A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli

ABSTRACT Bacterial ribosomes are composed of three rRNA and over 50 ribosomal protein (r-protein) molecules. r-proteins are essential for ribosome assembly and structural stability and also participate in almost all ribosome functions. Ribosomal components are present in stoichiometric amounts in th...

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Main Authors: Kaspar Reier, Petri-Jaan Lahtvee, Aivar Liiv, Jaanus Remme
Format: Article
Language:English
Published: American Society for Microbiology 2022-10-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.01873-22
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author Kaspar Reier
Petri-Jaan Lahtvee
Aivar Liiv
Jaanus Remme
author_facet Kaspar Reier
Petri-Jaan Lahtvee
Aivar Liiv
Jaanus Remme
author_sort Kaspar Reier
collection DOAJ
description ABSTRACT Bacterial ribosomes are composed of three rRNA and over 50 ribosomal protein (r-protein) molecules. r-proteins are essential for ribosome assembly and structural stability and also participate in almost all ribosome functions. Ribosomal components are present in stoichiometric amounts in the mature 70S ribosomes during exponential and early stationary growth phases. Ribosomes are degraded in stationary phase; however, the stability and fate of r-proteins during stationary growth phase are not known. In this study, we report a quantitative analysis of ribosomal components during extended stationary-phase growth in Escherichia coli. We show that (i) the quantity of ribosomes per cell mass decreases in stationary phase, (ii) 70S ribosomes contain r-proteins in stoichiometric amounts, (iii) 30S subunits are degraded faster than 50S subunits, (iv) the quantities of 21 r-proteins in the total proteome decrease during 14 days (short-lived r-proteins) concomitantly with the reduction of cellular RNA, and (e) 30 r-proteins are stable and form a pool of free r-proteins (stable r-proteins). Thus, r-proteins are present in nonstoichiometric amounts in the proteome of E. coli during the extended stationary phase. IMPORTANCE Ribosome degradation has been extensively described from the viewpoint of its main component, rRNA. Here, we aim to complement our knowledge by quantitatively analyzing r-protein degradation and stability both in the ribosomes and in the whole-cell proteome during stationary phase in E. coli. r-proteins are considered to be very stable in the proteome. Here, we show that a specific set of r-proteins are rapidly degraded after release from the rRNA. The degradation of r-proteins is an intriguing new aspect of r-protein metabolism in bacteria.
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spelling doaj.art-10f05cbf4c28428faa79a4cf2eccb3562022-12-22T03:28:59ZengAmerican Society for MicrobiologymBio2150-75112022-10-0113510.1128/mbio.01873-22A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coliKaspar Reier0Petri-Jaan Lahtvee1Aivar Liiv2Jaanus Remme3Institute of Molecular and Cell Biology, University of Tartu, Tartu, EstoniaDepartment of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, EstoniaInstitute of Molecular and Cell Biology, University of Tartu, Tartu, EstoniaInstitute of Molecular and Cell Biology, University of Tartu, Tartu, EstoniaABSTRACT Bacterial ribosomes are composed of three rRNA and over 50 ribosomal protein (r-protein) molecules. r-proteins are essential for ribosome assembly and structural stability and also participate in almost all ribosome functions. Ribosomal components are present in stoichiometric amounts in the mature 70S ribosomes during exponential and early stationary growth phases. Ribosomes are degraded in stationary phase; however, the stability and fate of r-proteins during stationary growth phase are not known. In this study, we report a quantitative analysis of ribosomal components during extended stationary-phase growth in Escherichia coli. We show that (i) the quantity of ribosomes per cell mass decreases in stationary phase, (ii) 70S ribosomes contain r-proteins in stoichiometric amounts, (iii) 30S subunits are degraded faster than 50S subunits, (iv) the quantities of 21 r-proteins in the total proteome decrease during 14 days (short-lived r-proteins) concomitantly with the reduction of cellular RNA, and (e) 30 r-proteins are stable and form a pool of free r-proteins (stable r-proteins). Thus, r-proteins are present in nonstoichiometric amounts in the proteome of E. coli during the extended stationary phase. IMPORTANCE Ribosome degradation has been extensively described from the viewpoint of its main component, rRNA. Here, we aim to complement our knowledge by quantitatively analyzing r-protein degradation and stability both in the ribosomes and in the whole-cell proteome during stationary phase in E. coli. r-proteins are considered to be very stable in the proteome. Here, we show that a specific set of r-proteins are rapidly degraded after release from the rRNA. The degradation of r-proteins is an intriguing new aspect of r-protein metabolism in bacteria.https://journals.asm.org/doi/10.1128/mbio.01873-22proteomicsrRNAribosomal proteinsribosomesstationary phase
spellingShingle Kaspar Reier
Petri-Jaan Lahtvee
Aivar Liiv
Jaanus Remme
A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli
mBio
proteomics
rRNA
ribosomal proteins
ribosomes
stationary phase
title A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli
title_full A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli
title_fullStr A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli
title_full_unstemmed A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli
title_short A Conundrum of r-Protein Stability: Unbalanced Stoichiometry of r-Proteins during Stationary Phase in Escherichia coli
title_sort conundrum of r protein stability unbalanced stoichiometry of r proteins during stationary phase in escherichia coli
topic proteomics
rRNA
ribosomal proteins
ribosomes
stationary phase
url https://journals.asm.org/doi/10.1128/mbio.01873-22
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