of life. However, the link between cell size and genome size has not yet been thoroughly explored with respect to chloroplasts, or organelles...
2 Citations Source Cite
Published on Dec 1, 2017in Current Biology 9.25
A. Del Cortona2
Estimated H-index: 2
,
Frederik Leliaert27
Estimated H-index: 27
(Ghent University)
+ 7 AuthorsOlivier De Clerck29
Estimated H-index: 29
(Ghent University)
Summary Virtually all plastid (chloroplast) genomes are circular double-stranded DNA molecules, typically between 100 and 200 kb in size and encoding circa 80–250 genes. Exceptions to this universal plastid genome architecture are very few and include the dinoflagellates, where genes are located on DNA minicircles. Here we report on the highly deviant chloroplast genome of Cladophorales green algae, which is entirely fragmented into hairpin chromosomes. Short- and long-read high-throughput seque...
14 Citations Source Cite
Published on Apr 1, 2018in Genome Biology and Evolution 3.94
Ma. Chiela M. Cremen4
Estimated H-index: 4
(University of Melbourne),
Frederik Leliaert27
Estimated H-index: 27
(Ghent University)
+ 1 AuthorsHeroen Verbruggen27
Estimated H-index: 27
(University of Melbourne)
4 Citations Source Cite
Published on Jul 1, 2018in New Phytologist 7.43
David Roy Smith26
Estimated H-index: 26
(University of Western Ontario)
3 Citations Source Cite