Eukaryote-to-eukaryote gene transfer gives rise to genome mosaicism in euglenids

Abstract

Background: 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. 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.

Results: We 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.

Conclusions: Our 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.

Figure 1

Maximum likelihood (RAxML) tree of the 'red lineage' proteins found in euglenids. The results of bootstrap analyses using RAxML (upper) and the Bayesian inference posterior probability values using MrBayes (lower) are shown on each branch. A, the best tree of the homogentisate phytyltransferase (HPT) family proteins shows that the E. gracilis HPT is closely related to the Chromalveolata and red algal homologues. B, the 'red lineage' genes encoding prokaryote-type ADP/ATP transporter have been found in euglenids and Chromalveolata. Thick branches represent BI and ML values not lower than 100 and 95, respectively. Eu, euglenids; CR, Chromalveolata plus Rhizaria; Red, red algae; Cyano, cyanobacteria. See supplementary figures for full trees.

Figure 2

Hypothesized evolutionary history of the 'red lineage' genes in euglenids. In this model, the 'red lineage' genes have been acquired by the common ancestor of euglenophytes and eukaryovorous euglenids.