What’s Eating Eu? The Role of Eukaryote/Eukaryote Endosymbioses in Plastid Origins

Abstract

The plastids of green algae, and their descendants the land plants, clearly arose from a cyanobacterium-like endocytobiont. An early eukaryote (thus far unidentified) is believed to have phagocytosed a photosynthetic prokaryote and retained it as an endocytobiont. Having relinquished its autonomy, the endocytobiont is now reduced to organelle status (exogenosome) within the former eukaryotic host. The two membranes surrounding the plastid probably represent the two membranes of the gram-negative endocytobiont. A third membrane (presumed to have been created from the host plasma membrane during the en-gulfment of the endocytobiont) is now apparently lost. This scenario for plastid origin in green algae is termed a primary endosymbiosis. Plastids of red algae probably also derive from a primary endosymbiosis, quite possibly the same one as led to green algal plastids. Origins of plastids in other algal groups are less clear. The three-membraned plastids of dinoflagellates and euglenoids could also have arisen from one or more primary endosymbioses but with the food vacuole membrane being retained. However, the paucity of molecular data, particularly from dinoflagellates, leaves the origin of their plastids open to several different interpretations. The origin of plastids surrounded by four membranes (as occur in heterokonts, haptophytes, cryptophytes, and chlorarachniophytes) is hypothesised to involve two sequential endocytobioses. First, a primary endosymbiosis between a eukaryote and a prokaryote created a photosynthetic eukaryote analogous to, or perhaps even homologous to, the archetypal algal cell. This primary endosymbiosis was then followed by secondary endosymbiosis between a phagotrophic eukaryote and the product of the primary endosymbiosis to create a eukaryote with a photosynthetic eukaryotic endocytobiont. Secondary endosymbiosis produces plastids with four membranes: two from the original gram-negative prokaryote, a third from the plasma membrane of the primary host, and a fourth from the food vacuole of the secondary host. Initially, the nucleus and cytoplasm of the endocytobiont probably persisted, but in the case of heterokonts and haptophytes these structures have now apparently vanished leaving an essentially empty space between the endocytobiont’s plasma membrane and the two membranes of the plastid. In the case of cryptomonads and chlorarachniophytes, however, it has now been shown that vestiges of the endocytobiont’s nucleus and cytoplasm are retained. Now much reduced, these nucleocytoplasmic remnants are an invaluable key to unraveling the history of plastid origins through eukaryote/eukaryote en-docytobioses. The extra membranes surrounding the plastids pose novel challenges for understanding targeting of proteins into plastids and a hypothesis for targeting is presented. The extraordinarily compact nuclear genomes of the en-docytobionts are now being sequenced and could prove to be useful models for the coming wave of eukaryotic genome research.