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Bacterial ribosome heterogeneity: Changes in ribosomal protein composition during transition into stationary growth phase.

Lilleorg S, Reier K, Pulk A, Liiv A, Tammsalu T, Peil L, Cate JHD, Remme J
Biochimie 156 169-180 (2019)
Cited: 26 times
EuropePMC logo PMID: 30359641

Abstract

Ribosomes consist of many small proteins and few large RNA molecules. Both components are necessary for ribosome functioning during translation. According to widely accepted view, bacterial ribosomes contain always the same complement of ribosomal proteins. Comparative bacterial genomics data indicates that several ribosomal proteins are encoded by multiple paralogous genes suggesting structural heterogeneity of ribosomes. In E. coli, two r-proteins bL31 and bL36 are encoded by two genes: rpmE and ykgM encode bL31 protein paralogs bL31A and bL31B, and rpmJ and ykgO encode bL36 protein paralogs bL36A and bL36B respectively. We have found several similarities and differences between ribosomes of exponential and stationary growth phases by using quantitative mass spectrometry and X-ray crystallography. First, composition of ribosome associating proteins changes profoundly as cells transition from exponential to stationary growth phase. Ribosomal core proteins bL31A and bL36A are replaced by bL31B and bL36B, respectively. Second, our X-ray structure of the 70S ribosome demonstrates that bL31B and bL36B proteins have similar ribosome binding sites to their A counterparts. Third, ribosome subpopulations containing A or B paralogs existed simultaneously demonstrating that E. coli ribosomes are heterogeneous with respect to their paralogous ribosomal protein composition that changes via protein exchange.

Articles - 6i7v mentioned but not cited (1)

  1. Zur and zinc increase expression of E. coli ribosomal protein L31 through RNA-mediated repression of the repressor L31p. Rasmussen RA, Wang S, Camarillo JM, Sosnowski V, Cho BK, Goo YA, Lucks JB, O'Halloran TV. Nucleic Acids Res 50 12739-12753 (2022)


Reviews citing this publication (7)

  1. Does functional specialization of ribosomes really exist? Ferretti MB, Karbstein K. RNA 25 521-538 (2019)
  2. An Update on Mitochondrial Ribosome Biology: The Plant Mitoribosome in the Spotlight. Tomal A, Kwasniak-Owczarek M, Janska H. Cells 8 E1562 (2019)
  3. Structural Heterogeneities of the Ribosome: New Frontiers and Opportunities for Cryo-EM. Poitevin F, Kushner A, Li X, Dao Duc K. Molecules 25 E4262 (2020)
  4. Analyzing Ribosome Remodeling in Health and Disease. Petelski AA, Slavov N. Proteomics 20 e2000039 (2020)
  5. Specialised ribosomes as versatile regulators of gene expression. Joo M, Yeom JH, Choi Y, Jun H, Song W, Kim HL, Lee K, Shin E. RNA Biol 19 1103-1114 (2022)
  6. Coping with stress: How bacteria fine-tune protein synthesis and protein transport. Njenga R, Boele J, Öztürk Y, Koch HG. J Biol Chem 299 105163 (2023)
  7. The Discovery of Ribosomal Protein bL31 from Escherichia coli: A Long Story Revisited. Wada A, Ueta M, Wada C. Int J Mol Sci 24 3445 (2023)

