Role of Ribosome Degradation in the Death of Starved Escherichia Coli Cells

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1986 May 1

PMID 2422153

Citations 65

Authors

B D Davis

S M Luger

P C Tai

Affiliations

Soon will be listed here.

Abstract

In Escherichia coli cultures limited for phosphate, the number of ribosomal particles was reduced to a small percentage of its earlier peak value by the time the viable cell count began to drop; the 30S subunits decreased more than the 50S subunits. Moreover, the ribosomal activity was reduced even more: these cells no longer synthesized protein, and their extracts could not translate phage RNA unless ribosomes were added. The translation initiation factors also disappeared, suggesting that they become less stable when released from their normal attachment to 30S subunits. In contrast, elongation factors, aminoacyl-tRNA synthetases, and tRNA persisted. During further incubation, until viability was reduced to 10(-5), the ribosomal particles disappeared altogether, while tRNA continued to be preserved. These results suggest that an excessive loss of ribosomes (and of initiation factors) may be a major cause of cell death during prolonged phosphate starvation.

Citing Articles

RudS: bacterial desulfidase responsible for tRNA 4-thiouridine de-modification.

Jamontas R, Laurynenas A, Povilaityte D, Meskys R, Aucynaite A Nucleic Acids Res. 2024; 52(17):10543-10562.

PMID: 39166491 PMC: 11417400. DOI: 10.1093/nar/gkae716.

Rippling life on a dormant planet: hibernation of ribosomes, RNA polymerases, and other essential enzymes.

Helena-Bueno K, Chan L, Melnikov S Front Microbiol. 2024; 15:1386179.

PMID: 38770025 PMC: 11102965. DOI: 10.3389/fmicb.2024.1386179.

ResR/McdR-regulated protein translation machinery contributes to drug resilience in Mycobacterium tuberculosis.

Pal P, Khan M, Sharma S, Kumar Y, Mangla N, Kaushal P Commun Biol. 2023; 6(1):708.

PMID: 37433855 PMC: 10336103. DOI: 10.1038/s42003-023-05059-8.

protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation.

Espinosa R, Sorensen M, Svenningsen S Front Microbiol. 2023; 13:989818.

PMID: 36620012 PMC: 9814008. DOI: 10.3389/fmicb.2022.989818.

tRNAs Are Stable After All: Pitfalls in Quantification of tRNA from Starved Escherichia coli Cultures Exposed by Validation of RNA Purification Methods.

Prossliner T, Agrawal S, Heidemann D, Sorensen M, Svenningsen S mBio. 2023; 14(1):e0280522.

PMID: 36598190 PMC: 9973347. DOI: 10.1128/mbio.02805-22.

References

Maruyama H, Mizuno D . The participation of ribonuclease in the degradation of Escherichia coli ribosomal ribonucleic acid as revealed by oligonucleotides accumulation in the phorphorus-deficient stage. Biochim Biophys Acta. 1965; 108(4):593-604. DOI: 10.1016/0005-2787(65)90056-0. View

DAWES E, Ribbons D . STUDIES ON THE ENDOGENOUS METABOLISM OF ESCHERICHIA COLI. Biochem J. 1965; 95:332-43. PMC: 1214327. DOI: 10.1042/bj0950332. View

Schlessinger D . Synthesis and breakdown of ribonucleic acid in Escherichia coli starving for nitrogen. Biochim Biophys Acta. 1966; 119(1):183-91. DOI: 10.1016/0005-2787(66)90049-9. View

Maruyama H, Mizuno D . Ribosome degradation and the degradation products in starved Escherichia coli. I. Comparison of the degradation rate and of the nucleotide pool between Escherichia coli B and Q-13 strains in phosphate deficiency. Biochim Biophys Acta. 1970; 199(1):159-65. View

Tai P, Ingraham J . A ribosome-like particle accumulated at low temperature by a cold-sensitive mutant of Salmonella typhimurium. Biochim Biophys Acta. 1971; 232(1):151-66. DOI: 10.1016/0005-2787(71)90499-0. View

