Dating the Origin and Spread of Plastids and Chromatophores

Abstract

Photosynthetic eukaryotes have shaped the Earth’s biosphere by producing oxygen and organic compounds using light energy in specialized organelles called plastids. Plastids evolved from free-living cyanobacteria ingested by heterotrophic unicellular eukaryotes. Two such independent engulfment processes, called cyanobacterial endosymbioses, have been reported. The first gave rise to primary plastids and three Archaeplastida lineages: glaucophytes, red algae, and green algae with land plants, whereas the second resulted in chromatophores in the rhizarian amoeba Paulinella. Importantly, Archaeplastidans donated their plastids to many protist groups, further spreading photosynthesis across the tree of life. To reveal complex plastid evolution, we performed comprehensive phylogenetic and molecular clock analyses using new fossil calibrations and the largest number yet of plastid-encoded proteins from 108 taxa, representing diverse photosynthetic organisms. Our results indicate that primary plastids evolved prior to 2.1–1.8 Ga, i.e., before glaucophytes diverged from other Archaeplastidans, and Paulinella chromatophores were likely before 292–266 Ma. Red and green algae were engulfed by cryptophyte and chlorarachniophyte ancestors between 1.7–1.4 Ga and 1.1–1.0 Ga, respectively; the former subsequently triggered plastid transfers to other eukaryotes. We also examined the impact of molecular clocks and calibration sets on age estimates, showing that clocks are the main source of variation.