Skip to main content
Science Progress logoLink to Science Progress
. 2019 Feb 27;87(3):137–152. doi: 10.3184/003685004783238517

Ribosome Inactivation for Preservation: Concepts and Reservations

Walid M El-Sharoud 1
PMCID: PMC10361172  PMID: 15884656

Abstract

The role of the bacterial ribosome in the cellular response to environmental stress has been widely considered over last decade. Certain ribosome-associated proteins have been shown to induce conformational changes that lead to the formation of inactive forms of ribosomes that are presumed to be more stable during stationary phase. This was found to aid the survival of bacteria in this phase. Such proteins include ribosome modulation factor (RMF), YfiA and YhbH. Examining the influence of RMF on the survival of E. coli under heat, acid and osmotic stress showed that it was important for bacterial viability under these environmental pressures. However, the mechanism by which this protein exerts its effect has not been fully elucidated. The present work reviews the involvement of ribosomes in determining cell behaviour during stress. It focuses on the action of the ribosome-associated proteins and their role in inactivating ribosomes for preserving their integrity and aiding cell survival under stress.

Keywords: bacterial ribosome, cellular response to environmental stress, RMF, YfiA, YhbH

Full Text

The Full Text of this article is available as a PDF (160.4 KB).

References

  • 1.Hsu D., Shih L-M., and Zee Y.C. (1994) Degradation of rRNA in Salmonella strains: a novel mechanism to regulate the concentrations of rRNA and ribosomes. J. Bacteriol., 176, 4761–4765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Wada A. (1998) Growth phase coupled modulation of Escherichia coli ribosomes. Genes Cells, 3, 203–208. [DOI] [PubMed] [Google Scholar]
  • 3.Strange R.E., and Shon M. (1964) Effects of thermal stress on viability and ribonucleic acid of Aerobacter aerogenes in aqueous suspension. J. Gen. Microbiol., 34, 99–114. [DOI] [PubMed] [Google Scholar]
  • 4.Strange R.E. (1964) Effect of magnesium on permeability control in chilled bacteria. Nature, 203, 1304–1305. [DOI] [PubMed] [Google Scholar]
  • 5.Rybkin A.I., and Ravin V.K. (1987) Decreased synthetic activity as a possible cause of the death of Escherichia coli bacteria during amino acid starvation. Mikrobiologiiia, 56, 227–231. [PubMed] [Google Scholar]
  • 6.Tolker-Nielsen T., and Molin S. (1996) Role of ribosome degradation in the death of heat-stressed Salmonella typhimurium. FEMS Microbiol.Lett., 142, 155–160. [DOI] [PubMed] [Google Scholar]
  • 7.Stephens P.J., and Jones M.V. (1993) Reduced ribosomal thermal denaturation in Listeria monocytogenes following osmotic and heat shocks. FEMS Microbiol. Lett., 106, 177–182. [DOI] [PubMed] [Google Scholar]
  • 8.Bayles D.O., Tunick M.H., Foglia T.A., and Miller A.J. (2000) Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl. Environ. Microbiol., 66, 4351–4355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Niven G.W., Miles C.A., and Mackey B.M. (1999) The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: an in vivo study using differential scanning calorimetry. Microbiology, 145, 419–425. [DOI] [PubMed] [Google Scholar]
  • 10.VanBogelen R.A., and Neidhardt F.C. (1990) Ribosomes as sensor of heat and cold shock in Escherichia coli. Proc.e Natl Acad. Sci. USA, 87, 5589–5593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Abee T., and Wouters J.A. (1999). Microbial stress response in minimal processing. Int. J. Food Microbio., 15, 65–91. [DOI] [PubMed] [Google Scholar]
  • 12.Zhang S., Scott J.M., and Haldenwang W.G. (2001) Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor sigma (B). J. Bacteriol., 183, 2316–2321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Ohara N., Naito M., Miyazaki C., Matsumoto S., Tabira Y., and Yamada T. (1997) HrpA, a new ribosome-associated protein which appears in heat-stressed Mycobacterium bovis Bacillus Calmette-Guerin. J. Bacteriol., 179, 6495–6498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Korber P., Stahl J., Nierhaus K., and Bardwell C. (2000) Hsp15: a ribosome-associated heat shock protein. EMBO J., 19, 741–748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Teixeira-Gomez A.P., Cloeckaert A., and Zygmunt M.S. (2000) Characterization of heat, oxidative, and acid stress responses in Brucella melitensis. Infect. Immun., 68, 2954–2961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Janosi L., Shimuzi I., and Kaji A. (1994) Ribosome recycling factor (ribosome releasing factor) is essential for bacterial growth. Proc. Natl Acad. Sci. USA, 91, 4249–4253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.El-Sharoud W.M. (2002) Locating a stress sensor. Microbiologist, 3, 34–35. [Google Scholar]
  • 18.Huisman G.W., Siegele D.A., Zambrano M.M., and Kolter R. (1996). Morphological and physiological changes during stationary phase. In: Escherichia coli and Salmonella, cellular and molecular biology, pp. 1672–11682. ASM Press, Washington, D.C. [Google Scholar]
