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Open Access Research article

An extended phylogenetic analysis reveals ancient origin of "non-green" phosphoribulokinase genes from two lineages of "green" secondary photosynthetic eukaryotes: Euglenophyta and Chlorarachniophyta

Yi Yang1, Shinichiro Maruyama12, Hiroyuki Sekimoto3, Hidetoshi Sakayama4 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 Department of Biochemistry and Molecular Biology, Dalhousie University, Sir Charles Tupper Medical Building, 5850 College Street, Halifax, Nova Scotia, B3H 4R2, Canada

3 Department of Chemical and Biological Sciences, Faculty of Science, Japan Women's University, 2-8-1 Mejirodai, Bunkyo-ku, Tokyo 112-8681, Japan

4 Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai-cho, Nada, Kobe-shi, Hyogo 657-8501, Japan

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BMC Research Notes 2011, 4:330  doi:10.1186/1756-0500-4-330

Published: 7 September 2011

Abstract

Background

Euglenophyta 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.

Results

Here, 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.

Conclusions

Our 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.