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The New Red Algal Subphylum Proteorhodophytina Comprises the Largest and Most Divergent Plastid Genomes Known
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.
  • References (70)
  • Cited By (23)
Hwan Su Yoon8
Estimated H-index: 8
(Bigelow Laboratory For Ocean Sciences),
Giuseppe C. Zuccarello8
Estimated H-index: 8
(Victoria University of Wellington),
Debashish Bhattacharya9
Estimated H-index: 9
(Rutgers University)
The red algae (Rhodophyta) form a distinct photosynthetic eukaryotic lineage that consists of around 6,000 species including unicellular to large multicellular taxa (http://www.algaebase.org/). The red algae are unique among eukaryotes in lacking both flagella and centrioles during their entire life cycle (Gabrielson et al., 1990; Graham and Wilcox, 2000). Pit connections, pit plugs, and a triphasic life cycle that are mostly found in the Florideophyceae are also distinguishing characters of the...
Ref 77Cited 18 Download Pdf Cite this paper
2015 in peerj
Marie-Mathilde Perrineau4
Estimated H-index: 4
(Rutgers University),
Dana C. Price7
Estimated H-index: 7
(Rutgers University),
Georg Mohr10
Estimated H-index: 10
(University of Texas at Austin)
... more
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...
Ref 42Cited 8 Download Pdf Cite this paper
Asuka Kushibiki1
Estimated H-index: 1
(Yamagata University),
Akiko Yokoyama5
Estimated H-index: 5
(University of Tsukuba),
Mitsunori Iwataki9
Estimated H-index: 9
(Yamagata University)
... more
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...
Ref 28Cited 6 Source Cite this paper
Hwan Su Yoon8
Estimated H-index: 8
(University of Iowa),
Jeremiah D. Hackett10
Estimated H-index: 10
(University of Iowa),
Gabriele Pinto8
Estimated H-index: 8
(University of Naples Federico II)
... more
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...
Ref 2Cited 281 Download Pdf Cite this paper
Susan E. Douglas10
Estimated H-index: 10
(National Research Council)
Plastids from extant plants exhibit considerable diversity in morphological and biochemical characters. Although most authors have agreed on xenogenous (endosymbiotic) rather than autogenous origins of plastids (discussed by Doolittle (1982) in ‘The Biology of Cyanobacteria’), details concerning the endosymbiotic events remain unresolved.
Ref 188Cited 71 Download Pdf Cite this paper
Natalia Volfovsky8
Estimated H-index: 8
,
Brian J. Haas10
Estimated H-index: 10
,
Steven L. Salzberg9
Estimated H-index: 9
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.
Ref 23Cited 118 Download Pdf Cite this paper
E. Kim1
Estimated H-index: 1
(Dalhousie University),
John M. Archibald10
Estimated H-index: 10
(Canadian Institute for Advanced Research)
Plastids, the light-harvesting organelles of plants and algae, are the descendants of cyanobacterial endosymbionts that became permanent fixtures inside nonphotosynthetic eukaryotic host cells. This chapter provides an overview of the structural, functional and molecular diversity of plastids in the context of current views on the evolutionary relationships among the eukaryotic hosts in which they reside. Green algae, land plants, red algae and glaucophyte algae harbor double-membrane-bound plas...
Ref 218Cited 34 Download Pdf Cite this paper
B. Franz Lang1
Estimated H-index: 1
(Université de Montréal),
Aurora M. Nedelcu8
Estimated H-index: 8
(University of New Brunswick)
Algae are characterized by the presence of plastids (chloroplasts), which are organelles of cyanobacterial origin. Plastids have their own genome, machineries for replication, transcription and translation, and are the site of photosynthesis (except in secondarily non-photosynthetic species) and a variety of other biological functions. Algae are subdivided into those whose plastids can be traced back to a common cyanobacterial endosymbiont (algae with primary plastids), and others in which plast...
Ref 156Cited 19 Download Pdf Cite this paper
Matthew S. Bennett8
Estimated H-index: 8
(Michigan State University),
Richard E. Triemer8
Estimated H-index: 8
(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...
