The colourless dictyochophyte Ciliophrys sp. Baltic secondarily lacks a plastid but hosts a bacterial endosymbiont

Abstract

The loss of an organelle represents an extreme case of reductive evolution. Only a few plastid loss events have been documented and they seem to be particularly rare in free-living ancestrally photosynthetic taxa. We isolated a new phagotrophic protist, Ciliophrys sp. Baltic, representing a poorly studied non-photosynthetic lineage in the stramenopile algal class Dictyochophyceae. Genomic and transcriptomic data from this organism demonstrate that it lacks a plastid genome and nuclear genes critical for plastid biogenesis. The plastid organelle is thus most likely secondarily missing from Ciliophrys sp. Baltic, although a few enzymes originally targeted to the plastid persist with a changed localization. Unexpectedly, Ciliophrys sp. Baltic harbors a bacterial endosymbiont, Candidatus Penulousia baltica sp. nov. (Rickettsiales). Analysis of its complete genome sequence uncovered unique aspects of its metabolism not previously reported in other Rickettsiales. The bacterium exploits its host metabolically and presumably manipulates it with an arsenal of putative effector proteins. However, we also found that it might help offset some of the biosynthetic deficiencies of its host stemming from the plastid loss by providing haem and a lysine precursor. Altogether, our study establishes a new single-cell model system for studying plastid loss and endosymbiont acquisition.