Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants (original) (raw)
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Ancient Recruitment by Chromists of Green Algal Genes Encoding Enzymes for Carotenoid Biosynthesis
Molecular Biology and Evolution, 2008
Chromist algae (stramenopiles, cryptophytes, and haptophytes) are major contributors to marine primary productivity. These eukaryotes acquired their plastid via secondary endosymbiosis, whereby an early-diverging red alga was engulfed by a protist and the plastid was retained and its associated nuclear-encoded genes were transferred to the host genome. Current data suggest, however, that chromists are paraphyletic; therefore, it remains unclear whether their plastids trace back to a single secondary endosymbiosis or, alternatively, this organelle has resulted from multiple independent events in the different chromist lineages. Both scenarios, however, predict that plastid-targeted, nucleus-encoded chromist proteins should be most closely related to their red algal homologs. Here we analyzed the biosynthetic pathway of carotenoids that are essential components of all photosynthetic eukaryotes and find a mosaic evolutionary origin of these enzymes in chromists. Surprisingly, about one-third (5/16) of the proteins are most closely related to green algal homologs with three branching within or sister to the early-diverging Prasinophyceae. This phylogenetic association is corroborated by shared diagnostic indels and the syntenic arrangement of a specific gene pair involved in the photoprotective xanthophyll cycle. The combined data suggest that the prasinophyte genes may have been acquired before the ancient split of stramenopiles, haptophytes, cryptophytes, and putatively also dinoflagellates. The latter point is supported by the observed monophyly of alveolates and stramenopiles in most molecular trees. One possible explanation for our results is that the green genes are remnants of a cryptic endosymbiosis that occurred early in chromalveolate evolution; that is, prior to the postulated split of stramenopiles, alveolates, haptophytes, and cryptophytes. The subsequent red algal capture would have led to the loss or replacement of most green genes via intracellular gene transfer from the new endosymbiont. We argue that the prasinophyte genes were retained because they enhance photosynthetic performance in chromalveolates, thus extending the niches available to these organisms. The alternate explanation of green gene origin via serial endosymbiotic or horizontal gene transfers is also plausible, but the latter would require the independent origins of the same five genes in some or all the different chromalveolate lineages.
Origin and Evolution of Photosynthesis: Clues from Genome Comparison
Photosynthesis. Energy from the Sun, 2008
Fifteen complete cyanobacterial genome sequences were characterized revealing 1054 protein families (Cyanobacterial clusters of Orthologous Groups of proteins, or CyOGs), encoded in at least 14 of them. While the majority of the core CyOGs were shared with other bacteria, 84 were exclusively shared by cyanobacteria and plants and/or other plastid-carrying eukaryotes that indicate their relation to the photosynthetic machinery (hereafter denoted as photosynthetic CyOGs). Only a few photosynthetic CyOGs find counterparts in the genomes of anoxygenic phototrophic bacteria Chlorobium tepidum, Rhodopseudomonas palustris, Chloroflexus aurantiacus or Heliobacillus mobilis. These observations, coupled with the recent geological data on the properties of the ancient phototrophs, suggest that photosynthesis has originated in the cyanobacterial lineage and spread to other phyla via horizontal gene transfer under the selective pressure of the UV light, availability of electron donors and, eventually, oxygen.
Endosymbiosis, 2013
Algae and plants rely on the plastid (e.g., chloroplast) to carry out photosynthesis. This organelle traces its origin to a cyanobacterium that was captured over a billion years ago by a single-celled protist. Three major photosynthetic lineages (the green algae and plants [Viridiplantae], red algae [Rhodophyta], and Glaucophyta) arose from this primary endosymbiotic event and are putatively united as the Plantae (also known as Archaeplastida). Glaucophytes comprise a handful of poorly studied species that retain ancestral features of the cyanobacterial endosymbiont such as a peptidoglycan cell wall. Testing the Plantae hypothesis and elucidating glaucophyte evolution has in the past been thwarted by the absence of complete genome data from these taxa. Furthermore, multigene phylogenetics has fueled controversy about the frequency of primary plastid acquisitions during
The cyanobacterial genome core and the origin of photosynthesis
Proceedings of The National Academy of Sciences, 2006
Comparative analysis of 15 complete cyanobacterial genome sequences, including ''near minimal'' genomes of five strains of Prochlorococcus spp., revealed 1,054 protein families [core cyanobacterial clusters of orthologous groups of proteins (core Cy-OGs)] encoded in at least 14 of them. The majority of the core CyOGs are involved in central cellular functions that are shared with other bacteria; 50 core CyOGs are specific for cyanobacteria, whereas 84 are exclusively shared by cyanobacteria and plants andÍžor other plastid-carrying eukaryotes, such as diatoms or apicomplexans. The latter group includes 35 families of uncharacterized proteins, which could also be involved in photosynthesis. Only a few components of cyanobacterial photosynthetic machinery are represented in the genomes of the anoxygenic phototrophic bacteria Chlorobium tepidum, Rhodopseudomonas palustris, Chloroflexus aurantiacus, or Heliobacillus mobilis. These observations, coupled with recent geological data on the properties of the ancient phototrophs, suggest that photosynthesis originated in the cyanobacterial lineage under the selective pressures of UV light and depletion of electron donors. We propose that the first phototrophs were anaerobic ancestors of cyanobacteria (''procyanobacteria'') that conducted anoxygenic photosynthesis using a photosystem I-like reaction center, somewhat similar to the heterocysts of modern filamentous cyanobacteria. From procyanobacteria, photosynthesis spread to other phyla by way of lateral gene transfer.
Genome Biology and Evolution, 2013
Cyanobacteria forged two major evolutionary transitions with the invention of oxygenic photosynthesis and the bestowal of photosynthetic lifestyle upon eukaryotes through endosymbiosis. Information germane to understanding those transitions is imprinted in cyanobacterial genomes, but deciphering it is complicated by lateral gene transfer (LGT). Here, we report genome sequences for the morphologically most complex true-branching cyanobacteria, and for Scytonema hofmanni PCC 7110, which with 12,356 proteins is the most gene-rich prokaryote currently known. We investigated components of cyanobacterial evolution that have been vertically inherited, horizontally transferred, and donated to eukaryotes at plastid origin. The vertical component indicates a freshwater origin for water-splitting photosynthesis. Networks of the horizontal component reveal that 60% of cyanobacterial gene families have been affected by LGT. Plant nuclear genes acquired from cyanobacteria define a lower bound frequency of 611 multigene families that, in turn, specify diazotrophic cyanobacterial lineages as having a gene collection most similar to that possessed by the plastid ancestor.
Evolution: red algal genome affirms a common origin of all plastids
Current biology : CB, 2004
Photosynthetic organelles (plastids) come in many forms and were originally thought to have multiple origins. The complete genome of the thermophilic red alga Cyanidioschizon merolae provides further evidence that all plastids derive from a single endosymbiotic event more than 600 million years ago.