Abstract
The plastids of chlorarachniophytes were derived from an ancestral green alga via secondary endosymbiosis. Thus, genes from the “green” lineage via secondary endosymbiotic gene transfer (EGT) are expected in the nuclear genomes of the Chlorarachniophyta. However, several recent studies have revealed the presence of “red” genes in their nuclear genomes. To elucidate the origin of such “red” genes in chlorarachniophyte nuclear genomes, we carried out exhaustive single-gene phylogenetic analyses, including two operational taxonomic units (OTUs) that represent two divergent sister lineages of the Chlorarachniophyta, Amorphochlora amoeboformis ( = Lotharella amoeboformis; based on RNA sequences newly determined here) and Bigelowiella natans (based on the published genome sequence). We identified 10 genes of cyanobacterial origin, phylogenetic analysis of which showed the chlorarachniophytes to branch with the red lineage (red algae and/or red algal secondary or tertiary plastid-containing eukaryotes). Of the 10 genes, 7 demonstrated robust monophyly of the two chlorarachniophyte OTUs. Thus, the common ancestor of the extant chlorarachniophytes likely experienced multiple horizontal gene transfers from the red lineage. Because 4 of the 10 genes are obviously photosynthesis- and/or plastid-related, and almost all of the eukaryotic OTUs in the 10 trees possess plastids, such red genes most likely originated directly from photosynthetic eukaryotes. This situation could be explained by a possible cryptic endosymbiosis of a red algal plastid before the secondary endosymbiosis of the green algal plastid, or a long-term feeding on a single (or multiple closely related) red algal plastid-containing eukaryote(s) after the green secondary endosymbiosis.
Highlights
One billion years ago, an ancient cyanobacterium was engulfed by a heterotrophic eukaryote
Gene mining To elucidate the contribution of genes of the red lineage to genome mosaicism in Chlorarachniophyta, we searched the proteome of B. natans for proteins showing red algal affiliations
Out of the 21,708 queries, 3,436 proteins had more than 10 operational taxonomic units (OTUs) with which to construct phylogenetic trees, and their affinities were examined in an automated fashion using a ruby script
Summary
One billion years ago, an ancient cyanobacterium was engulfed by a heterotrophic eukaryote. A primary plastid is assumed to have evolved directly from the uptake of this cyanobacterium [1], [2], [3]. Recent studies suggest that primary endosymbiosis might have occurred in another lineage: the cercozoan amoeba Paulinella chromatophora [5]. The red and green algal ancestors were involved in secondary endosymbioses, becoming complex secondary plastids. All of the eukaryotes with red algal-derived secondary and tertiary plastids (hereafter, ‘‘CASH lineage’’ [6]; cryptophytes, alveolates, stramenopiles [Heterokontophyta], and haptophytes) were assigned to the supergroup Chromalveolata in 2005 [4]. Recent studies suggest that the green secondary plastids in these lineages may originate from two independent endosymbioses of green algae [10], [11]. Multigene phylogenetic analyses of various eukaryotic lineages has demonstrated that stramenopiles, alveolates, and Rhizaria form a monophyletic group [8], [9], [12], [13], [14] that was very recently reclassified as the supergroup ‘‘SAR’’ (Stramenopiles, Alveolates, and Rhizaria) [15]
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