Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis

Abstract

AbstractKleptoplasts are distinct among photosynthetic organelles in eukaryotes (i.e, plastids) because they are routinely sequestered from prey algal cells and function only temporarily in the new host cell. Therefore, the hosts of kleptoplasts benefit from photosynthesis without constitutive photoendosymbiosis. Here, we report that the euglenozoanRapaza viridishas only kleptoplasts derived from a specific strain of green alga,Tetraselmissp., but no canonical plastids like those found in its sister group, the Euglenophyceae.R. viridisshowed a dynamic change in the accumulation of cytosolic polysaccharides in response to light– dark cycles, and13C isotopic labeling of ambient bicarbonate demonstrated that these polysaccharides originatein situvia photosynthesis; these data indicate that the kleptoplasts ofR. viridisare functionally active. We also identified 247 sequences encoding putative plastid-targeting proteins and 35 sequences of presumed kleptoplast transporters in the transcriptome ofR. viridis. These genes originated in a wide range of algae other thanTetraselmissp., the source of the kleptoplasts, suggesting a long history of repeated horizontal gene transfer events from different algal prey cells. Many of the kleptoplast proteins, as well as the protein-targeting system, inR. viridiswere shared with members of the Euglenophyceae, providing evidence that the early stages in the endosymbiotic origin of euglenophyte plastids also involved kleptoplasty.