Targeting Plastids in an Animal Cell

Sacoglossa display one of nature’s most curious photosymbiotic systems. Instead of establishing a symbiosis with an algal partner, like other photosymbiotic animals, these slugs sequester only the plastids of their macroalgal prey. The stolen plastids—kleptoplasts—are phagocytized by epithelial cells of the digestive gland system and are initially encapsulated by a phagosomal membrane. In some sacoglossan species, the kleptoplasts remain photosynthetically active over weeks or months, autonomously and separated from the genetic support the algal nucleus offers. The photosynthetic activity of the kleptoplasts resulted in a decade-long debate on whether the slugs support the kleptoplasts with proteins the animals encode due to genes horizontally transferred from the alga. Transcriptome and genome analyses have revealed that slugs do not encode algal-derived genes, and other unknown mechanisms that explain kleptoplast longevity in Sacoglossa are at work. In algae and plants, dual-targeting nuclear-encoded proteins to mitochondria and plastids is common. The correct targeting of the proteins is based on a sequence and its charge, and a median charge could allow the translocation of mitochondrial slug proteins to the chloroplasts. Whether dual targeting is involved in plastid longevity in sacoglossan sea slugs is unknown. A major challenge would be first to translocate the proteins across the phagosomal membrane, if not removed, before they can enter the kleptoplasts. The system is even more complex as some sacoglossan species sequester heterokontophyte plastids that are surrounded by four membranes in their native host. However, only the inner two of those four membranes appear to be retained in the animal cells. In this chapter, we summarize the current knowledge on the slug-kleptoplast system from a cell biology point of view and provide a theoretical road map on how animal proteins could be translocated to the kleptoplasts—or what would hinder such transport.