Evolution of Photosynthetic Organelles Based on Studies of the Thecamoeba Paulinella chromatophora
Final Report Abstract
Endosymbiotic acquisition of bacteria by a protist, with subsequent evolution of the bacteria into mitochondria and plastids, had a transformative impact on eukaryotic biology. Reconstructing events that created a stable association between endosymbiont and host during the process of organellogenesis ‐ including establishment of regulated protein import into nascent organelles ‐ is difficult since these events date back >1 BYA. The amoeba Paulinella chromatophora contains nascent photosynthetic organelles of more recent evolutionary origin (~60 MYA) termed chromatophores. After the initial endosymbiotic event, the chromatophore genome was reduced to ~30% of its presumed original size and at least two genes were transferred from the chromatophore to the nuclear genome by a process termed endosymbiotic gene transfer (EGT). The main aims of this project were to identify further nuclear genes in P. chromatophora obtained by EGT, to assess the extent of EGT from the chromatophore, to test whether proteins encoded by these EGT genes are synthesized in the amoeba, and if so whether some of them acquired the ability to traffic back into the chromatophore. By phylogenetic analyses of a comprehensive transcriptome dataset of P. chromatophora that was generated in a collaboration with Prof. Michael Melkonian (University of Cologne) and Dr. Gernot Glöckner (Leibniz Institute for Freshwater Ecology and Inland Fisheries, Berlin) we identified >30 expressed genes that were transferred from the chromatophore to the amoebal nuclear genome. Three transferred genes, psaE, psaK1, and psaK2, encode subunits of photosystem I (PSI). By immunogold electron microscopy, isolation of PSI complexes, and differential labeling of proteins synthesized in chromatophore and cytoplasm, we obtained biochemical evidence that PsaE, PsaK1, and PsaK2 are synthesized in the amoeba cytoplasm and traffic into chromatophores where they assemble with chromatophore‐encoded subunits into PSI complexes. Additionally, our data suggest that proteins routed to chromatophores pass through the Golgi. Although genome reduction and transfer of genes from bacterial to host genome occur in other obligate bacterial endosymbioses, this is the first report of import of proteins encoded by such transferred genes into the compartment derived from the bacterial endosymbiont (outside of the one established for plastids and mitochondria). Our study showcases P. chromatophora as an exceptional model to study early events in organellogenesis, and suggests that protein import into bacterial endosymbionts might be a phenomenon much more widespread than currently assumed.
Publications
- (2011). Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol. Biol. Evol. 28: 407‐422
Nowack, E. C. M., Vogel, H., Groth, M., Grossman, A. R., Melkonian, M., and Glöckner, G.
- 10th Annual Meeting of the German Society for Endocytobiology, Düsseldorf, Germany, September 2011; “Paulinella chromatophora – The acquisition of a photosynthetic organelle”
- 59th Annual Meeting of the British Phycological Society, Cardiff, GB, January 2011; “Paulinella chromatophora – The acquisition of a photosynthetic organelle”
- (2012). Evolution eines photosynthetischen Organells. BIOspektrum 3: 337
Nowack, E. C. M.
- (2012). Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc. Natl. Acad. Sci. USA 109: 5340‐5345
Nowack, E. C. M. and Grossman, A. R.