Ref 28Cited 22 Source Cite this paper
C Bernard1
Estimated H-index: 1
(Centre national de la recherche scientifique),
J C Thomas1
Estimated H-index: 1
(Centre national de la recherche scientifique),
Didier Mazel10
Estimated H-index: 10
(Centre national de la recherche scientifique)
... more
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 ...
Cited 25 Download Pdf Cite this paper
  • References (70)
  • Cited By (23)
2017 in elife
Richard G. Dorrell8
Estimated H-index: 8
(École Normale Supérieure),
Gillian Gile2
Estimated H-index: 2
(Arizona State University),
Giselle McCallum1
Estimated H-index: 1
(École Normale Supérieure)
... more
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 ...
Ref 148Cited 12 Source Cite this paper
Jong Im Kim6
Estimated H-index: 6
(Chungnam National University),
Christa E. Moore4
Estimated H-index: 4
(Dalhousie University),
John M. Archibald10
Estimated H-index: 10
(Dalhousie University)
... more
Ref 81Cited 5 Source Cite this paper
2017 in current biology [IF: 8.85]
David Moreira5
Estimated H-index: 5
(Université Paris-Saclay),
Purificación López-García10
Estimated H-index: 10
(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.
Ref 16Cited 1 Source Cite this paper
Richard G. Dorrell8
Estimated H-index: 8
(École Normale Supérieure),
Chris Bowler9
Estimated H-index: 9
(École Normale Supérieure)
Abstract The stramenopiles encompass an incredible diversity of organisms, including ecologically fundamental single-celled algae such as diatoms, giant macroalgae such as kelps, as well as photo-mixotrophic and heterotrophic species. The photosynthetic species possess plastids of secondary or higher red algal origin. The diversity of stramenopile species provides an ideal system for exploring the fundamental features underpinning plastid establishment in eukaryotes, and also how plastid metabol...
Ref 187 Source Cite this paper
Louise A. Lewis7
Estimated H-index: 7
(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...
Ref 19Cited 3 Source Cite this paper
Lucia Hadariová1
Estimated H-index: 1
(Charles University in Prague),
Matej Vesteg1
Estimated H-index: 1
(Matej Bel University),
Vladimír Hampl9
Estimated H-index: 9
(Charles University in Prague)
... more
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...
Ref 226Cited 1 Download Pdf Cite this paper
2018 in journal of phycology [IF: 2.61]
Monica O. Paiano2
Estimated H-index: 2
(Sao Paulo State University),
Andrea Del Cortona2
Estimated H-index: 2
(Ghent University),
Joana F. Costa6
Estimated H-index: 6
(University of Melbourne)
... more
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...
Ref 41Cited 3 Download Pdf Cite this paper
David Roy Smith8
Estimated H-index: 8
(University of Western Ontario)
Abstract Photosynthesis is an awe-inspiring process. It has shaped, coloured, and diversified the biological world in innumerable ways and supplies us with the air we breathe. Photosynthetic organisms are literally our lifelines on Earth. Without them we perish. Perhaps this is why many of us are uncomfortable with and confused by the concept of a photosynthetic organism forfeiting its ability to convert sunlight into chemical energy, giving up its life-sustaining powers. Indeed, the evolutionar...
Ref 87 Source Cite this paper
Sergio A. Muñoz-Gómez7
Estimated H-index: 7
(Dalhousie University),
Claudio H. Slamovits9
Estimated H-index: 9
(Dalhousie University)
Abstract The myzozoa encompasses quite disparate protists, like the infamous apicomplexan parasites, or the famous dinoflagellate phytoplankton. Collectively, myzozoans display a wide diversity of plastids; they all most likely descended from a common myzozoan plastid ancestor. Some myzozoan plastids are photosynthetic whereas others are not; some have plastid genomes (plastomes) but others have lost them. The only two eukaryotes known to have lost plastids altogether are myzozoans. In this chap...
Ref 135 Source Cite this paper
David Roy Smith8
Estimated H-index: 8
(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...
Ref 56Cited 1 Source Cite this paper