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9.C.18. The Chromatophore Protein Entry System (CPES) Family 

Paulinella chromatophora is a cercozoan amoeba that contains 'chromatophores,' which are photosynthetic inclusions of cyanobacterial origin. The discovery that chromatophores evolved independently of plastids, underwent major genome reduction, and transferred genes to the host nucleus about ~100 M years ago, has highlighted P. chromatophora as a model to infer early steps in the evolution of photosynthetic organelles (Nowack et al. 2011Oberleitner et al. 2020). At least one-third of the chromatophore proteome consists of nucleus-encoded (NE) proteins that are imported across the chromatophore double envelope membranes (Archibald 2017). Protein import of nuclearly encoded genes into the compartment derived from the bacterial endosymbiont is poorly characterized (Nowack and Grossman 2012). Two photosynthesis-related genes (psaI and csos4A) are encoded by both the nuclear and chromatophore genomes (Zhang et al. 2017). Chromatophore-targeted proteins exceeding 250 aas carry a conserved N-terminal extension, presumably involved in protein targeting, termed the chromatophore transit peptide (crTP). Short imported proteins do not carry discernable targeting signals (Singer et al. 2017). To explore whether the import of proteins is accompanied by their N-terminal processing, Oberleitner et al. 2022 identified the N-termini of 208 chromatophore-localized proteins by a mass spectrometry-based approach. This study revealed extensive N-terminal acetylation and proteolytic processing in both NE and chromatophore-encoded (CE) fractions of the chromatophore proteome. Mature N-termini of 37 crTP-carrying proteins were identified, of which 30 were cleaved in a common processing region. Only the N-terminal approximately 50 aas (part 1) become cleaved upon import. This part contains a conserved adaptor protein-1 complex-binding motif known to mediate protein sorting at the trans-Golgi network followed by a predicted TMS, implying that part 1 anchors the protein co-translationally in the endoplasmic reticulum and mediates trafficking to the chromatophore via the Golgi. The C-terminal part 2 contains conserved secondary structural elements, remains attached to the mature proteins, and might mediate translocation across the chromatophore inner membrane. Short imported proteins remain largely unprocessed. Thus, N-terminal processing of proteins encoded in an evolutionary-early-stage organelle and suggests host-derived posttranslationally acting factors involved in regulation of the CE chromatophore proteome (Oberleitner et al. 2022).

References associated with 9.C.18 family:

Archibald, J.M. (2017). Evolution: Protein Import in a Nascent Photosynthetic Organelle. Curr. Biol. 27: R1004-R1006. 28950079
Nowack, E.C. and A.R. Grossman. (2012). Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc. Natl. Acad. Sci. USA 109: 5340-5345. 22371600
Nowack, E.C., H. Vogel, M. Groth, A.R. Grossman, M. Melkonian, and G. Glöckner. (2011). Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol Biol Evol 28: 407-422. 20702568
Oberleitner, L., A. Perrar, L. Macorano, P.F. Huesgen, and E.C.M. Nowack. (2022). A bipartite chromatophore transit peptide and N-terminal protein processing in the Paulinella chromatophore. Plant Physiol. 189: 152-164. 35043947
Oberleitner, L., G. Poschmann, L. Macorano, S. Schott-Verdugo, H. Gohlke, K. Stühler, and E.C.M. Nowack. (2020). The Puzzle of Metabolite Exchange and Identification of Putative Octotrico Peptide Repeat Expression Regulators in the Nascent Photosynthetic Organelles of. Front Microbiol 11: 607182. 33329499
Singer, A., G. Poschmann, C. Mühlich, C. Valadez-Cano, S. Hänsch, V. Hüren, S.A. Rensing, K. Stühler, and E.C.M. Nowack. (2017). Massive Protein Import into the Early-Evolutionary-Stage Photosynthetic Organelle of the Amoeba Paulinella chromatophora. Curr. Biol. 27: 2763-2773.e5. 28889978
Zhang, R., E.C. Nowack, D.C. Price, D. Bhattacharya, and A.R. Grossman. (2017). Impact of light intensity and quality on chromatophore and nuclear gene expression in Paulinella chromatophora, an amoeba with nascent photosynthetic organelles. Plant J. 90: 221-234. 28182317