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BACKGROUND: The Cyanidiophyceae is an early-diverged red algal class that thrives in extreme conditions around acidic hot springs. Although this lineage has been highlighted as a model for understanding the biology of extremophilic eukaryotes, little is known about the molecular evolution of their mitochondrial genomes (mitogenomes). RESULTS: To fill this knowledge gap, we sequenced five mitogenomes from representative clades of Cyanidiophyceae and identified two major groups, here referred to as Galdieria-type (G-type) and Cyanidium-type (C-type). G-type mitogenomes exhibit the following three features: (i) reduction in genome size and gene inventory, (ii) evolution of unique protein properties including charge, hydropathy, stability, amino acid composition, and protein size, and (iii) distinctive GC-content and skewness of nucleotides. Based on GC-skew-associated characteristics, we postulate that unidirectional DNA replication may have resulted in the rapid evolution of G-type mitogenomes. CONCLUSIONS: The high divergence of G-type mitogenomes was likely driven by natural selection in the multiple extreme environments that Galdieria species inhabit combined with their highly flexible heterotrophic metabolism. We speculate that the interplay between mitogenome divergence and adaptation may help explain the dominance of Galdieria species in diverse extreme habitats.
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Evolução Molecular , Genoma Mitocondrial , Rodófitas , Ácidos , Composição de Bases , Extremófilos/genética , Fontes Termais , Filogenia , Rodófitas/genéticaRESUMO
We examined 12 strains representing eight species classified in the algal class Phaeothamniophyceae (Heterokontophyta). Based upon a five-gene molecular phylogeny (nuclear-encoded SSU rRNA and plastid-encoded psaA, psbA, psbC, and rbcL) and light microscopic observations, we describe five new species: Phaeoschizochlamys santosii sp. nov., Phaeoschizochlamys siveri sp. nov., Phaeothamnion wetherbeei sp. nov., Stichogloea dopii sp. nov. and Stichogloea fawleyi sp. nov. The Phaeothamniophyceae, as delimited here, form a natural group that is sister to the Aurearenophyceae. Molecular phylogenetic analyses proved more reliable than morphological characters for distinguishing species. Evolutionary trends with the SI clade of the heterokont algae are discussed.
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Plastídeos , Estramenópilas , Núcleo Celular , Filogenia , RNA Ribossômico , Análise de Sequência de DNA , Estramenópilas/genéticaRESUMO
Red algae (Rhodophyta) underwent two phases of large-scale genome reduction during their early evolution. The red seaweeds did not attain genome sizes or gene inventories typical of other multicellular eukaryotes. We generated a high-quality 92.1 Mb draft genome assembly from the red seaweed Gracilariopsis chorda, including methylation and small (s)RNA data. We analyzed these and other Archaeplastida genomes to address three questions: 1) What is the role of repeats and transposable elements (TEs) in explaining Rhodophyta genome size variation, 2) what is the history of genome duplication and gene family expansion/reduction in these taxa, and 3) is there evidence for TE suppression in red algae? We find that the number of predicted genes in red algae is relatively small (4,803-13,125 genes), particularly when compared with land plants, with no evidence of polyploidization. Genome size variation is primarily explained by TE expansion with the red seaweeds having the largest genomes. Long terminal repeat elements and DNA repeats are the major contributors to genome size growth. About 8.3% of the G. chorda genome undergoes cytosine methylation among gene bodies, promoters, and TEs, and 71.5% of TEs contain methylated-DNA with 57% of these regions associated with sRNAs. These latter results suggest a role for TE-associated sRNAs in RNA-dependent DNA methylation to facilitate silencing. We postulate that the evolution of genome size in red algae is the result of the combined action of TE spread and the concomitant emergence of its epigenetic suppression, together with other important factors such as changes in population size.
