Abstract
BackgroundEuglenophyta and Chlorarachniophyta are groups of photosynthetic eukaryotes harboring secondary plastids of distinct green algal origins. Although previous phylogenetic analyses of genes encoding Calvin cycle enzymes demonstrated the presence of genes apparently not derived from green algal endosymbionts in the nuclear genomes of Euglena gracilis (Euglenophyta) and Bigelowiella natans (Chlorarachniophyta), the origins of these "non-green" genes in "green" secondary phototrophs were unclear due to the limited taxon sampling.ResultsHere, we sequenced five new phosphoribulokinase (PRK) genes (from one euglenophyte, two chlorarachniophytes, and two glaucophytes) and performed an extended phylogenetic analysis of the genes based on a phylum-wide taxon sampling from various photosynthetic eukaryotes. Our phylogenetic analyses demonstrated that the PRK sequences form two genera of Euglenophyta formed a robust monophyletic group within a large clade including stramenopiles, haptophytes and a cryptophyte, and three genera of Chlorarachniophyta were placed within the red algal clade. These "non-green" affiliations were supported by the taxon-specific insertion/deletion sequences in the PRK alignment, especially between euglenophytes and stramenopiles. In addition, phylogenetic analysis of another Calvin cycle enzyme, plastid-targeted sedoheptulose-bisphosphatase (SBP), showed that the SBP sequences from two genera of Chlorarachniophyta were positioned within a red algal clade.ConclusionsOur results suggest that PRK genes may have been transferred from a "stramenopile" ancestor to Euglenophyta and from a "red algal" ancestor to Chlorarachniophyta before radiation of extant taxa of these two "green" secondary phototrophs. The presence of two of key Calvin cycle enzymes, PRK and SBP, of red algal origins in Chlorarachniophyta indicate that the contribution of "non-green" algae to the plastid proteome in the "green" secondary phototrophs is more significant than ever thought. These "non-green" putative plastid-targeted enzymes from Chlorarachniophyta are likely to have originated from an ancestral red alga via horizontal gene transfer, or from a cryptic red algal endosymbiosis in the common ancestor of the extant chlorarachniophytes.
Highlights
Euglenophyta and Chlorarachniophyta are groups of photosynthetic eukaryotes harboring secondary plastids of distinct green algal origins
In the process of primary and secondary endosymbioses, the genomic contents of the endosymbionts are reduced when compared to their presumed ancestors [2,6] via gene loss and a process known as endosymbiotic gene transfer (EGT), in which a set of genes mostly assigned to the endosymbiont’s functions is moved to the nucleus of the host and merged into the chromosome [7,8,9,10,11,12,13]
EGT can be regarded as a special case of horizontal gene transfer (HGT), which is applicable to broader biological contexts such as a predacious or parasitic process [10,14,15]
Summary
Euglenophyta and Chlorarachniophyta are groups of photosynthetic eukaryotes harboring secondary plastids of distinct green algal origins. Previous phylogenetic analyses of genes encoding Calvin cycle enzymes demonstrated the presence of genes apparently not derived from green algal endosymbionts in the nuclear genomes of Euglena gracilis (Euglenophyta) and Bigelowiella natans (Chlorarachniophyta), the origins of these “non-green” genes in “green” secondary phototrophs were unclear due to the limited taxon sampling. Extensive molecular phylogenetic analysis and careful examination of multiple possible HGT-derived genes are keys to give insights into historical events of endosymbioses (even including a cryptic endosymbiosis) in a eukaryotic cell [16]. Some CC genes are affiliated with non-cyanobacterial prokaryotic homologs [12,13], the Class II PRK genes of the photosynthetic eukaryotes form a robust monophyletic group with cyanobacterial homologs, suggesting no gene replacement after the primary endosymbiosis (Additional file 1). PRK may be an ideal gene to trace the historical events of endosymbioses of the plastids
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