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Open Access Research article

Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes

Shinichiro Maruyama1*, Kazuharu Misawa14, Mineo Iseki2, Masakatsu Watanabe3 and Hisayoshi Nozaki1

Author Affiliations

1 Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo 113-0033, Japan

2 Hayama Center for Advanced Studies, Graduate University for Advanced Studies (SOKENDAI), Hayama, Kanagawa 240-0193, Japan

3 School of Advanced Sciences, Graduate University for Advanced Studies (SOKENDAI), Hayama, Kanagawa 240-0193, Japan

4 Research Program for Computational Science, Riken, 4-6-1 Shirokane-dai, Minato-ku, Tokyo 108-8639, Japan

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BMC Evolutionary Biology 2008, 8:151  doi:10.1186/1471-2148-8-151

Published: 17 May 2008

Abstract

Background

Plastids have inherited their own genomes from a single cyanobacterial ancestor, but the majority of cyanobacterial genes, once retained in the ancestral plastid genome, have been lost or transferred into the eukaryotic host nuclear genome via endosymbiotic gene transfer. Although previous studies showed that cyanobacterial gnd genes, which encode 6-phosphogluconate dehydrogenase, are present in several plastid-lacking protists as well as primary and secondary plastid-containing phototrophic eukaryotes, the evolutionary paths of these genes remain elusive.

Results

Here we show an extended phylogenetic analysis including novel gnd gene sequences from Excavata and Glaucophyta. Our analysis demonstrated the patchy distribution of the excavate genes in the gnd gene phylogeny. The Diplonema gene was related to cytosol-type genes in red algae and Opisthokonta, while heterolobosean genes occupied basal phylogenetic positions with plastid-type red algal genes within the monophyletic eukaryotic group that is sister to cyanobacterial genes. Statistical tests based on exhaustive maximum likelihood analyses strongly rejected that heterolobosean gnd genes were derived from a secondary plastid of green lineage. In addition, the cyanobacterial gnd genes from phototrophic and phagotrophic species in Euglenida were robustly monophyletic with Stramenopiles, and this monophyletic clade was moderately separated from those of red algae. These data suggest that these secondary phototrophic groups might have acquired the cyanobacterial genes independently of secondary endosymbioses.

Conclusion

We propose an evolutionary scenario in which plastid-lacking Excavata acquired cyanobacterial gnd genes via eukaryote-to-eukaryote lateral gene transfer or primary endosymbiotic gene transfer early in eukaryotic evolution, and then lost either their pre-existing or cyanobacterial gene.