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Evolução Biológica , Elementos de DNA Transponíveis , Tamanho do Genoma , Rodófitas/genética , Metilação de DNA , Epigênese Genética , Duplicação Gênica , Regulação da Expressão GênicaRESUMO
Dictyochophyceae (silicoflagellates) are unicellular freshwater and marine algae (Heterokontophyta, stramenopiles). Despite their abundance in global oceans and potential ecological significance, discovered in recent years, neither nuclear nor organellar genomes of representatives of this group were sequenced until now. Here, we present the first complete plastid genome sequences of Dictyochophyceae, obtained from four species: Dictyocha speculum, Rhizochromulina marina, Florenciella parvula and Pseudopedinella elastica. Despite their comparable size and genetic content, these four plastid genomes exhibit variability in their organization: plastid genomes of F. parvula and P. elastica possess conventional quadripartite structure with a pair of inverted repeats, R. marina instead possesses two direct repeats with the same orientation and D. speculum possesses no repeats at all. We also observed a number of unusual traits in the plastid genome of D. speculum, including expansion of the intergenic regions, presence of an intron in the otherwise non-intron-bearing psaA gene, and an additional copy of the large subunit of RuBisCO gene (rbcL), the last of which has never been observed in any plastid genome. We conclude that despite noticeable gene content similarities between the plastid genomes of Dictyochophyceae and their relatives (pelagophytes, diatoms), the number of distinctive features observed in this lineage strongly suggests that additional taxa require further investigation.
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Genomas de Plastídeos , Estramenópilas , Evolução Molecular , Filogenia , Análise de Sequência de DNARESUMO
Brown algae are the only group of heterokont protists exhibiting complex multicellularity. Since their origin, brown algae have adapted to various marine habitats, evolving diverse thallus morphologies and gamete types. However, the evolutionary processes behind these transitions remain unclear due to a lack of a robust phylogenetic framework and problems with time estimation. To address these issues, we employed plastid genome data from 138 species, including heterokont algae, red algae, and other red-derived algae. Based on a robust phylogeny and new interpretations of algal fossils, we estimated the geological times for brown algal origin and diversification. The results reveal that brown algae first evolved true multicellularity, with plasmodesmata and reproductive cell differentiation, during the late Ordovician Period (ca. 450 Ma), coinciding with a major diversification of marine fauna (the Great Ordovician Biodiversification Event) and a proliferation of multicellular green algae. Despite its early Paleozoic origin, the diversification of major orders within this brown algal clade accelerated only during the Mesozoic Era, coincident with both Pangea rifting and the diversification of other heterokont algae (e.g., diatoms), coccolithophores, and dinoflagellates, with their red algal-derived plastids. The transition from ancestral isogamy to oogamy was followed by three simultaneous reappearances of isogamy during the Cretaceous Period. These are concordant with a positive character correlation between parthenogenesis and isogamy. Our new brown algal timeline, combined with a knowledge of past environmental conditions, shed new light on brown algal diversification and the intertwined evolution of multicellularity and sexual reproduction.
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Phaeophyceae , Rodófitas , Filogenia , Eucariotos/genética , Plantas , Rodófitas/genética , Plastídeos/genética , Phaeophyceae/genética , Evolução MolecularRESUMO
Human activity is an important driver of ecological and evolutionary change on our planet. In particular, domestication and biological introductions have important and long-lasting effects on species' genomic architecture and diversity. However, genome-wide analysis of independent domestication and introduction events within a single species has not previously been performed. The Pacific kelp Undaria pinnatifida provides such an opportunity because it has been cultivated in its native range in Northeast Asia but also introduced to four other continents in the past 50 years. Here we present the results of a genome-wide analysis of natural, cultivated and introduced populations of U. pinnatifida to elucidate human-driven evolutionary change. We demonstrate that these three categories of origin can be distinguished at the genome level, reflecting the combined influence of neutral (demography and migration) and non-neutral (selection) processes.
