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

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.

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

“…As discussed above, other stramenopile-like and red alga-like putative plastid-targeted enzymes are recognized in Euglenophyta and Chlorarachniophyta, respectively, allowing us to speculate a cryptic endosymbiosis of a non-green algal ancestor in each of the phyla [47]. Thus, the contribution of "non-green" algae to the plastid proteome in the "green" secondary phototrophs is more significant than ever thought.…”

What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses

“…Nuclear genes for chloroplast-targeted proteins of multiple phylogenetic affinities have been identified in many taxa that are not known to have undergone serial endosymbiosis, including Paulinella chromatophora, the chlorarachniophyte Bigelowiella natans, the euglenid Euglena gracilis (Archibald et al, 2003;Maruyama et al, 2011;Nowack et al, 2011) and, notably, Dinophysis acuminata, which appears to have acquired at least two genes for chloroplast-targeted proteins from a haptophyte lineage donor (Wisecaver and Hackett, 2010). On a larger scale, the identification of extensive numbers of green-algal-derived genes in diatoms and other taxa harbouring red-algal-derived chloroplasts might point to a cryptic green algal symbiosis in these lineages (Dorrell and Smith, 2011;Moustafa et al, 2009).…”

Evolutionary Origin of Euglena

“…For example, several genes encoding enzymes of the Calvin-Benson cycle share an ancestry with red algae and/or chromophytes (organisms with secondary plastids derived from red-algae) (Markunas and Triemer 2016). It seems that some of these genes were already present in the cell of the phagotrophic euglenid which enslaved the green algal endosymbiont and their presence would have facilitated the transition from an endosymbiont to a chloroplast (Maruyama et al 2011;Markunas and Triemer 2016). Such examples show the impact of lateral/ endosymbiotic gene transfers (LGT/EGT) on the evolutionary history of euglenids, the structure of their genomes and the position they hold in ecological niches.…”

“…It is uncertain whether red algal genes were acquired by lateral gene transfer (LGT) or whether they are evidence of a past endosymbiosis with a red alga. Nonetheless, the observed mosaicism of euglenid genome is a result of acquisition of genes derived from not only a distant ancestor and a green algal endosymbiont but also from other evolutionary lineages (Maruyama et al 2011). For example, several genes encoding enzymes of the Calvin-Benson cycle share an ancestry with red algae and/or chromophytes (organisms with secondary plastids derived from red-algae) (Markunas and Triemer 2016).…”

“…Surprisingly, it was revealed that the E. gracilis nuclear genome contains not only genes of green algal origin but also genes of red algal origin. Genes of red algal origin have also been found in the primary heterotrophic euglenid Peranema trichophorum (Maruyama et al 2011). It is uncertain whether red algal genes were acquired by lateral gene transfer (LGT) or whether they are evidence of a past endosymbiosis with a red alga.…”