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

This work was performed while JH held a National Research Council AssociateshipAward at the NASA Astrobiology Institute at the Marine BiologicalLaboratory in Woods Hole, Massachusetts (NCC2-1054). Additionalsupport was provided through NSF (MCB-0237197) and NASA AISR(NNG04GP90G) grants to JPG.

© 2007 Huang and Gogarten. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The definitive version was published in Genome Biology 8 (2007): R99, doi:10.1186/gb-2007-8-6-r99.

Ancient endosymbioses are responsible for the origins of mitochondria and plastids,and they contribute to the divergence of several major eukaryotic groups. Although chlamydiae, agroup of obligate intracellular bacteria, are not found in plants, an unexpected number of chlamydialgenes are most similar to plant homologs, which, interestingly, often contain a plastid-targetingsignal. This observation has prompted several hypotheses, including gene transfer betweenchlamydiae and plant-related groups and an ancestral relationship between chlamydiae andcyanobacteria.We conducted phylogenomic analyses of the red alga Cyanidioschyzon merolae to identifygenes specifically related to chlamydial homologs. We show that at least 21 genes were transferredbetween chlamydiae and primary photosynthetic eukaryotes, with the donor most similar to theenvironmental Protochlamydia. Such an unusually high number of transferred genes suggests anancient chlamydial endosymbiosis with the ancestral primary photosynthetic eukaryote. Wehypothesize 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 cyanobacterialendosymbiont.Our findings provide a glimpse into the complex interactions that were necessary toestablish the primary endosymbiotic relationship between plastid and host cytoplasms, and therebyexplain the rarity with which long-term successful endosymbiotic relationships betweenheterotrophs and photoautotrophs were established. Our data also provide strong andindependent support for a common origin of all primary photosynthetic eukaryotes and of theplastids they harbor.