Structural insights into thermophilic chaperonin complexes

Zengwei Liao; Chai C Gopalasingam; Masafumi Kameya; Christoph Gerle; Hideki Shigematsu; Masaharu Ishii; Takatoshi Arakawa; Shinya Fushinobu

doi:10.1016/j.str.2024.02.012

Structural insights into thermophilic chaperonin complexes

Structure. 2024 Mar 6:S0969-2126(24)00051-0. doi: 10.1016/j.str.2024.02.012. Online ahead of print.

Authors

Zengwei Liao¹, Chai C Gopalasingam², Masafumi Kameya³, Christoph Gerle², Hideki Shigematsu⁴, Masaharu Ishii³, Takatoshi Arakawa⁵, Shinya Fushinobu⁶

Affiliations

¹ Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo City, Tokyo 113-8654, Japan.
² Life Science Research Infrastructure Group, RIKEN SPring-8 Center, Kouto, Sayo, Hyogo 1-1-1, Japan.
³ Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo City, Tokyo 113-8654, Japan; Collaborative Research Institute for Innovative Microbiology, The University of Tokyo, Bunkyo City, Tokyo 113-8654, Japan.
⁴ Structural Biology Division, Japan Synchrotron Radiation Research Institute, SPring-8, Sayo, Hyogo, Japan.
⁵ Faculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, Chiba 278-8510, Japan. Electronic address: arakawa@rs.tus.ac.jp.
⁶ Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo City, Tokyo 113-8654, Japan; Collaborative Research Institute for Innovative Microbiology, The University of Tokyo, Bunkyo City, Tokyo 113-8654, Japan. Electronic address: asfushi@mail.ecc.u-tokyo.ac.jp.

PMID: 38492570
DOI: 10.1016/j.str.2024.02.012

Abstract

Group I chaperonins are dual heptamer protein complexes that play significant roles in protein homeostasis. The structure and function of the Escherichia coli chaperonin are well characterized. However, the dynamic properties of chaperonins, such as large ATPase-dependent conformational changes by binding of lid-like co-chaperonin GroES, have made structural analyses challenging, and our understanding of these changes during the turnover of chaperonin complex formation is limited. In this study, we used single-particle cryogenic electron microscopy to investigate the structures of GroES-bound chaperonin complexes from the thermophilic hydrogen-oxidizing bacteria Hydrogenophilus thermoluteolus and Hydrogenobacter thermophilus in the presence of ATP and AMP-PNP. We captured the structure of an intermediate state chaperonin complex, designated as an asymmetric football-shaped complex, and performed analyses to decipher the dynamic structural variations. Our structural analyses of inter- and intra-subunit communications revealed a unique mechanism of complex formation through the binding of a second GroES to a bullet-shaped complex.

Keywords: GroELS; chaperonin; cryo-EM; cryogenic electron microscopy; hydrogen-oxidizing bacteria; molecular chaperone; single particle analysis; thermophilic bacteria.