Diatom pyrenoids are encased in a protein shell that enables efficient CO2 fixation
Ginga Shimakawa, Manon Demulder, Serena Flori, Akihiro Kawamoto, Yoshinori Tsuji, Hermanus Nawaly, Atsuko Tanaka, Rei Tohda, Tadayoshi Ota, Hiroaki Matsui, Natsumi Morishima, Ryosuke Okubo, Wojciech Wietrzyñski, Lorenz Lamm, Ricardo D. Righetto, Clarisse Uwizeye, Benoît Gallet, Pierre‐Henri Jouneau, Christoph Gerle, Genji Kurisu, Giovanni Finazzi, Benjamin D. Engel, Yusuke Matsuda
Abstract
Pyrenoids are subcompartments of algal chloroplasts that increase the efficiency of Rubisco-driven CO 2 fixation. Diatoms fix up to 20% of global CO 2 , but their pyrenoids remain poorly characterized. Here, we used in vivo photo-crosslinking to identify pyrenoid shell (PyShell) proteins, which we localized to the pyrenoid periphery of model pennate and centric diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana . In situ cryo-electron tomography revealed that pyrenoids of both diatom species are encased in a lattice-like protein sheath. Single-particle cryo-EM yielded a 2.4-Å-resolution structure of an in vitro TpPyShell1 lattice, which showed how protein subunits interlock. T. pseudonana TpPyShell1/2 knockout mutants had no PyShell sheath, altered pyrenoid morphology, and a high-CO 2 requiring phenotype, with reduced photosynthetic efficiency and impaired growth under standard atmospheric conditions. The structure and function of the diatom PyShell provide a molecular view of how CO 2 is assimilated in the ocean, a critical ecosystem undergoing rapid change.