Host retargeting predominated over gene transfer during early chromatophore integration in Paulinella micropora

Abstract

The relative contributions of gene acquisition and protein retargeting to early organellogenesis remain debated. We addressed this question for the recently evolved chromatophore of Paulinella micropora, which provides a unique window into the initial stages of primary organelle integration. Using a stringent phylogenomic pipeline, we identified 282 P. micropora gene families whose origin can be attributed to horizontal gene transfer (HGT) with high confidence, including 115 for which we could confidently assess the donor lineages. In addition to the expected cyanobacterial signal from the chromatophore ancestor, we detected recurrent contributions from Gammaproteobacteria, Bacteroidota, Actinobacteriota, and Chlamydiota. Relative stem-length analyses indicate that these donors contributed in temporally structured periods (waves), with several non-cyanobacterial signals older than the median cyanobacterial signal and others clearly more recent. HGT-derived genes are enriched in transport and metabolic functions, which might have been relevant to host-symbiont interaction. However, based on computational predictions, the chromatophore-targeted proteome is dominated by vertically inherited host genes with only 36 of 287 predicted chromatophore-targeted nucleus-encoded proteins being of HGT origin, the majority of which are absent in Paulinella chromatophora, suggesting a recent origin in P. microporalineage. Thus, although repeated horizontal acquisition from multiple bacterial partners shaped the nuclear genome of P. micropora, early chromatophore integration appears to have been dominated by host-derived retargeting, with HGT providing a smaller but detectable complementary contribution. These results support a mixed model of organellogenesis in which targeting and gene transfer act together, but with host retargeting playing the dominant early role.