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Kelp , Alga Marinha , Undaria , Agricultura , Humanos , Kelp/genéticaRESUMO
Among the brown algal lineages, Ectocarpales species have isogamous fertilization in which male and female gametes are morphologically similar. In contrast, female gametes are much larger than male gametes in the oogamous species found in many other brown algal lineages. It has been reported that the plastids of isogamous species are biparentally inherited whereas the plastids of oogamous species are maternally inherited. In contrast, in both isogamous and oogamous species, the mitochondria are usually inherited maternally. To investigate whether there is any relationship between the modes of inheritance and organellar genome architecture, we sequenced six plastid genomes (ptDNA) and two mitochondrial genomes (mtDNA) of isogamous species from the Ectocarpales and compared them with previously sequenced organellar genomes. We found that the biparentally inherited ptDNAs of isogamous species presented distinctive structural rearrangements whereas maternally inherited ptDNAs of oogamous species showed no rearrangements. Our analysis permits the hypothesis that structural rearrangements in ptDNAs may be a consequence of the mode of inheritance.
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Genoma Mitocondrial , Genomas de Plastídeos , Padrões de Herança , Phaeophyceae/genética , DNA Mitocondrial/genética , Evolução Molecular , Rearranjo Gênico , Genômica , Plastídeos/genética , Análise de Sequência de DNARESUMO
The relationships among the Aurearenophyceae, Phaeothamniophyceae, Phaeophyceae and Xanthophyceae lineages of the Heterokontophyta SI clade are not well known. By adding previously unexamined taxa related to these classes in a five gene phylogeny (SSU rRNA, atpB, psaA, psaB, rbcL), we recovered an assemblage of taxa previously unrecognized. We propose the class Phaeosacciophyceae class. nov., that includes Phaeosaccion collinsii, Phaeosaccion multiseriatum sp. nov., Phaeosaccion okellyi sp. nov., Antarctosaccion applanatum, Tetrasporopsis fuscescens, Tetrasporopsis moei sp. nov., and Psammochrysis cassiotisii gen. & sp. nov. We re-examine the literature for Chrysomeris, Nematochrysis, Chrysowaernella and the invalid name "Giraudyopsis" and conclude some taxa in previous studies are misidentified or misnamed, i.e. Chrysomeris and Chrysowaernella, respectively. We also show that Nematochrysis sessilis var. vectensis and Nematochrysis hieroglyphica may belong in the recently described class Chrysoparadoxophyceae. The phylogenetic relationships of Phaeobotrys solitaria and Pleurochloridella botrydiopsis are not clearly resolved, but they branch near the Xanthophyceae. Here we describe a new class Phaeosacciophyceae, a new order Phaeosacciales, a new family Tetrasporopsidaceae, a new genus Psammochrysis and four new species.
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Filogenia , Estramenópilas/classificação , DNA de Protozoário/genética , DNA Ribossômico/genética , Especificidade da Espécie , Estramenópilas/genéticaRESUMO
Systematists increasingly use molecular markers to identify species; however, most microalgae were described before gene sequencing and type specimens were often ink drawings. Cryptic speciation and biogeographic isolation are other potential problems when anchoring an old species name with a modern gene sequence. Therefore when biological type material is absent, the best approach is to recollect the alga from the type locality and sequence genes. Sarcinochrysis marina, described in 1930 by Geitler from the Canary Islands, Spain, is the oldest Pelagophyceae genus. Geitler used two cultures in his study, but these cultures no longer exist. We re-isolated S. marina from the type locality near Las Palmas, Gran Canaria. Furthermore, we included additional Pelagophyceae strains that were isolated from natural habitats for this study or were obtained from culture collections. We produced 85 sequences, representing the nuclear-encoded SSU rRNA and the plastid-encoded rbcL, psaA, psaB, psbA, and psbC genes. The sequences were used to infer maximum likelihood phylogenetic trees. We anchored the name Sarcinochrysis marina using the Las Palmas isolate, and we described four new genera (Arachnochrysis, Pelagospilus, Sargassococcus, Sungminbooa) and nine new species in the Sarcinochrysidales. We also described a new family, Chrysocystaceae, based upon molecular phylogenetic analyses.
