Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista

Abstract

Assembling the global eukaryotic tree of life has long been a major effort of Biology. In recent years, pushed by the new availability of genome-scale data for microbial eukaryotes, it has become possible to revisit many evolutionary enigmas. However, some of the most ancient nodes, which are essential for inferring a stable tree, have remained highly controversial. Among other reasons, the lack of adequate genomic datasets for key taxa has prevented the robust reconstruction of early diversification events. In this context, the centrohelid heliozoans are particularly relevant for reconstructing the tree of eukaryotes because they represent one of the last substantial groups that was missing large and diverse genomic data. Here, we filled this gap by sequencing high-quality transcriptomes for four centrohelid lineages, each corresponding to a different family. Combining these new data with a broad eukaryotic sampling, we produced a gene-rich taxon-rich phylogenomic dataset that enabled us to refine the structure of the tree. Specifically, we show that (i) centrohelids relate to haptophytes, confirming Haptista; (ii) Haptista relates to SAR; (iii) Cryptista share strong affinity with Archaeplastida; and (iv) Haptista + SAR is sister to Cryptista + Archaeplastida. The implications of this topology are discussed in the broader context of plastid evolution.

Keywords: centrohelids; eukaryotes; phylogenomics; plastid evolution; tree of life.

Figure 1.

Phylogenetic tree of eukaryotes inferred from the complete dataset (150/250). The topology shown corresponds to the ML tree under the LG + C60 + F model, with both ML and Bayesian support value reported. Black dots on branches mean maximal support (i.e. 100% UFboot and SH-aLRT, and 1.0 Bayesian PP; the Bayesian CAT + GTR + Γ4 topology is shown in electronic supplementary material, figure S1). When not maximal, values are indicated only if deemed robust as follows: UFboot ≥ 95%/SH-aLRT ≥ 80%/PP ≥ 0.9. The tree is drawn rooted between Obazoa, Amoebozoa, Collodictyon, Malawimonas and the rest of eukaryotes after [42], though we note that the position of the root is under active debate.

Figure 2.

Schematics of the new backbone for the eukaryotic tree, highlighting the relationships among the main groups. The topology is based on the 148/250-slow supermatrix, and corresponds to both ML and Bayesian reconstructions under the LG + C60 + F and CAT + GTR + Γ4 models, respectively. The complete tree is presented in electronic supplementary material, figure SX. Black dots on branches mean maximal support (i.e. 100% UFboot and SH-aLRT, and 1.0 Bayesian PP). When not maximal values are indicated as followed: UFboot/SH-aLRT/PP. All supergroups indicated by the triangles received maximal support, with the exception of the grouping of Viridiplantae and glaucophytes, which was unsupported (shown by dashed lines). The size of the triangles roughly represents the diversity of taxa included in our analyses, as well as the length of the longest branch in each group. The root is placed in the same position as in figure 1.

Figure 3.

Scenarios for the origin and evolution of complex red plastids. These scenarios do not refer to any specific taxa, but rather illustrate the various possibilities discussed in the text, and show that the same diversity of plastid types can be generated by different combinations of events. (a) A single secondary endosymbiosis in the ancestor of all red plastid-bearing eukaryotes was followed only by descent with modification, as formalized in the chromalveolate hypothesis; this scenario is not supported by the current analyses. (b) Multiple independent secondary endosymbioses take place with different red algal symbionts, followed by descent with modification; this is compatible with current phylogenetic evidence from hosts, but not with evidence from plastids. (c) A single secondary endosymbiosis takes place, but is followed by serial eukaryote-to-eukaryote endosymbioses; several versions of this scenario have been proposed (see text for references), and they are consistent with current phylogenetic data.