Collaborative Research: Evolution of acquired phototrophy by organelle sequestration in Mesodinium ciliates

This project offers a unique perspective into evolutionary processes that showcase both the extraordinary complexity of eukaryotic cells and help us to better understand how chloroplasts have spread around the tree of life. Research generated by this project will reveal adaptations for maintaining this cellular complexity in a unicellular organism, which has diverged from ancestors inhabiting ponds, estuaries, and sediment surface habitats, to become a major photosynthetic planktonic species in the world’s coastal oceans with wide reaching ecological roles. This transition is even more remarkable due its precariousness - its cellular and metabolic complexity and photosynthetic capabilities are the result of stealing and repurposing cell parts and genes of its algal prey. This research will determine how this process happens, and thereby shed some light on important, yet enigmatic, evolutionary processes. The project will help to train two postdoctoral scientists and prepare them for a professional career in scientific research. The project will also train undergraduate students in the laboratory, and will engage with the Zephyr Foundation, a marine science literacy and education program, which serves regional schools (levels 6-12), including districts with predominantly underrepresented groups in sciences. The project will also engage with the public in a collaboration with the Santa Barbara Museum of Natural History’s Underwater Parks Day to help educate the public about the oceans’ “invisible” (i.e., microscopic) biodiversity. The project will compare cellular, metabolic, and genetic adaptations across a genus of ciliates that span functional nutritional modes of heterotrophy to phototrophy, through a continuum of mixotrophy. Mixotrophy in Mesodinium is driven by organelle stealing (or kleptoplasty), which in M. chamaeleon evenly supports its nutritional and energy needs between feeding and photosynthesis. However, in M. rubrum it is more a means to steal organelles, including the active nucleus of its prey, to fully exploit its prey’s photosynthetic metabolism. Understanding how M. rubrum has adapted to be fully reliant on stolen organelles and their metabolism for its survival is one of the main objectives of this project. The project will use comparative omics approaches between these two species and the heterotroph, M. pulex, to illuminate genetic and metabolic adaptations and innovations. The project will also use spatial proteomics and immunochemistry, to understand how proteins from the stolen nucleus in M. rubrum transit to the chloroplasts, despite massive reorganization and loss of endomembrane continuity in their new host. The same techniques will also seek to understand what ciliate genes may be contributing to maintaining and controlling stolen organelles and facilitating exploitation of their metabolism. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.