Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin

Abstract

The transition from endosymbiont to organelle in eukaryotic cells involves the transfer of significant numbers of genes to the host genomes, a process known as endosymbiotic gene transfer (EGT). In the case of plastid organelles, EGTs have been shown to leave a footprint in the nuclear genome that can be indicative of ancient photosynthetic activity in present-day plastid-lacking organisms, or even hint at the existence of cryptic plastids. Here, we evaluated the impact of EGT on eukaryote genomes by reanalyzing the recently published EST dataset for Chromera velia, an interesting test case of a photosynthetic alga closely related to apicomplexan parasites. Previously, 513 genes were reported to originate from red and green algae in a 1:1 ratio. In contrast, by manually inspecting newly generated trees indicating putative algal ancestry, we recovered only 51 genes congruent with EGT, of which 23 and 9 were of red and green algal origin, respectively, whereas 19 were ambiguous regarding the algal provenance. Our approach also uncovered 109 genes that branched within a monocot angiosperm clade, most likely representing a contamination. We emphasize the lack of congruence and the subjectivity resulting from independent phylogenomic screens for EGT, which appear to call for extreme caution when drawing conclusions for major evolutionary events.

Fig. 1.—

Examples of maximum likelihood trees congruent with EGT from a red algal endosymbiont. (a) Signal recognition particle-docking protein. (b) Folate biopterin transporter. (c) Vitamin k epoxide reductase. Numbers at nodes represent bootstrap proportion; only values higher than 60% are shown. For clarity, only the relevant taxa are shown (complete taxon list is available in Supplementary Material online); branches and taxa are colored according to their taxonomy: dark blue: C. velia; red: red algae; green: viridiplantae; orange: stramenopiles; light blue: haptophytes, cryptophytes; brown: Rhizaria; pink: alveolates; black: prokaryotes, animals, fungi, Amoebozoa. All trees congruent with EGT from a red algal endosymbiont are found in supplementary figure S2 (Supplementary Material online).

Fig. 2.—

Examples of maximum likelihood trees congruent with EGT from a green algal endosymbiont. (a) Fructose-bisphosphate aldolase c. (b) No function prediction. (c) Gun4 domain protein. Numbers at nodes represent bootstrap proportion; only values higher than 60% are shown. For clarity, only the relevant taxa are shown (complete taxon list is available in Supplementary Material online); branches and taxa are colored according to their taxonomy: dark blue: C. velia; red: red algae; green: viridiplantae; orange: stramenopiles; light blue: haptophytes, cryptophytes; brown: Rhizaria; pink: alveolates; black: prokaryotes, animals, fungi, Amoebozoa. All trees congruent with a green algal origin are found in supplementary figure S3 (Supplementary Material online).

Fig. 3.—

Examples of maximum likelihood trees congruent with EGT from an algal endosymbiont, but the algal type could not be determined. (a) Plastid terminal oxidase. (b) Chlorophyll synthetase. Numbers at nodes represent bootstrap proportion; only values higher than 60% are shown. For clarity, only the relevant taxa are shown (complete taxon list is available in Supplementary Material online); branches and taxa are colored according to their taxonomy: dark blue: C. velia; red: red algae; green: viridiplantae; orange: stramenopiles; light blue: haptophytes, cryptophytes; brown: Rhizaria; turquoise green: glaucophytes; black: prokaryotes, animals, fungi, Amoebozoa. All trees congruent with an algal origin are found in supplementary figure S4 (Supplementary Material online).

Fig. 4.—

Venn diagram showing the number of overlapping genes between this study and Woehle et al. (2011). The filled circles correspond to the genes recovered in this study.