Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis

Significance Endosymbiotic gene transfer from the plastid genome to the nucleus comprises the most significant source of horizontal gene transfer in photosynthetic eukaryotes. We investigated genomic data at the infragenic level to determine whether the cyanobacterial endosymbiont also contributed gene fragments (i.e., domains) to create novel nuclear-encoded proteins. We found 67 such gene families that are expressed as RNA and widely distributed among plants and algae. At least 23 genes are putatively involved in redox regulation and light response, namely the maintenance of a photodynamic organelle. Our results add a new layer of complexity to plastid integration and point to the role of fused proteins as key players in this process. The integration of foreign genetic information is central to the evolution of eukaryotes, as has been demonstrated for the origin of the Calvin cycle and of the heme and carotenoid biosynthesis pathways in algae and plants. For photosynthetic lineages, this coordination involved three genomes of divergent phylogenetic origins (the nucleus, plastid, and mitochondrion). Major hurdles overcome by the ancestor of these lineages were harnessing the oxygen-evolving organelle, optimizing the use of light, and stabilizing the partnership between the plastid endosymbiont and host through retargeting of proteins to the nascent organelle. Here we used protein similarity networks that can disentangle reticulate gene histories to explore how these significant challenges were met. We discovered a previously hidden component of algal and plant nuclear genomes that originated from the plastid endosymbiont: symbiogenetic genes (S genes). These composite proteins, exclusive to photosynthetic eukaryotes, encode a cyanobacterium-derived domain fused to one of cyanobacterial or another prokaryotic origin and have emerged multiple, independent times during evolution. Transcriptome data demonstrate the existence and expression of S genes across a wide swath of algae and plants, and functional data indicate their involvement in tolerance to oxidative stress, phototropism, and adaptation to nitrogen limitation. Our research demonstrates the “recycling” of genetic information by photosynthetic eukaryotes to generate novel composite genes, many of which function in plastid maintenance.