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Estramenópilas/classificação , Estramenópilas/genética , Núcleo Celular/genética , Filogenia , Plastídeos/genética , RNA Ribossômico 16S/genética , Espanha , Estramenópilas/isolamento & purificaçãoRESUMO
Coccophora langsdorfii (Turner) Greville (Fucales) is an intertidal brown alga that is endemic to Northeast Asia and increasingly endangered by habitat loss and climate change. We sequenced the complete circular plastid and mitochondrial genomes of C. langsdorfii. The circular plastid genome is 124,450 bp and contains 139 protein-coding, 28 tRNA and 6 rRNA genes. The circular mitochondrial genome is 35,660 bp and contains 38 protein-coding, 25 tRNA and 3 rRNA genes. The structure and gene content of the C. langsdorfii plastid genome is similar to those of other species in the Fucales. The plastid genomes of brown algae in other orders share similar gene content but exhibit large structural recombination. The large in-frame insert in the cox2 gene in the mitochondrial genome of C. langsdorfii is typical of other brown algae. We explored the effect of this insertion on the structure and function of the cox2 protein. We estimated the usefulness of 135 plastid genes and 35 mitochondrial genes for developing molecular markers. This study shows that 29 organellar genes will prove efficient for resolving brown algal phylogeny. In addition, we propose a new molecular marker suitable for the study of intraspecific genetic diversity that should be tested in a large survey of populations of C. langsdorfii.
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Marcadores Genéticos , Genoma Mitocondrial , Phaeophyceae/genética , Plastídeos/genética , Códon , Phaeophyceae/classificação , FilogeniaRESUMO
The brown algal species Sargassum thunbergii (Fucales, Phaeophyceae) is widely distributed in coastal area of East Asia. This alga is ecologically and economically important seaweeds; however, no genome data was reported thus far. To get a better understanding of organellar genome of S. thunbergii, we sequenced and annotated its complete plastid genome. The circular plastid genome is 124,592bp in size with 30.4% GC content, which is composed of a large single-copy (LSC) region of 73,668bp, a small single-copy (SSC) region of 40,032bp, and two inverted repeat (IR) of 5446bp each. The plastid genome of S. thunbergii includes 139 protein-coding genes, six ribosomal RNA (rRNA) operons, 28 transfer RNA (tRNA) sequences, and one intron (214bp) in tRNA-Leu (trnL) gene. Five overlapping genes were identified in the compact plastid genome. Base on the comparison with previously published five brown algae plastid genomes, we found that the gene content and gene order of S. thunbergii are identical to that of other Fucales species Fucus vesiculosus.
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Genomas de Plastídeos , Sargassum/genética , Análise de Sequência de RNARESUMO
The Florideophyceae is the most abundant and taxonomically diverse class of red algae (Rhodophyta). However, many aspects of the systematics and divergence times of the group remain unresolved. Using a seven-gene concatenated dataset (nuclear EF2, LSU and SSU rRNAs, mitochondrial cox1, and plastid rbcL, psaA and psbA genes), we generated a robust phylogeny of red algae to provide an evolutionary timeline for florideophyte diversification. Our relaxed molecular clock analysis suggests that the Florideophyceae diverged approximately 943 (817-1,049) million years ago (Ma). The major divergences in this class involved the emergence of Hildenbrandiophycidae [ca. 781 (681-879) Ma], Nemaliophycidae [ca. 661 (597-736) Ma], Corallinophycidae [ca. 579 (543-617) Ma], and the split of Ahnfeltiophycidae and Rhodymeniophycidae [ca. 508 (442-580) Ma]. Within these clades, extant diversity reflects largely Phanerozoic diversification. Divergences within Florideophyceae were accompanied by evolutionary changes in the carposporophyte stage, leading to a successful strategy for maximizing spore production from each fertilization event. Our research provides robust estimates for the divergence times of major lineages within the Florideophyceae. This timeline was used to interpret the emergence of key morphological innovations that characterize these multicellular red algae.