Elsevier

Gene

Volume 402, Issues 1–2, 1 November 2007, Pages 35-39
Gene

Genome history in the symbiotic hybrid Euglena gracilis

https://doi.org/10.1016/j.gene.2007.07.023Get rights and content

Abstract

Euglena gracilis has a chimeric gene collection in which some genes were inherited from its heterotrophic host and others were acquired from a photoautotrophic endosymbiont during secondary endosymbiosis. The evolutionary reconstruction of such a hybrid genome poses a challenge for standard phylogenetic tools that produce bifurcating trees because genome evolution by endosymbiotic gene transfer is a non tree-like process. We sequenced 2770 ESTs from E. gracilis, of which 841 have homologues in a sample of other eukaryotes. Most of these homologues are found in all of the eukaryotes in our sample, but 117 of them are specific to photoautotrophic eukaryotes. A phylogenetic tree fails to account for this observation but the distribution of homologues and a phylogenetic network clearly show the common origin of E. gracilis from both kinetoplastid and photoautotrophic ancestors.

Introduction

Most photoautotrophic eukaryotes acquired their photosynthetic lifestyle from a cyanobacterial endosymbiont (McFadden, 2001). The genome of the endosymbiont itself has since then been reduced and the endosymbiont evolved into a DNA possessing organelle – a primary plastid – as found in green and red algae, land plants and glaucocystophytes (Adl et al., 2005). Several independent eukaryotic lineages have acquired their photosynthetic lifestyle from a secondary endosymbiont — a eukaryotic alga that became engulfed by another eukaryote (Gibbs, 1978, Stoebe and Maier, 2002). Both primary and secondary endosymbiosis were accompanied by endosymbiotic gene transfer (EGT) — the relocation of genes from the organelle to the chromosomes of the host (Martin et al., 1993, Archibald et al., 2003, Timmis et al., 2004). Estimations for the frequency of EGT during the primary endosymbiosis range between 18% of the Arabidopsis thaliana genome (Martin et al., 2002) and 11% of the Cyanophora genome (Reyes-Prieto et al., 2006).

Euglena gracilis is well suited for the study of endosymbiosis and endosymbiotic gene transfer because its plastid was acquired by a secondary endosymbiosis, but it includes no remains of the endosymbiotic nucleus (McFadden, 2001). Moreover, E. gracilis shares a common ancestor with the Kinetoplastida (Adl et al., 2005), none of which seem to have experienced a secondary endosymbiosis (Rogers et al., 2006). Hence, by the sequence similarity criterion, the genome of E. gracilis is expected to be a hybrid composed of four main gene classes: (i) Euglena-specific genes, (ii) Kinetoplastida-specific genes, (iii) eukaryotic genes that are spread in other eukaryotes, and (iv) genes acquired during the secondary endosymbiosis. Clear candidates for the latter group are genes that have homologues only in photoautotrophic eukaryotes. In some cases the acquired gene replaced an orthologous gene within the host (Henze et al., 1995). Such genes have homologues in both photoautotrophic and heterotrophic eukaryotes, but are closely related to the former. Because of these distinct gene origins, a single bifurcating tree cannot accurately describe the chimeric gene collection of E. gracilis because genome evolution by endosymbiotic gene transfer is a non tree-like process. Here, we describe the genome composition of E. gracilis as estimated from random cDNA sequences while investigating methods for reconstructing the genomic history of symbiotic hybrids.

Section snippets

Materials and methods

From E. gracilis cDNA libraries prepared from cells grown under aerobic and anaerobic conditions (Rotte et al., 2001), 10,793 clones (5450 from aerobically and 5343 from anaerobically cultured cells) were sequenced. That fell into 2667 unique sequences (accessions EL579575–EL582344 in dbEST). The ESTs were BLASTed (Altschul et al., 1997) against 14 eukaryotic genomes (Table S1) using BLASTX. Reading frames were determined by BLASTX alignment. Forty-one ESTs harbored conflicting reading frames

Results and discussion

We sequenced a sample of 2770 E. gracilis ESTs, of which 841 sequences had homologues in a sample of 14 other eukaryotic genomes. One approach to examine the genomic history of symbiotic hybrids is to examine patterns of shared genes. We classified the 841 genes into the following gene classes: genes that have homologues in Kinetoplastida, homologues in heterotrophic eukaryotes (animals and fungi), homologues in photoautotrophic eukaryotes (a plant, a green alga and a diatom) and all of the

Conclusions

The genome of E. gracilis is a hybrid of photoautotrophic and heterotrophic genomes as the nearest neighbors of its genes attest. However, no phylogenetic tree can illustrate this evolutionary history because phylogenetic trees are designed to reflect only scenarios of vertical evolution with descent from a single common ancestor (Dagan and Martin, 2006), whereas the E. gracilis genome has two distinct ancestors. The phylogenetic tree reconstructed for the globally distributed genes in our

Acknowledgements

We thank Gabriel Gelius-Dietrich for his help in analyzing the data and Katrin Henze and Toni Gabaldón for helpful feedback.

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