Abstract

BackgroundEuglenophytes are a group of photosynthetic flagellates possessing a plastid derived from a green algal endosymbiont, which was incorporated into an ancestral host cell via secondary endosymbiosis. However, the impact of endosymbiosis on the euglenophyte nuclear genome is not fully understood due to its complex nature as a 'hybrid' of a non-photosynthetic host cell and a secondary endosymbiont.ResultsWe analyzed an EST dataset of the model euglenophyte Euglena gracilis using a gene mining program designed to detect laterally transferred genes. We found E. gracilis genes showing affinity not only with green algae, from which the secondary plastid in euglenophytes evolved, but also red algae and/or secondary algae containing red algal-derived plastids. Phylogenetic analyses of these 'red lineage' genes suggest that E. gracilis acquired at least 14 genes via eukaryote-to-eukaryote lateral gene transfer from algal sources other than the green algal endosymbiont that gave rise to its current plastid. We constructed an EST library of the aplastidic euglenid Peranema trichophorum, which is a eukaryovorous relative of euglenophytes, and also identified 'red lineage' genes in its genome.ConclusionsOur data show genome mosaicism in E. gracilis and P. trichophorum. One possible explanation for the presence of these genes in these organisms is that some or all of them were independently acquired by lateral gene transfer and contributed to the successful integration and functioning of the green algal endosymbiont as a secondary plastid. Alternative hypotheses include the presence of a phagocytosed alga as the single source of those genes, or a cryptic tertiary endosymbiont harboring secondary plastid of red algal origin, which the eukaryovorous ancestor of euglenophytes had acquired prior to the secondary endosymbiosis of a green alga.

Highlights

  • Euglenophytes are a group of photosynthetic flagellates possessing a plastid derived from a green algal endosymbiont, which was incorporated into an ancestral host cell via secondary endosymbiosis

  • To understand the nature and extent of genome mosaicism in E. gracilis, we searched for E. gracilis genes showing specific affinity to homologues of photosynthetic eukaryotes other than green algae, the latter being the unambiguous source of the endosymbiont that gave rise to the secondary plastid in euglenophytes

  • Using the E. gracilis protein sequences generated from the expressed sequence tag (EST) database as queries, we assembled a set of sequences showing strong similarity to green algal/plant proteins in preliminary phylogenetic trees

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Summary

Introduction

Euglenophytes are a group of photosynthetic flagellates possessing a plastid derived from a green algal endosymbiont, which was incorporated into an ancestral host cell via secondary endosymbiosis. The impact of endosymbiosis on the euglenophyte nuclear genome is not fully understood due to its complex nature as a ‘hybrid’ of a non-photosynthetic host cell and a secondary endosymbiont. Subsequent to the evolution of primary plastids, two independent lineages of green algae were captured by two distinct lineages of phagotrophic (Excavata) and chlorarachniophytes (Rhizaria). Chloroplast genome analyses suggest that the chlorarachniophyte plastid is derived from a green alga belonging to the ulvophytetrebouxiophyte-chlorophyte group, while the ancestor of the euglenophyte plastid is related to prasinophyte green algae [8,9]

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