  • 19.Hsu D., Zee Y.C., Ingraham J., and Shih L.M. (1992) Diversity of cleavage patterns of Salmonella 23S rRNA. J. Gen. Microbiol., 138, 199–203. [DOI] [PubMed] [Google Scholar]
  • 20.Kaplan R., and Apirion D. (1975) The fate of ribosomes in Escherichia coli cells starved for a carbon source. J. Biol. Chem., 250, 1854–1863. [PubMed] [Google Scholar]
  • 21.Subramanian V.R., Haase C., and Giesen M. (1976) Isolation and character-ization of a growth-cycle-reflecting, high-molecular-weight protein associated with Escherichia coli ribosomes. Eur. J. Bioche., 67, 591–601. [DOI] [PubMed] [Google Scholar]
  • 22.Wada A. (1986) Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. 1. Detection of four new proteins. J. Biochem., (Tokyo) 100, 1583–1594. [DOI] [PubMed] [Google Scholar]
  • 23.Wada A. (1986) Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. 2. Characterization of four new proteins. J. Biochem. (Tokyo), 100, 1595–1605. [DOI] [PubMed] [Google Scholar]
  • 24.Tissieres A., and Watson J.D. (1958) Ribonucleoprotein particles from Escherichia coli. Nature, 182, 778–780. [DOI] [PubMed] [Google Scholar]
  • 25.McCarthy B.J. (1960) Variations in bacterial ribosomes. Biochim. Biophys. Acta, 39, 563–564. [Google Scholar]
  • 26.Sabo B., and Spirin A.S. (1970) Dissociation of 70S monoribosomes of Escherichia coli in relation to ionic strength, pH, and termperature. Molec. Biol., 4, 628–631. [Google Scholar]
  • 27.Wada A., Yamazaki Y., Fujita N., and Ishihama A. (1990) Structure and probable genetic location of a “ribosome modulation factor” associated with 100S ribosomes in stationary- phase”Escherichia coli cells. Proc. Natl Acad. Sci. USA, 87, 2657–2661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Yamagishi M., Matsushima H., Wada A., Sakagami M., Fujita N., and Ishihama A. (1993) Regulation of Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase- and growth rate-dependent control. EMBO J., 12, 625–630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Wada A., Igarashi K., Yoshimura S., Aimoto S., and Ishihama A. (1995) Ribosome modulation factor: stationary growth-phase specific inhibitor of ribosome functions from Escherichia coli. Biochem. Biophys. Res. Commun., 14, 410–417. [DOI] [PubMed] [Google Scholar]
  • 30.Wada A., Mikkola R., Kurland C.G., and Ishihama (2000) Growth phase-coupled changes of the ribosome profile in natural isolates and laboratory strains of Escherichia coli. J. Bacteriol., 182, 2893–2899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Yoshida H., Yamamoto H., Uchiumi T., and Wada A. (2004) RMF inactivates ribosomes by covering the peptidyl transferase centre and entrance of peptide exit tunnel. Genes to cells, 9, 271–278. [DOI] [PubMed] [Google Scholar]
  • 32.Maki Y., Yoshida H., and Wada A. (2000). Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary Escherichia coli. Genes to cells 5, 965–974. [DOI] [PubMed] [Google Scholar]
  • 33.Ishihama A. (1999) Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes to Cells, 4, 135–143. [DOI] [PubMed] [Google Scholar]
  • 34.El-Sharoud W.M. (2004) Effect of ribosome modulation factor on the behaviour of Escherichia coli under acid stress and in milk fermentation systems. PhD thesis (The University of Reading, UK: ) [Google Scholar]
  • 35.Agafonov D.E., Kolb V.A., Nazimov I.V., and Spirin A.S. (1999) A protein residing at the subunit interface of the bacterial ribosome. Proc. Natl Acad. Sci. USA, 96, 12345–12349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Agafonov D.E., Kolb V.A., and Spirin A.S. (2001) Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. Eur. Molec. Biol. Org. Rep., 2, 399–402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Garay-Arroyo A., Colmenero-Flores J.M., Garciarrubio A., and Covarrubias A.A. (2000) Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J. Biol. Chem., 25, 5668–5674. [DOI] [PubMed] [Google Scholar]
  • 38.Niven G.W. (2004) Ribosome modulation factor protects Escherichia coli during heat stress, but this may not be dependent on ribosome dimerisation. Arch.Microbiol., 162, 60–66. [DOI] [PubMed] [Google Scholar]
  • 39.Nissen P., Hansen J., Ban N., Moore P.B., and Steitz T.A. (2000) The structural basis of ribosome activity in peptide bond synthesis. Science, 289, 920–930. [DOI] [PubMed] [Google Scholar]
  • 40.Izutsu K., Wada C., and Wada A. (2001). Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp. Genes to Cells 6, 665–676. [DOI] [PubMed] [Google Scholar]
  • 41.Apirakaramwong A., Kashiwagi K., Raj V.S., Sakata K., Kakinuma Y., Ishihama A., and Igarashi K. (1999) Involvement of ppGpp, ribosome modulation factor, and stationary phase-specific sigma factor in the decrease in cell viability caused by spermidine. Biochem. Biophys., Res. Commun., 264, 643–647. [DOI] [PubMed] [Google Scholar]
  • 42.Mackey B.M., Miles C.A., Parsons S.E., and Seymour D.A. (1991). Thermal denaturation of whole cells and cell components of Escherichia coli examined by differential scanning calorimetry. J. Gen. Microbiol., 137, 2361–2374. [DOI] [PubMed] [Google Scholar]

Articles from Science Progress are provided here courtesy of SAGE Publications

RESOURCES