Alternate conformational trajectories in ribosome translocation

PLoS Comput Biol. 2024 Aug 14;20(8):e1012319. doi: 10.1371/journal.pcbi.1012319. eCollection 2024 Aug.

Abstract

Translocation in protein synthesis entails the efficient and accurate movement of the mRNA-[tRNA]2 substrate through the ribosome after peptide bond formation. An essential conformational change during this process is the swiveling of the small subunit head domain about two rRNA 'hinge' elements. Using iterative selection and molecular dynamics simulations, we derive alternate hinge elements capable of translocation in vitro and in vivo and describe their effects on the conformational trajectory of the EF-G-bound, translocating ribosome. In these alternate conformational pathways, we observe a diversity of swivel kinetics, hinge motions, three-dimensional head domain trajectories and tRNA dynamics. By finding alternate conformational pathways of translocation, we identify motions and intermediates that are essential or malleable in this process. These findings highlight the plasticity of protein synthesis and provide a more thorough understanding of the available sequence and conformational landscape of a central biological process.

MeSH terms

  • Computational Biology
  • Molecular Dynamics Simulation*
  • Nucleic Acid Conformation
  • Peptide Elongation Factor G / chemistry
  • Peptide Elongation Factor G / genetics
  • Peptide Elongation Factor G / metabolism
  • Protein Biosynthesis
  • RNA, Messenger / chemistry
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Transfer* / chemistry
  • RNA, Transfer* / genetics
  • RNA, Transfer* / metabolism
  • Ribosomes* / chemistry
  • Ribosomes* / metabolism

Substances

  • RNA, Transfer
  • RNA, Messenger
  • Peptide Elongation Factor G

Grants and funding

This work was supported by the Alfred P. Sloan Foundation grant G-2022-19420 (K.P.A.), Howard Hughes Medical Institute Hanna Gray fellowship grant GT11084 (J.L.A.), the Arkansas Biosciences Institute, the major research component of the Arkansas Tobacco Settlement Act of 2000 (D.G.); and the start-up fund of the University of Arkansas (D.G.). M.C.J. and J.A.W. gratefully acknowledge support from the Army Research Office [W911NF-16-1-0372] and Army Contracting Command [W52P1J-21-9-3023]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.