Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora

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 because they date back more than 1 billion years. The amoeba Paulinella chromatophora contains nascent photosynthetic organelles of more recent evolutionary origin (∼60 Mya) termed chromatophores (CRs). After the initial endosymbiotic event, the CR genome was reduced to approximately 30% of its presumed original size and more than 30 expressed genes were transferred from the CR to the amoebal nuclear genome. Three transferred genes— psaE , psaK1 , and psaK2 —encode subunits of photosystem I. Here we report biochemical evidence that PsaE, PsaK1, and PsaK2 are synthesized in the amoeba cytoplasm and traffic into CRs, where they assemble with CR-encoded subunits into photosystem I complexes. Additionally, our data suggest that proteins routed to CRs pass through the Golgi apparatus. Whereas genome reduction and transfer of genes from bacterial to host genome have been reported to occur in other obligate bacterial endosymbioses, this report outlines the import of proteins encoded by such transferred genes into the compartment derived from the bacterial endosymbiont. Our study showcases P . chromatophora as an exceptional model in which to study early events in organellogenesis, and suggests that protein import into bacterial endosymbionts might be a phenomenon much more widespread than currently assumed.

Symbiosis as a General Principle in Eukaryotic Evolution

“…Unlike mitochondria, which evolved just once, chloroplasts have evolved from two different cyanobacterial groups (Keeling 2013). One cyanobacterial-derived chloroplast is allied to Synechoccus and has been reported in the rhizarian amoeba Paulinella chromatophora (Nakayama and Ishida 2009; Nowack and Grossman 2012). The other lineage is in the very successful Archaeplastids, including both algae (e.g., Rhodophytes, Chlorophytes) and terrestrial plants, with the subsequent evolution of some algae into secondary, and even tertiary, chloroplasts in further groups of eukaryotes (Keeling 2013).…”

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

“…Some of these symbioses can form highly integrated organismal and genetic mosaics that, in many ways, resemble organelles (8)(9)(10)(11). Like organelles, these endosymbionts have genomes encoding few genes (12,13), rely on gene products of bacterial origin that are encoded on the host genome (9-11, 14, 15), and in some cases, import protein products encoded by these horizontally transferred genes back into the symbiont (16,17). The names given to these bacteria-endosymbiont, protoorganelle, or bona fide organelle-are a matter of debate (18)(19)(20)(21).…”

Protein translocons in photosynthetic organelles of Paulinella chromatophora

“…Mackiewicz et al [20] also identified additional putative elements of the system, for example chaperons in the intermembrane space and components of the molecular motor responsible for pulling the imported proteins into the chromatophore stroma. It should be noted that part of the model, concerning the vesicular trafficking to the outer chromatophore membrane, has recently been confirmed by Nowack et al [21]. They used immunogold labeling electron microscopy to show that PsaE, PsaK1 and PsaK2 from Paulinella CCAC 0185 strain are localized both in chromatophores and the endomembrane system, including the Golgi apparatus.…”