Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?

Abstract

Eukaryotes acquired the ability to process photosynthesis by engulfing a cyanobacterium and transforming it into a genuine organelle called the plastid. This event, named primary endosymbiosis, occurred once more than a billion years ago, and allowed the emergence of the Archaeplastida, a monophyletic supergroup comprising the green algae and plants, the red algae and the glaucophytes. Of the other known cases of symbiosis between cyanobacteria and eukaryotes, none has achieved a comparable level of cell integration nor reached the same evolutionary and ecological success than primary endosymbiosis did. Reasons for this unique accomplishment are still unknown and difficult to comprehend. The exploration of plant genomes has revealed a considerable amount of genes closely related to homologs of Chlamydiae bacteria, and probably acquired by horizontal gene transfer. Several studies have proposed that these transferred genes, which are mostly involved in the functioning of the plastid, may have helped the settlement of primary endosymbiosis. Some of these studies propose that Chlamydiae and cyanobacterial symbionts coexisted in the eukaryotic host of the primary endosymbiosis, and that Chlamydiae provided solutions for the metabolic symbiosis between the cyanobacterium and the host, ensuring the success of primary endosymbiosis. In this review, I present a reevaluation of the contribution of Chlamydiae genes to the genome of Archaeplastida and discuss the strengths and weaknesses of this tripartite model for primary endosymbiosis.

The Glaucophyta: the blue-green plants in a nutshell

“…A controversial bacterial signature identified in Archaeplastida genomes, recently corroborated by the inclusion of the Cyanophora genome data, is the dozens (between 50 and 70) of genes putatively acquired from Chlamydiaelike bacteria via gene transfer early in the evolution of this eukaryote supergroup [8,22,[93][94][95]. Interestingly, some of these Chlamydiae-derived proteins are plastid-localized, or contain predicted plastid-targeting signals [93,94].…”

“…An alternative scenario notes that the number of Chlamydiae-like genes is relatively small and lower than the number of Archaeplastida genes that are likely derived from other bacterial groups (e.g., a few hundreds from diverse proteobacteria and actinobacteria), and that typical HGT from free-living bacteria better explains the presence of Chlamydiae-like sequences [97]. Regardless of the likelihood of the proposed tripartite scenario, the significant physiological roles of some of the Chlamydiae-derived proteins in plastid functions (e.g., NTT and UhpC-type transporter) and polysaccharide metabolism (e.g., GlgA), shared by glaucophytes, red algae and viridiplants, suggests that the recruitment of these proteins from Chlamydiae occurred in the common ancestor of the Archaeplastida [93][94][95].…”

“…Briefly, this hypothesis postulates that the metabolic interaction of three symbiotic partners (i.e., eukaryote, Chlamydiae-like, and cyanobacterium) established a steady flux of carbon compounds, which resulted in a key event to consolidate a stable eukaryote-cyanobacterium endosymbiosis [22,96]. A recent review published in Acta Societatis Botanicorum Poloniae thoroughly discusses diverse aspects of this tripartite hypothesis [95].…”

Symbiogenesis, gradualism, and mitochondrial energy in eukaryote origin

“…That idea involves a chlamydial symbiont that helped the cyanobacterium become a plastid. The "chlamydioplast" notion was construed entirely from genome data; for a critical review of the idea explaining its a flaws in context, see (155). Importantly, the phylogenies that are claimed as support for the chlamydia story do not support it at all (155,156).…”

Letter from the Editors

“…According to one of the recent hypotheses, the cyanobacterial ancestor of primary plastids received some help during its initial evolution from a concomitant chlamydial endosymbiont [5]. This hot topic is critically discussed by Deschamps [6].…”