Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs

Some sea slug species sequester chloroplasts from algal food in their digestive gland cells and photosynthesize for up to several months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity within the animal cell without the algal nucleus. As a mechanism of the retention, there have been debates on horizontal gene transfer from the algal nucleus to animal nucleus. To settle the arguments, we, here, report the genome of a kleptoplastic sea slug Plakobranchus ocellatus and found no evidence that photosynthetic genes are encoded on its genome. Nevertheless, our long-term incubation experiment confirmed that kleptoplast photosynthesis prolongs the life of sea slug under starvation. The data present a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic and transcriptomic analysis showed that animal genes for proteolysis and immune response underwent gene expansion in the lineage to the sea slug and are upregulated in the chloroplast-enriched tissue, suggesting that these molluscan genes are involved in this DNA-independent transformation.