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Ornithine capture by a translating ribosome controls bacterial polyamine synthesis.

<div class='caption-title'>Mechanism of speF induction.</div>
<div class='caption-title'>Structural basis for the specific recognition of L-ornithine by the SpeFL-70S complex.</div>
<div class='caption-title'>Inhibition of peptide release by SpeFL.</div>
Herrero Del Valle A, Seip B, Cervera-Marzal I, Sacheau G, Seefeldt AC, Innis CA
OpenAccess logo Nat Microbiol 5 554-561 (2020)
Cited: 24 times
EuropePMC logo PMID: 32094585

Abstract

Polyamines are essential metabolites that play an important role in cell growth, stress adaptation and microbial virulence1-3. To survive and multiply within a human host, pathogenic bacteria adjust the expression and activity of polyamine biosynthetic enzymes in response to different environmental stresses and metabolic cues2. Here, we show that ornithine capture by the ribosome and the nascent peptide SpeFL controls polyamine synthesis in γ-proteobacteria by inducing the expression of the ornithine decarboxylase SpeF4, via a mechanism involving ribosome stalling and transcription antitermination. In addition, we present the cryogenic electron microscopy structure of an Escherichia coli ribosome stalled during translation of speFL in the presence of ornithine. The structure shows how the ribosome and the SpeFL sensor domain form a highly selective binding pocket that accommodates a single ornithine molecule but excludes near-cognate ligands. Ornithine pre-associates with the ribosome and is then held in place by the sensor domain, leading to the compaction of the SpeFL effector domain and blocking the action of release factor 1. Thus, our study not only reveals basic strategies by which nascent peptides assist the ribosome in detecting a specific metabolite, but also provides a framework for assessing how ornithine promotes virulence in several human pathogens.

Articles - 6tc3 mentioned but not cited (5)

  1. Ornithine capture by a translating ribosome controls bacterial polyamine synthesis. Herrero Del Valle A, Seip B, Cervera-Marzal I, Sacheau G, Seefeldt AC, Innis CA. Nat Microbiol 5 554-561 (2020)
  2. Structural basis for the context-specific action of the classic peptidyl transferase inhibitor chloramphenicol. Syroegin EA, Flemmich L, Klepacki D, Vazquez-Laslop N, Micura R, Polikanov YS. Nat Struct Mol Biol 29 152-161 (2022)
  3. Insights into the ribosome function from the structures of non-arrested ribosome-nascent chain complexes. Syroegin EA, Aleksandrova EV, Polikanov YS. Nat Chem 15 143-153 (2023)
  4. Regulation of the macrolide resistance ABC-F translation factor MsrD. Fostier CR, Ousalem F, Leroy EC, Ngo S, Soufari H, Innis CA, Hashem Y, Boël G. Nat Commun 14 3891 (2023)
  5. Functional domains of a ribosome arresting peptide are affected by surrounding nonconserved residues. Judd HNG, Martínez AK, Klepacki D, Vázquez-Laslop N, Sachs MS, Cruz-Vera LR. J Biol Chem 300 105780 (2024)


Reviews citing this publication (7)

  1. Escherichia coli Small Proteome. Hemm MR, Weaver J, Storz G. EcoSal Plus 9 (2020)
  2. Conserved Upstream Open Reading Frame Nascent Peptides That Control Translation. Dever TE, Ivanov IP, Sachs MS. Annu Rev Genet 54 237-264 (2020)
  3. ABC-F translation factors: from antibiotic resistance to immune response. Fostier CR, Monlezun L, Ousalem F, Singh S, Hunt JF, Boël G. FEBS Lett 595 675-706 (2021)
  4. Is Protein Folding a Thermodynamically Unfavorable, Active, Energy-Dependent Process? Sorokina I, Mushegian AR, Koonin EV. Int J Mol Sci 23 521 (2022)
  5. Gut microbiota bridges dietary nutrients and host immunity. Fan L, Xia Y, Wang Y, Han D, Liu Y, Li J, Fu J, Wang L, Gan Z, Liu B, Fu J, Zhu C, Wu Z, Zhao J, Han H, Wu H, He Y, Tang Y, Zhang Q, Wang Y, Zhang F, Zong X, Yin J, Zhou X, Yang X, Wang J, Yin Y, Ren W. Sci China Life Sci 66 2466-2514 (2023)
  6. Protein-Ligand Interactions in Scarcity: The Stringent Response from Bacteria to Metazoa, and the Unanswered Questions. Barik S. Int J Mol Sci 24 3999 (2023)
  7. Synthesis of Peptidyl-tRNA Mimics for Structural Biology Applications. Polikanov YS, Etheve-Quelquejeu M, Micura R. Acc Chem Res 56 2713-2725 (2023)

