Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids

Abstract

BackgroundHeterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived plastids. The chromalveolate hypothesis proposes that the red-algal derived plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived plastid genomes.ResultsThe chloroplast genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus, have been fully sequenced. These species represent two distinct orders of the Phaeophyceae, which is a major group within the heterokont lineage. The sizes of the circular plastid genomes are 139,954 and 124,986 base pairs, respectively, the size difference being due principally to the presence of longer inverted repeat and intergenic regions in E. siliculosus. Gene contents of the two plastids are similar with 139-148 protein-coding genes, 28-31 tRNA genes, and 3 ribosomal RNA genes. The two genomes also exhibit very similar rearrangements compared to other sequenced plastid genomes. The tRNA-Leu gene of E. siliculosus lacks an intron, in contrast to the F. vesiculosus and other heterokont plastid homologues, suggesting its recent loss in the Ectocarpales. Most of the brown algal plastid genes are shared with other red-algal derived plastid genomes, but a few are absent from raphidophyte or diatom plastid genomes. One of these regions is most similar to an apicomplexan nuclear sequence. The phylogenetic relationship between heterokonts, cryptophytes and haptophytes (collectively referred to as chromists) plastids was investigated using several datasets of concatenated proteins from two cyanobacterial genomes and 18 plastid genomes, including most of the available red algal and chromist plastid genomes.ConclusionThe phylogenetic studies using concatenated plastid proteins still do not resolve the question of the monophyly of all chromist plastids. However, these results support both the monophyly of heterokont plastids and that of cryptophyte and haptophyte plastids, in agreement with nuclear phylogenies.

Do Red and Green Make Brown?: Perspectives on Plastid Acquisitions within Chromalveolates

“…Given the current taxonomic composition of the CCTH and SAR clades, it is difficult to determine whether an ancient endosymbiosis, followed by multiple independent loss events, is more parsimonious than a scenario where chloroplasts were acquired independently by different photosynthetic chromalveolates. Critically, in contrast to nuclear gene phylogenies, there is strong evidence for the monophyly of chromalveolate chloroplasts (7,52,60); hence, if chloroplasts were acquired independently by different chromalveolate lineages, they must have been transferred between different chromalveolate lineages by tertiary endosymbiosis rather than acquired via multiple independent secondary endosymbioses. Sanchez-Puerta and Delwiche (105) and Bodył et al (9) have proposed serial endosymbiotic models wherein secondary red algal chloroplasts were originally acquired by an ancestor of the CCTH clade and then transferred laterally by tertiary endosymbiosis into the SAR clade.…”

“…In addition, if phylogenies of chloroplast genes result in a topology different from that of nuclear genes, this would specifically point to tertiary, internal endosymbiotic events. While some chloroplast phylogenies neatly assign chromalveolates to the CCTH and SAR clades (52,60), others suggest alternative groupings, such as a close relationship between haptophyte and SAR clade plastids to the exclusion of cryptomonads (22,55,64,104,125), which could provide evidence for a tertiary endosymbiotic acquisition of a haptophyte ancestor by an early member of the SAR clade. Even if future nuclear and chloroplast gene phylogenies support the monophyly of the chromalveolates and the CCTH and SAR clades, an internal tertiary endosymbiosis could have occurred, for example, after the divergence of the CCTH and SAR clades but prior to the radiation of the constituent photosynthetic phyla.…”

Chloroplast genome of Sargassum horneri (Sargassaceae, Phaeophyceae): comparative chloroplast genomics of brown algae

“…The DNA sequence of the complete chloroplast genome of S. horneri was determined by comparison with published sequences for three brown algae (Le Corguillé et al 2009;Wang et al 2013). …”

“…To date, over 40 plastid genomes have been sequenced among stramenopiles. However, only three of them are from brown algae including Fucus vesiculosus (order Fucales), Saccharina japonica (order Laminariales), and Ectocarpus siliculosus (order Ectocarpales) (Le Corguillé et al 2009;Wang et al 2013). The brown algal plastid genomes are Electronic supplementary material The online version of this article (doi:10.1007/s10811-015-0609-2) contains supplementary material, which is available to authorized users.…”

Evolution of Bacterial-Like Phosphoprotein Phosphatases in Photosynthetic Eukaryotes Features Ancestral Mitochondrial or Archaeal Origin and Possible Lateral Gene Transfer

“…This can include the development of healthier, disease-or stress-resistant crops in addition to treatments for parasitic organisms such as Plasmodium spp. (malaria; Patzewitz et al, 2013) and other chromoalveolates (Kutuzov and Andreeva, 2008;Uhrig and Moorhead, 2011b) that are derived from photosynthetic eukaryotes and maintain a remnant chloroplast (apicoplast; Le Corguillé et al, 2009;Janouskovec et al, 2010;Kalanon and McFadden, 2010;Walker et al, 2011). The existence of proteins that are conserved across diverse eukaryotic phyla but absent in metazoa, such as the majority of bacterial-like PPP protein phosphatases described here, presents unique research opportunities.…”