Nauman R, Silverman D, Voelz H . Ribosomal helices: formation in Escherichia coli during acidic growth. J Bacteriol. 1971; 107(1):358-60. PMC: 246922. DOI: 10.1128/jb.107.1.358-360.1971. View

Nath K, Koch A . Protein degradation in Escherichia coli. II. Strain differences in the degradation of protein and nucleic acid resulting from starvation. J Biol Chem. 1971; 246(22):6956-67. View

Maruyama H, Okamura S . Ribosome degradation and the degradation products in starved Escherichia coli. V. Ribonucleoprotein particles from glucose-starved cells. J Bacteriol. 1972; 110(1):442-6. PMC: 247426. DOI: 10.1128/jb.110.1.442-446.1972. View

Tai P, Wallace B, Herzog E, Davis B . Properties of initiation-free polysomes of Escherichia coli. Biochemistry. 1973; 12(4):609-15. DOI: 10.1021/bi00728a007. View

10.

Okamura S, Maruyama H, Yanagita T . Ribosome degradation and degradation products in starved Escherichia coli. VI. Prolonged culture during glucose starvation. J Biochem. 1973; 73(5):915-22. DOI: 10.1093/oxfordjournals.jbchem.a130174. View

11.

MONTAGUE M, DAWES E . The survival of Peptococcus prévotii in relation to the adenylate energy charge. J Gen Microbiol. 1974; 80(1):291-9. DOI: 10.1099/00221287-80-1-291. View

12.

Kaplan R, Apirion D . The fate of ribosomes in Escherichia coli cells starved for a carbon source. J Biol Chem. 1975; 250(5):1854-63. View

13.

Kaplan R, Apirion D . Decay of ribosomal ribonucleic acid in Escherichia coli cells starved for various nutrients. J Biol Chem. 1975; 250(8):3174-8. View

14.

Dennis P . Synthesis and stability of individual ribosomal proteins in the presence of rifampicin. Mol Gen Genet. 1974; 134(1):39-47. DOI: 10.1007/BF00332811. View

15.

Furano A . Content of elongation factor Tu in Escherichia coli. Proc Natl Acad Sci U S A. 1975; 72(12):4780-4. PMC: 388815. DOI: 10.1073/pnas.72.12.4780. View

16.

Aharonowitz Y, Ron E . Translocation in Bacillus subtilis: irreversible inactivation of elongation factor G and viability of a temperature- sensitive mutant. J Bacteriol. 1976; 125(3):1229-31. PMC: 236208. DOI: 10.1128/jb.125.3.1229-1231.1976. View

17.

Tal M, Silberstein A, Moyner K . In vivo reassembly of 30-S ribosomal subunits following their specific destruction by thermal shock. Biochim Biophys Acta. 1977; 479(4):479-96. DOI: 10.1016/0005-2787(77)90041-7. View

18.

Fallon A, Jinks C, Yamamoto M, Nomura M . Expression of ribosomal protein genes cloned in a hybrid plasmid in Escherichia coli: gene dosage effects on synthesis of ribosomal proteins and ribosomal protein messenger ribonucleic acid. J Bacteriol. 1979; 138(2):383-96. PMC: 218189. DOI: 10.1128/jb.138.2.383-396.1979. View

19.

St John A, GOLDBERG A . Effects of starvation for potassium and other inorganic ions on protein degradation and ribonucleic acid synthesis in Escherichia coli. J Bacteriol. 1980; 143(3):1223-33. PMC: 294483. DOI: 10.1128/jb.143.3.1223-1233.1980. View

20.

Geyl D, Bock A, Isono K . An improved method for two-dimensional gel-electrophoresis: analysis of mutationally altered ribosomal proteins of Escherichia coli. Mol Gen Genet. 1981; 181(3):309-12. DOI: 10.1007/BF00425603. View