Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?

Abstract

Background: Ancient endosymbioses are responsible for the origins of mitochondria and plastids, and they contribute to the divergence of several major eukaryotic groups. Although chlamydiae, a group of obligate intracellular bacteria, are not found in plants, an unexpected number of chlamydial genes are most similar to plant homologs, which, interestingly, often contain a plastid-targeting signal. This observation has prompted several hypotheses, including gene transfer between chlamydiae and plant-related groups and an ancestral relationship between chlamydiae and cyanobacteria.

Results: We conducted phylogenomic analyses of the red alga Cyanidioschyzon merolae to identify genes specifically related to chlamydial homologs. We show that at least 21 genes were transferred between chlamydiae and primary photosynthetic eukaryotes, with the donor most similar to the environmental Protochlamydia. Such an unusually high number of transferred genes suggests an ancient chlamydial endosymbiosis with the ancestral primary photosynthetic eukaryote. We hypothesize that three organisms were involved in establishing the primary photosynthetic lineage: the eukaryotic host cell, the cyanobacterial endosymbiont that provided photosynthetic capability, and a chlamydial endosymbiont or parasite that facilitated the establishment of the cyanobacterial endosymbiont.

Conclusion: Our findings provide a glimpse into the complex interactions that were necessary to establish the primary endosymbiotic relationship between plastid and host cytoplasms, and thereby explain the rarity with which long-term successful endosymbiotic relationships between heterotrophs and photoautotrophs were established. Our data also provide strong and independent support for a common origin of all primary photosynthetic eukaryotes and of the plastids they harbor.

Figure 1

Phylogenetic analyses of chlamydiae-like genes in primary photosynthetic eukaryotes. Numbers above the branch show bootstrap values for maximum likelihood and distance analyses, respectively. Asterisks indicate values lower than 50%. (a) 2-C-methyl-D-erythritol 4-phosphate cytidylyltransferase (ispD). (b) 4-diphosphocytidyl-2-C-methyl-D-erythritol kinase (ispE). (c) β-Ketoacyl-ACP synthase (fabF). (d) Aspartate transaminase. Note that red algal and green plant sequences form a well supported monophyletic group with environmental Protochlamydia homologs. mt, mitochondrial precursor. Colors represent different phylogenetic affiliations.

Figure 2

Primary photosynthetic eukaryotes contain gene copies of both plastidic and chlamydial origin. Numbers above the branch show bootstrap values for maximum likelihood and distance analyses, respectively. Asterisks indicate values lower than 50%. (a) 4-hydroxy-3-methylbut-2-en-1-yl diphosphate synthase (gcpE). (b) Enoyl-ACP reductase (fabI). Note that in panel (a) sequences from red algae and glaucophytes are of plastidic origin, whereas those from green plants, apicomplexans, haptophytes, and chlorarachniophytes are of chlamydial origin. Also note that that in panel (b) sequences from green plants, diatoms, chlorarachniophytes, and apicomplexans form a strongly supported group, whereas cyanobacterial and red alga Cyanidioschyzon homologs form another group. Colors represent different phylogenetic affiliations.

Figure 3

Hypothetic stages of plastid origin and establishment. The stages (as discussed in the text) are displayed as follows: (a,b) first stage; (c) second stage; (d) third stage; and (e) fourth stage. White, yellow, and green colors show α-proteobacterial (mitochondrial), chlamydial, and cyanobacterial endosymbionts, as well as genes and proteins of their respective origins. Arrows directly from the endosymbiont point to the symbiotic partner that receives the benefit, and the thickness of the arrow indicates the degree of benefit. Dashed lines indicate directions of intracellular gene transfer, whereas solid lines show protein targeting of the transferred genes. Crosses indicate chlamydial endosymbiont and gene transfer processes that might not exist in extant photosynthetic eukaryotes. Note that chlamydial endosymbiont was initially a bacterial parasite in the first stage, but it had a transient mutualistic relationship with the host cell in the second and third stages, and then might have degenerated in modern photosynthetic eukaryotes. Note also that the cyanobacterial endosymbiont was initially captured to solely benefit the host cell (panel b), and then received metabolites from the host cell (a process facilitated by the chlamydial endosymbiont) and was gradually transformed into a plastid organelle in the host cell (panels d and e).