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  1. One-carbon metabolism, folate, zinc and translation. Danchin A, Sekowska A, You C. Microb Biotechnol 13 899-925 (2020)
  2. Ribosome engineering reveals the importance of 5S rRNA autonomy for ribosome assembly. Huang S, Aleksashin NA, Loveland AB, Klepacki D, Reier K, Kefi A, Szal T, Remme J, Jaeger L, Vázquez-Laslop N, Korostelev AA, Mankin AS. Nat Commun 11 2900 (2020)
  3. Phenotypic effects of paralogous ribosomal proteins bL31A and bL31B in E. coli. Lilleorg S, Reier K, Volõnkin P, Remme J, Liiv A. Sci Rep 10 11682 (2020)
  4. Cryo-electron microscopy structure of the 70S ribosome from Enterococcus faecalis. Murphy EL, Singh KV, Avila B, Kleffmann T, Gregory ST, Murray BE, Krause KL, Khayat R, Jogl G. Sci Rep 10 16301 (2020)
  5. Reduced ATP-dependent proteolysis of functional proteins during nutrient limitation speeds the return of microbes to a growth state. Yeom J, Groisman EA. Sci Signal 14 eabc4235 (2021)
  6. Elucidation of a Novel Role of YebC in Surface Polysaccharides Regulation of Escherichia coli bipA-Deletion. Choi E, Jeon H, Oh C, Hwang J. Front Microbiol 11 597515 (2020)
  7. Autogenous regulation in vivo of the rpmE gene encoding ribosomal protein L31 (bL31), a key component of the protein-protein intersubunit bridge B1b. Aseev LV, Koledinskaya LS, Boni IV. RNA 26 814-826 (2020)
  8. Genetically engineered rpsL merodiploidy impacts secondary metabolism and antibiotic resistance in Streptomyces. Koshla O, Lopatniuk M, Borys O, Misaki Y, Kravets V, Ostash I, Shemediuk A, Ochi K, Luzhetskyy A, Fedorenko V, Ostash B. World J Microbiol Biotechnol 37 62 (2021)
  9. Isolation and characterization of a salt-tolerant denitrifying bacterium Alishewanella sp. F2 from seawall muddy water. Cheng R, Wang X, Zhu H, Yan B, Shutes B, Xu Y, Fu B, Wen H. Sci Rep 10 10002 (2020)
  10. Proteome Dynamics during Antibiotic Persistence and Resuscitation. Semanjski M, Gratani FL, Englert T, Nashier P, Beke V, Nalpas N, Germain E, George S, Wolz C, Gerdes K, Macek B. mSystems 6 e0054921 (2021)
  11. A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli. Reier K, Lahtvee PJ, Liiv A, Remme J. mBio 13 e0187322 (2022)
  12. Ribosome Protein Composition Mediates Translation during the Escherichia coli Stationary Phase. Reier K, Liiv A, Remme J. Int J Mol Sci 24 3128 (2023)
  13. Ribosomes lacking bS21 gain function to regulate protein synthesis in Flavobacterium johnsoniae. McNutt ZA, Roy B, Gemler BT, Shatoff EA, Moon KM, Foster LJ, Bundschuh R, Fredrick K. Nucleic Acids Res 51 1927-1942 (2023)
  14. Differential Paralog-Specific Expression of Multiple Small Subunit Proteins Cause Variations in Rpl42/eL42 Incorporation in Ribosome in Fission Yeast. Li W, Zhang J, Cheng W, Li Y, Feng J, Qin J, He X. Cells 11 2381 (2022)
  15. E. coli Toxin YjjJ (HipH) Is a Ser/Thr Protein Kinase That Impacts Cell Division, Carbon Metabolism, and Ribosome Assembly. Gratani FL, Englert T, Nashier P, Sass P, Czech L, Neumann N, Doello S, Mann P, Blobelt R, Alberti S, Forchhammer K, Bange G, Höfer K, Macek B. mSystems 8 e0104322 (2023)
  16. Label-Free Quantitation of Ribosomal Proteins from Bacillus subtilis for Antibiotic Research. Schäkermann S, Dietze P, Bandow JE. Methods Mol Biol 2601 363-378 (2023)
  17. Reconsidering Dogmas about the Growth of Bacterial Populations. Ughy B, Nagyapati S, Lajko DB, Letoha T, Prohaszka A, Deeb D, Der A, Pettko-Szandtner A, Szilak L. Cells 12 1430 (2023)
  18. Riboproteome remodeling during quiescence exit in Saccharomyces cerevisiae. Solari CA, Ortolá Martínez MC, Fernandez JM, Bates C, Cueto G, Valacco MP, Morales-Polanco F, Moreno S, Rossi S, Ashe MP, Portela P. iScience 27 108727 (2024)


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