Loss of key endosymbiont genes may facilitate early host control of the chromatophore in Paulinella

The primary plastid endosymbiosis (∼124 Mya) that occurred in the heterotrophic amoeba lineage, Paulinella, is at an earlier stage of evolution than in Archaeplastida, and provides an excellent model for studying organelle integration. Using genomic data from photosynthetic Paulinella, we identified a plausible mechanism for the evolution of host control of endosymbiont (termed the chromatophore) biosynthetic pathways and functions. Specifically, random gene loss from the chromatophore and compensation by nuclear-encoded gene copies enables host control of key pathways through a minimal number of evolutionary innovations. These gene losses impact critical enzymatic steps in nucleotide biosynthesis and the more peripheral components of multi-protein DNA replication complexes. Gene retention in the chromatophore likely reflects the need to maintain a specific stoichiometric balance of the encoded products (e.g., involved in DNA replication) rather than redox state, as in the highly reduced plastid genomes of algae and plants.