Non-photosynthetic Plastid Replacement by a Primary Plastid in the Making

Abstract

The integration of a cyanobacterium into a heterotrophic eukaryote gave rise to the primary plastid [~]1.5 Gya. This rare cyanobacterium-to-plastid transition has only been reported once more in Paulinella chromatophora [~]100 Mya. Unfortunately, the order and relative importance of organellogenesis events have been blurred by time in primary plastids and obscured by P. chromatophora becoming phototrophic. Here, we characterize the tripartite symbiosis in a benthic dinoflagellate (Sinophysis sp.) using diverse single-cell methods. Sinophysis houses a photosynthetic cyanobacterium closely interacting with an alphaproteobacterial endosymbiont. The cyanobacterium is in the intermediate stage of symbiont-to-organelle transition, with the host likely supporting it with metabolites and proteins, and controlling its cell division. Surprisingly, it seems to have replaced the hosts remnant non-photosynthetic plastid. Our results support mixotrophy, horizontal gene transfer, co-symbioses, and cell division control as early drivers of primary plastid origin and highlight the importance of protists for deciphering organellogenesis events.