A Molecular Timeline for the Origin of Photosynthetic Eukaryotes

Abstract

The appearance of photosynthetic eukaryotes (algae and plants) dramatically altered the Earth's ecosystem, making possible all vertebrate life on land, including humans. Dating algal origin is, however, frustrated by a meager fossil record. We generated a plastid multi-gene phylogeny with Bayesian inference and then used maximum likelihood molecular clock methods to estimate algal divergence times. The plastid tree was used as a surrogate for algal host evolution because of recent phylogenetic evidence supporting the vertical ancestry of the plastid in the red, green, and glaucophyte algae. Nodes in the plastid tree were constrained with six reliable fossil dates and a maximum age of 3,500 MYA based on the earliest known eubacterial fossil. Our analyses support an ancient (late Paleoproterozoic) origin of photosynthetic eukaryotes with the primary endosymbiosis that gave rise to the first alga having occurred after the split of the Plantae (i.e., red, green, and glaucophyte algae plus land plants) from the opisthokonts sometime before 1,558 MYA. The split of the red and green algae is calculated to have occurred about 1,500 MYA, and the putative single red algal secondary endosymbiosis that gave rise to the plastid in the cryptophyte, haptophyte, and stramenopile algae (chromists) occurred about 1,300 MYA. These dates, which are consistent with fossil evidence for putative marine algae (i.e., acritarchs) from the early Mesoproterozoic (1,500 MYA) and with a major eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic, provide a molecular timeline for understanding algal evolution.

Ultrastructural study of plasmodesmata in the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae)

“…Brown algae (Phaeophyceae) are a member of the multicellular organisms that evolved in aquatic environment and are phylogenetically distant from the other multicellular groups such as animals, fungi, green plants and red algae (Yoon et al 2004). They are dominant in the coastal environment, forming the seaweed forests which give good habitats to aquatic animals, and contributing to the ocean carbon fixation.…”

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

“…The 'primary' plastids of red algae, glaucophyte algae and green algae, and their land-plant descendants, probably arose just once, more than a billion years ago 3,4 . Subsequent to this key event, the primary plastids of red and green algae were laterally transferred to other eukaryotes by secondary and tertiary endosymbioses, spawning some of the most abundant and ecologically important aquatic photosynthesizers on Earth such as diatoms, giant kelp, bloom-forming haptophytes and toxic dinoflagellates, as well as parasites such as the malaria pathogen Plasmodium 3 .…”

Oxygenic photosynthesis and the distribution of chloroplasts

“…It is widely accepted that chloroplasts are derived from a single one-time event where a cyanobacterium was taken up into a eukaryotic single-celled organism (Delwiche 1999) which formed the base for all eukaryotic photosynthetic organisms (Green 2010;Ryes-Prieto et al 2008;Yoon et al 2004). This idea has become a paradigm that is widely illustrated in text books and continues to have considerable support from phylogenomic analyses (Hackett et al 2007;Keeling 2010).…”

“…1, Payne et al 2010;Frei et al 2009) at the time when the proposed cyanobacterial-to-chloroplast uptake occurred in the early Proterozoic Eon. A potential eukaryotic host could have come from the base of the animal ancestral lineage, possibly related to opisthokonts (Yoon et al 2004). According to timeline calculations by Yoon et al (2004), the cyanobacterial endosymbiotic event of the cyanobacterial-to-chloroplast transition would have been somewhat prior to ca.…”

“…A potential eukaryotic host could have come from the base of the animal ancestral lineage, possibly related to opisthokonts (Yoon et al 2004). According to timeline calculations by Yoon et al (2004), the cyanobacterial endosymbiotic event of the cyanobacterial-to-chloroplast transition would have been somewhat prior to ca. 1.6 BYa with a subsequent split into the glaucophyte and red-green algal separation.…”