Articles citing this publication (12)

  1. Regulatory roles of Escherichia coli 5' UTR and ORF-internal RNAs detected by 3' end mapping. Adams PP, Baniulyte G, Esnault C, Chegireddy K, Singh N, Monge M, Dale RK, Storz G, Wade JT. Elife 10 e62438 (2021)
  2. Structural and mechanistic basis for translation inhibition by macrolide and ketolide antibiotics. Beckert B, Leroy EC, Sothiselvam S, Bock LV, Svetlov MS, Graf M, Arenz S, Abdelshahid M, Seip B, Grubmüller H, Mankin AS, Innis CA, Vázquez-Laslop N, Wilson DN. Nat Commun 12 4466 (2021)
  3. Human ribosomal G-quadruplexes regulate heme bioavailability. Mestre-Fos S, Ito C, Moore CM, Reddi AR, Williams LD. J Biol Chem 295 14855-14865 (2020)
  4. Structural basis for the tryptophan sensitivity of TnaC-mediated ribosome stalling. van der Stel AX, Gordon ER, Sengupta A, Martínez AK, Klepacki D, Perry TN, Herrero Del Valle A, Vázquez-Laslop N, Sachs MS, Cruz-Vera LR, Innis CA. Nat Commun 12 5340 (2021)
  5. Structural basis of l-tryptophan-dependent inhibition of release factor 2 by the TnaC arrest peptide. Su T, Kudva R, Becker T, Buschauer R, Komar T, Berninghausen O, von Heijne G, Cheng J, Beckmann R. Nucleic Acids Res 49 9539-9547 (2021)
  6. Polyamines and linear DNA mediate bacterial threat assessment of bacteriophage infection. de Mattos CD, Faith DR, Nemudryi AA, Schmidt AK, Bublitz DC, Hammond L, Kinnersley MA, Schwartzkopf CM, Robinson AJ, Joyce A, Michaels LA, Brzozowski RS, Coluccio A, Xing DD, Uchiyama J, Jennings LK, Eswara P, Wiedenheft B, Secor PR. Proc Natl Acad Sci U S A 120 e2216430120 (2023)
  7. Folding of VemP into translation-arresting secondary structure is driven by the ribosome exit tunnel. Kolář MH, Nagy G, Kunkel J, Vaiana SM, Bock LV, Grubmüller H. Nucleic Acids Res 50 2258-2269 (2022)
  8. Extensive diversity in RNA termination and regulation revealed by transcriptome mapping for the Lyme pathogen Borrelia burgdorferi. Petroni E, Esnault C, Tetreault D, Dale RK, Storz G, Adams PP. Nat Commun 14 3931 (2023)
  9. A nascent polypeptide sequence modulates DnaA translation elongation in response to nutrient availability. Felletti M, Romilly C, Wagner EGH, Jonas K. Elife 10 e71611 (2021)
  10. Practical Synthesis of N-Formylmethionylated Peptidyl-tRNA Mimics. Thaler J, Syroegin EA, Breuker K, Polikanov YS, Micura R. ACS Chem Biol 18 2233-2239 (2023)
  11. Rational design of a genome-based insulated system in Escherichia coli facilitates heterologous uricase expression for hyperuricemia treatment. He L, Tang W, Huang L, Zhou W, Huang S, Zou L, Yuan L, Men D, Chen S, Hu Y. Bioeng Transl Med 8 e10449 (2023)
  12. Maternal Supplementation with Ornithine Promotes Placental Angiogenesis and Improves Intestinal Development of Suckling Piglets. Yang Y, Hou G, Ji F, Zhou H, Lv R, Hu C. Animals (Basel) 14 689 (2024)


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