The appearance of photosynthetic eukaryotes (algae and plants) dramatically altered the Earth's ecosystem, making possible all vertebrate life on land, including humans. Dating algal origin is, however, frustrated by a meager fossil record. We generated a plastid multi-gene phylogeny with Bayesian inference and then used maximum likelihood molecular clock methods to estimate algal divergence times. The plastid tree was used as a surrogate for algal host evolution because of recent phylogenetic evidence supporting the vertical ancestry of the plastid in the red, green, and glaucophyte algae. Nodes in the plastid tree were constrained with six reliable fossil dates and a maximum age of 3,500 MYA based on the earliest known eubacterial fossil. Our analyses support an ancient (late Paleoproterozoic) origin of photosynthetic eukaryotes with the primary endosymbiosis that gave rise to the first alga having occurred after the split of the Plantae (i.e., red, green, and glaucophyte algae plus land plants) from the opisthokonts sometime before 1,558 MYA. The split of the red and green algae is calculated to have occurred about 1,500 MYA, and the putative single red algal secondary endosymbiosis that gave rise to the plastid in the cryptophyte, haptophyte, and stramenopile algae (chromists) occurred about 1,300 MYA. These dates, which are consistent with fossil evidence for putative marine algae (i.e., acritarchs) from the early Mesoproterozoic (1,500 MYA) and with a major eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic, provide a molecular timeline for understanding algal evolution.
The primary endosymbiotic origin of the plastid in eukaryotes more than 1 billion years ago led to the evolution of algae and plants. We analyzed draft genome and transcriptome data from the basally diverging alga Cyanophora paradoxa and provide evidence for a single origin of the primary plastid in the eukaryote supergroup Plantae. C. paradoxa retains ancestral features of starch biosynthesis, fermentation, and plastid protein translocation common to plants and algae but lacks typical eukaryotic light-harvesting complex proteins. Traces of an ancient link to parasites such as Chlamydiae were found in the genomes of C. paradoxa and other Plantae. Apparently, Chlamydia-like bacteria donated genes that allow export of photosynthate from the plastid and its polymerization into storage polysaccharide in the cytosol.
Whole-genome shotgun sequence data from three individual cells isolated from seawater, followed by analysis of ribosomal DNA, indicated that the cells represented three divergent clades of picobiliphytes. In contrast with the recent description of this phylum, we found no evidence of plastid DNA nor of nuclear-encoded plastid-targeted proteins, which suggests that these picobiliphytes are heterotrophs. Genome data from one cell were dominated by sequences from a widespread single-stranded DNA virus. This virus was absent from the other two cells, both of which contained non-eukaryote DNA derived from marine Bacteroidetes and large DNA viruses. By using shotgun sequencing of uncultured marine picobiliphytes, we revealed the distinct interactions of individual cells.
The most widely distributed dinoflagellate plastid contains chlorophyll c 2 and peridinin as the major carotenoid. A second plastid type, found in taxa such as Karlodinium micrum and Karenia spp., contains chlorophylls c 1 ؉ c2 and 19 -hexanoyloxy-fucoxanthin and͞or 19 -butanoyloxy-fucoxanthin but lacks peridinin. Because the presence of chlorophylls c 1 ؉ c2 and fucoxanthin is typical of haptophyte algae, the second plastid type is believed to have originated from a haptophyte tertiary endosymbiosis in an ancestral peridinin-containing dinoflagellate. This hypothesis has, however, never been thoroughly tested in plastid trees that contain genes from both peridinin-and fucoxanthin-containing dinoflagellates. To address this issue, we sequenced the plastid-encoded psaA (photosystem I P700 chlorophyll a apoprotein A1), psbA (photosystem II reaction center protein D1), and ''Form I'' rbcL (ribulose-1,5-bisphosphate carboxylase͞oxygenase) genes from various red and dinoflagellate algae. The combined psaA ؉ psbA tree shows significant support for the monophyly of peridinin-and fucoxanthin-containing dinoflagellates as sister to the haptophytes. The monophyly with haptophytes is robustly recovered in the psbA phylogeny in which we increased the sampling of dinoflagellates to 14 species. As expected from previous analyses, the fucoxanthin-containing dinoflagellates formed a wellsupported sister group with haptophytes in the rbcL tree. Based on these analyses, we postulate that the plastid of peridinin-and fucoxanthin-containing dinoflagellates originated from a haptophyte tertiary endosymbiosis that occurred before the split of these lineages. Our findings imply that the presence of chlorophylls c 1 ؉ c2 and fucoxanthin, and the Form I rbcL gene are in fact the primitive (not derived, as widely believed) condition in dinoflagellates.
