Early photosynthetic eukaryotes inhabited low-salinity habitats

Abstract

The early evolutionary history of the chloroplast lineage remains an open question. It is widely accepted that the endosymbiosis that established the chloroplast lineage in eukaryotes can be traced back to a single event, in which a cyanobacterium was incorporated into a protistan host. It is still unclear, however, which Cyanobacteria are most closely related to the chloroplast, when the plastid lineage first evolved, and in what habitats this endosymbiotic event occurred. We present phylogenomic and molecular clock analyses, including data from cyanobacterial and chloroplast genomes using a Bayesian approach, with the aim of estimating the age for the primary endosymbiotic event, the ages of crown groups for photosynthetic eukaryotes, and the independent incorporation of a cyanobacterial endosymbiont by Paulinella Our analyses include both broad taxon sampling (119 taxa) and 18 fossil calibrations across all Cyanobacteria and photosynthetic eukaryotes. Phylogenomic analyses support the hypothesis that the chloroplast lineage diverged from its closet relative Gloeomargarita, a basal cyanobacterial lineage, ∼2.1 billion y ago (Bya). Our analyses suggest that the Archaeplastida, consisting of glaucophytes, red algae, green algae, and land plants, share a common ancestor that lived ∼1.9 Bya. Whereas crown group Rhodophyta evolved in the Mesoproterozoic Era (1,600-1,000 Mya), crown groups Chlorophyta and Streptophyta began to radiate early in the Neoproterozoic (1,000-542 Mya). Stochastic mapping analyses indicate that the first endosymbiotic event occurred in low-salinity environments. Both red and green algae colonized marine environments early in their histories, with prasinophyte green phytoplankton diversifying 850-650 Mya.

Keywords: Cyanobacteria; chloroplast; photosynthetic eukaryotes; phylogenomics; relaxed molecular clock.

Fig. 1.

The origin and diversification of photosynthetic eukaryotes and Cyanobacteria as inferred from geologic time. The phylogenetic tree shown was estimated based on 26 genes from 117 taxa implementing Phylobayes 1.7a (97). Bayesian relaxed molecular clock analyses were carried out in Phylobayes 4.1 (39) implementing the UGAM (42) and the CAT-GTR substitution model (Table 2). Six calibration points for Cyanobacteria and 12 calibrations points for photosynthetic eukaryotes (brown circles) were used (Table 1) for the tree shown and treated as soft bounds. The root of the tree was set with a maximum age of 2.7 Bya (98) and a minimum age of 2.32 Bya (2). Age estimates for the numbered nodes (1–9) indicated are given in Table 1, which includes the corresponding values for the posterior 95% confidence intervals. GOE, Great Oxygenation Event.

Fig. 2.

Alternative hypotheses illustrating the deep-branching relationships within the Archaeplastida: ML and Bayesian topologies.

Fig. 3.

Comparison of molecular clock estimates for the studies of the divergences of the crown group of photosynthetic eukaryotes and the split of the plastid lineages from their cyanobacteria ancestors. Age divergences for this study correspond to median ages in analyses shown in Fig. 1. Circles and triangles are the mean ages for the origin of the crown group of photosynthetic eukaryotes and the common ancestor with Cyanobacteria, respectively, and the rectangles represent the confidence intervals.

Fig. 4.

Stochastic mapping analyses of the evolution of habitat. Phylogenetic tree including 119 taxa was estimated in Phylobayes 1.7a (97). A pie chart at each node indicates the MLs for three character states as follows: blue circle, marine; yellow circle, freshwater; red circle, brackish. Character states and full scientific names for abbreviated taxon names, shown here, are listed in SI Appendix, Table S2.