The colorless dictyochophyte Ciliophrys sp. Baltic has lost a plastid but hosts a bacterial endosymbiont

Organelle loss represents an extreme case of reductive evolution, with very few cases of plastid elimination known in free-living ancestrally photosynthetic taxa. Here we show that Ciliophrys sp. Baltic, representing a poorly studied non-photosynthetic lineage within the stramenopile algal class Dictyochophyceae, has undergone a secondary loss of its plastid. Genomic and transcriptomic analyses demonstrate the absence of both a plastid genome and nuclear genes critical for plastid biogenesis, although a few original plastid-targeted enzymes persist with a changed localization. Unexpectedly, Ciliophrys sp. Baltic harbors a bacterial endosymbiont, Candidatus Penulousia baltica sp. nov. (Rickettsiales). Analysis of its genome revealed previously unrecognized metabolic features among Rickettsiales. The bacterium exploits its host metabolically and presumably manipulates it with an arsenal of putative effector proteins. However, it might help offset some of the biosynthetic deficiencies of its host stemming from the plastid loss by providing heme and a lysine precursor. Our study establishes a single-cell model system for studying plastid loss and endosymbiont acquisition. A study reveals an independent case of plastid loss and a metabolic partnership with a bacterial endosymbiont in an understudied lineage of non-photosynthetic ochrophytes.