Previous phylogenetic studies of the Rhodophyta have provided a framework for understanding red algal phylogeny, but there still exists the need for a comprehensive analysis using a broad sampling of taxa and sufficient phylogenetic information to clearly define the major lineages. In this study, we determined 48 sequences of the PSI P700 chl a apoprotein A1 (psaA) and rbcL coding regions and established a robust red algal phylogeny to identify the major clades. The tree included most of the lineages of the Bangiophyceae (25 genera, 48 taxa). Seven well-supported lineages were identified with this analysis with the Cyanidiales having the earliest divergence and being distinct from the remaining taxa; i.e. the Porphyridiales 1-3, Bangiales, Florideophyceae, and Compsopogonales. We also analyzed data sets with fewer taxa but using seven proteins or the DNA sequence from nine genes to resolve inter-clade relationships. Based on all of these analyses, we propose that the Rhodophyta contains two new subphyla, the Cyanidiophytina with a single class, the Cyanidiophyceae, and the Rhodophytina with six classes, the Bangiophyceae, Compsopogonophyceae, Florideophyceae, Porphyridiophyceae classis nov. (which contains Porphyridium, Flintiella, and Erythrolobus), Rhodellophyceae, and Stylonematophyceae classis nov. (which contains Stylonema, Bangiopsis, Chroodactylon, Chroothece, Purpureofilum, Rhodosorus, Rhodospora, and Rufusia). We also describe a new order, Rhodellales, and a new family, Rhodellaceae (with Rhodella, Dixoniella, and Glaucosphaera).
The Cyanidiales is a group of asexual, unicellular red algae, which thrive in acidic and high temperature conditions around hot springs. These unicellular taxa have a relatively simple morphology and are currently classified into three genera, Cyanidium, Cyanidioschyzon and Galdieria. Little is known, however, about the biodiversity of Cyanidiales, their population structure and their phylogenetic relationships. Here we used a taxonomically broadly sampled three-gene data set of plastid sequences to infer a robust phylogenetic framework for the Cyanidiales. The phylogenetic analyses support the existence of at least four distinct Cyanidiales lineages: the Galdieria spp. lineage (excluding Galdieria maxima), the Cyanidium caldarium lineage, a novel monophyletic lineage of mesophilic Cyanidium spp. and the Cyanidioschyzon merolae plus Galdieria maxima lineage. Our analyses do not support the notion of a mesophilic ancestry of the Cyanidiales and suggest that these algae were ancestrally thermo-acidotolerant. We also used environmental polymerase chain reaction (PCR) for the rbcL gene to sample Cyanidiales biodiversity at five ecologically distinct sites at Pisciarelli in the Phlegrean Fields in Italy. This analysis showed a high level of sequence divergence among Cyanidiales species and the partitioning of taxa based on environmental conditions. Our research revealed an unexpected level of genetic diversity among Cyanidiales that revises current thinking about the phylogeny and biodiversity of this group. We predict that future environmental PCR studies will significantly augment known biodiversity that we have discovered and demonstrate the Cyanidiales to be a species-rich branch of red algal evolution.
Here we use phylogenomics with expressed sequence tag (EST) data from the ecologically important coccolithophore-forming alga Emiliania huxleyi and the plastid-lacking cryptophyte Goniomonas cf. pacifica to establish their phylogenetic positions in the eukaryotic tree. Haptophytes and cryptophytes are members of the putative eukaryotic supergroup Chromalveolata (chromists [cryptophytes, haptophytes, stramenopiles] and alveolates [apicomplexans, ciliates, and dinoflagellates]). The chromalveolates are postulated to be monophyletic on the basis of plastid pigmentation in photosynthetic members, plastid gene and genome relationships, nuclear "host" phylogenies of some chromalveolate lineages, unique gene duplication and replacements shared by these taxa, and the evolutionary history of components of the plastid import and translocation systems. However the phylogenetic position of cryptophytes and haptophytes and the monophyly of chromalveolates as a whole remain to be substantiated. Here we assess chromalveolate monophyly using a multigene dataset of nuclear genes that includes members of all 6 eukaryotic supergroups. An automated phylogenomics pipeline followed by targeted database searches was used to assemble a 16-protein dataset (6,735 aa) from 46 taxa for tree inference. Maximum likelihood and Bayesian analyses of these data support the monophyly of haptophytes and cryptophytes. This relationship is consistent with a gene replacement via horizontal gene transfer of plastid-encoded rpl36 that is uniquely shared by these taxa. The haptophytes + cryptophytes are sister to a clade that includes all other chromalveolates and, surprisingly, two members of the Rhizaria, Reticulomyxa filosa and Bigelowiella natans. The association of the two Rhizaria with chromalveolates is supported by the approximately unbiased (AU)-test and when the fastest evolving amino acid sites are removed from the 16-protein alignment.
The photosynthetic organelle of algae and plants (the plastid) traces its origin to a primary endosymbiotic event in which a previously non-photosynthetic protist engulfed and enslaved a cyanobacterium. This eukaryote then gave rise to the red, green and glaucophyte algae. However, many algal lineages, such as the chlorophyll c-containing chromists, have a more complicated evolutionary history involving a secondary endosymbiotic event, in which a protist engulfed an existing eukaryotic alga (in this case, a red alga). Chromists such as diatoms and kelps then rose to great importance in aquatic habitats. Another algal group, the dinoflagellates, has undergone tertiary (engulfment of a secondary plastid) and even quaternary endosymbioses. In this review, we examine algal diversity and show endosymbiosis to be a major force in algal evolution. This area of research has advanced rapidly and long-standing issues such as the chromalveolate hypothesis and the extent of endosymbiotic gene transfer have recently been clarified.
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