Towards deciphering the evolutionary process of endosymbiont – organelle transition of chromatophores in Paulinella chromatophora by MS-based spatial proteomics (LOPIT-DC)

Paulinella chromatophora stands out for its fascinating genetic, proteomic, and endosymbiotic characteristics.[1] Unlike most eukaryotes that acquired photosynthesis through primary endosymbiosis long (~1.6 billion years) ago, in which cyanobacteria were engulfed and evolved into plastids, Paulinella is the only known case in which this primary endosymbiotic event was repeated. This latest cyanobacterium uptake occurred much more recently (~0.09–0.14 billion years ago) and led to the formation of chromatophores, specialized photosynthetic organelles with a distinct genetic makeup, and provides a unique case of convergent evolution to study organellogenesis, i.e., the transition from endosymbiont to organelle. The transport mechanisms and protein targeting signals in chromatophores also differ from those in conventional plastids, underscoring their independent genetic evolution and functional specialization.

Chromatophores in P. chromatophora exhibit reductive genome evolution, reducing their coding capacity to ~25% of their initial one (still being 5–10 times larger than a typical plastid genome) and necessitating the import of nucleus-encoded proteins for various metabolic pathways. This integration of chromatophore genes into the nuclear genome, alongside the loss of specific metabolic pathways within the chromatophore itself, indicates a complex genetic and proteomic relationship between the organelle and the host cell.

Here, we performed mass spectrometry based proteomic profiling of P. chromatophora cellular fractions obtained by high-resolution separation of organelles and subcellular compartments employing the Localisation of Organelle Proteins by Isotope Tagging after Differential ultraCentrifugation (LOPIT-DC)[2] approach. Studying the spatial proteome of P. chromatophora provided valuable insights into the host - endosymbiont interplay and the evolutionary processes of organellogenesis.

Macorano L, Nowack ECM: Paulinella chromatophora. Curr Biol 2021, 31(17):R1024-R1026.Geladaki A, Kočevar Britovšek N, Breckels LM, Smith TS, Vennard OL, Mulvey CM, Crook OM, Gatto L, Lilley KS: Combining LOPIT with differential ultracentrifugation for high-resolution spatial proteomics. Nature Communications 2019, 10(1):331.