An Early-Branching Freshwater Cyanobacterium at the Origin of Plastids

Abstract

Photosynthesis evolved in eukaryotes by the endosymbiosis of a cyanobacterium, the future plastid, within a heterotrophic host. This primary endosymbiosis occurred in the ancestor of Archaeplastida, a eukaryotic supergroup that includes glaucophytes, red algae, green algae, and land plants [1-4]. However, although the endosymbiotic origin of plastids from a single cyanobacterial ancestor is firmly established, the nature of that ancestor remains controversial: plastids have been proposed to derive from either early- or late-branching cyanobacterial lineages [5-11]. To solve this issue, we carried out phylogenomic and supernetwork analyses of the most comprehensive dataset analyzed so far including plastid-encoded proteins and nucleus-encoded proteins of plastid origin resulting from endosymbiotic gene transfer (EGT) of primary photosynthetic eukaryotes, as well as wide-ranging genome data from cyanobacteria, including novel lineages. Our analyses strongly support that plastids evolved from deep-branching cyanobacteria and that the present-day closest cultured relative of primary plastids is Gloeomargarita lithophora. This species belongs to a recently discovered cyanobacterial lineage widespread in freshwater microbialites and microbial mats [12, 13]. The ecological distribution of this lineage sheds new light on the environmental conditions where the emergence of photosynthetic eukaryotes occurred, most likely in a terrestrial-freshwater setting. The fact that glaucophytes, the first archaeplastid lineage to diverge, are exclusively found in freshwater ecosystems reinforces this hypothesis. Therefore, not only did plastids emerge early within cyanobacteria, but the first photosynthetic eukaryotes most likely evolved in terrestrial-freshwater settings, not in oceans as commonly thought.

Keywords: chloroplasts; cyanobacteria; evolution; molecular phylogeny; phylogenomics; plastids.

Figure 1. The Position of Plastids in the Cyanobacterial Phylogeny

This Bayesian phylogenetic tree is based on the concatenation of 97 plastid-encoded proteins and their cyanobacterial homologues. Branches supported by posterior probability 1 are labeled with black circles. Maximum likelihood bootstrap value is also indicated for the branch uniting plastids with the cyanobacterium Gloeomargarita lithophora. A false-colored scanning electron microscopy image of this cyanobacterium is shown in the center of the tree. Information about the habitat and morphology of the cyanobacterial species is provided. For the complete tree, see Figure S1.

Figure 2. Supernetwork Analysis of Plastid-Encoded Proteins and Cyanobacterial Homologues

This phylogenetic supernetwork is based on the individual maximum likelihood trees of 97 plastid-encoded proteins. For a distance-based analysis of these individual proteins, see Figure S2.