Functional control and metabolic integration of stolen organelles in a photosynthetic ciliate

Abstract

Stealing prey plastids for metabolic gain is a common phenomenon among protists within aquatic ecosystems. Ciliates of the Mesodinium rubrum species complex are unique in that they also steal a transcriptionally active but non-dividing prey nucleus, the kleptokaryon, from certain cryptophytes. The kleptokaryon enables full control and replication of kleptoplastids but has a half-life of about 10 days. Once the kleptokaryon is lost, the ciliate experiences a slow loss of photosynthetic metabolism and eventually death. This transient ability to function phototrophically allows M. rubrum to form productive blooms in coastal waters. Here, we show, using multi-omics approaches, that an Antarctic strain of the ciliate not only depends on stolen Geminigera cryophila organelles for photosynthesis but also for anabolic synthesis of fatty acids, amino acids, and other essential macromolecules. Transcription of diverse pathways was higher in the kleptokaryon than that in G. cryophila, and many increased in higher light. Proteins of major biosynthetic pathways were found in greater numbers in the kleptokaryon relative to M. rubrum, implying anabolic dependency on foreign metabolism. We show that despite losing transcriptional control of the kleptokaryon, M. rubrum regulates kleptoplastid pigments with changing light, implying an important role for post-transcriptional control. These findings demonstrate that the integration of foreign organelles and their gene and protein expression, energy metabolism, and anabolism occur in the absence of a stable endosymbiotic association. Our results shed light on potential events early in the process of complex plastid acquisition and broaden our understanding of symbiogenesis.