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Peer-reviewedCC BY-NC-NDProceedings of the National Academy of Sciences

Structural basis of long-range transcription–translation coupling

  • Chengyuan Wang1,2
  • Vadim Molodtsov3,4,2
  • Shashank Shandilya2
  • Linlin You2
  • Jing Zhang1
  • Konstantin Kuznedelov2
  • Bryce E. Nickels5
  • Jason T. Kaelber6
  • Gregor Blaha7
  • Richard H. Ebright2
7 affiliations
  1. 1Shanghai Institute of Materia Medica, Chinese Academy of Sciences,
  2. 2Waksman Institute and Department of Chemistry and Chemical Biology, Rutgers University
  3. 3Research Institute of Molecular and Cellular Medicine, RUDN University
  4. 4Skolkovo Institute of Science and Technology
  5. 5Waksman Institute and Department of Genetics, Rutgers University
  6. 6Rutgers CryoEM and Nanoimaging Facility and Institute for Quantitative Biomedicine, Rutgers University
  7. 7Department of Biochemistry, University of California
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Abstract

. In these molecular assemblies, termed "coupled transcription-translation complexes" or "TTC-B," RNA polymerase (RNAP) directly interacts with the ribosome, the transcription elongation factor NusG or its paralog RfaH forms a bridge between RNAP and ribosome, and the transcription elongation factor NusA optionally forms a second bridge between RNAP and ribosome. Here, we report structures of coupled transcription-translation complexes having mRNA spacers between RNAP and ribosome longer than the maximum-length mRNA spacer compatible with formation of TTC-B. The results define a class of coupled transcription-translation complex, termed "TTC-LC," where "LC" denotes "long-range coupling." TTC-LC differs from TTC-B by a ~60° rotation and ~70 Å translation of RNAP relative to ribosome, resulting in loss of direct interactions between RNAP and ribosome and creation of a ~70 Å gap between RNAP and ribosome. TTC-LC accommodates long mRNA spacers by looping out mRNA from the gap between RNAP and ribosome. We present evidence that TTC-LC is a functional intermediate in assembling and disassembling TTC-B, mediating pre-TTC-B transcription-translation coupling before a ribosome catches up to RNAP, and mediating post-TTC-B transcription-translation coupling after a ribosome stops moving and RNAP continues moving. We show that TTC-B, but not TTC-LC, is severely defective in RNA-hairpin-dependent transcription termination, and that both TTC-B and TTC-LC are severely defective in Rho-dependent transcription termination.

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Cite

BibTeXRIS
BibTeX
@article{wang2026structural,
  title = {{Structural basis of long-range transcription–translation coupling}},
  author = {Chengyuan Wang and Vadim Molodtsov and Shashank Shandilya and Linlin You and Jing Zhang and Konstantin Kuznedelov and Bryce E. Nickels and Jason T. Kaelber and Gregor Blaha and Richard H. Ebright},
  journal = {Proceedings of the National Academy of Sciences},
  year = {2026},
  month = jun,
  doi = {10.1073/pnas.2528970123},
  url = {https://doi.org/10.1073/pnas.2528970123},
  note = {CC BY-NC-ND},
}
RIS
TY  - JOUR
TI  - Structural basis of long-range transcription–translation coupling
AU  - Chengyuan Wang
AU  - Vadim Molodtsov
AU  - Shashank Shandilya
AU  - Linlin You
AU  - Jing Zhang
AU  - Konstantin Kuznedelov
AU  - Bryce E. Nickels
AU  - Jason T. Kaelber
AU  - Gregor Blaha
AU  - Richard H. Ebright
PY  - 2026
DA  - 2026/06/10
JO  - Proceedings of the National Academy of Sciences
DO  - 10.1073/pnas.2528970123
UR  - https://doi.org/10.1073/pnas.2528970123
AB  - . In these molecular assemblies, termed "coupled transcription-translation complexes" or "TTC-B," RNA polymerase (RNAP) directly interacts with the ribosome, the transcription elongation factor NusG or its paralog RfaH forms a bridge between RNAP and ribosome, and the transcription elongation factor NusA optionally forms a second bridge between RNAP and ribosome. Here, we report structures of coupled transcription-translation complexes having mRNA spacers between RNAP and ribosome longer than the maximum-length mRNA spacer compatible with formation of TTC-B. The results define a class of coupled transcription-translation complex, termed "TTC-LC," where "LC" denotes "long-range coupling." TTC-LC differs from TTC-B by a ~60° rotation and ~70 Å translation of RNAP relative to ribosome, resulting in loss of direct interactions between RNAP and ribosome and creation of a ~70 Å gap between RNAP and ribosome. TTC-LC accommodates long mRNA spacers by looping out mRNA from the gap between RNAP and ribosome. We present evidence that TTC-LC is a functional intermediate in assembling and disassembling TTC-B, mediating pre-TTC-B transcription-translation coupling before a ribosome catches up to RNAP, and mediating post-TTC-B transcription-translation coupling after a ribosome stops moving and RNAP continues moving. We show that TTC-B, but not TTC-LC, is severely defective in RNA-hairpin-dependent transcription termination, and that both TTC-B and TTC-LC are severely defective in Rho-dependent transcription termination.
SN  - 0027-8424
SN  - 1091-6490
ER  -