Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population

Abstract Ribosomes are responsible for the synthesis of proteins, the major component of cellular biomass. Classical experiments have established a linear relationship between the fraction of resources invested in ribosomal proteins and the rate of balanced growth of a microbial population. Very lit...

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Main Authors: Antrea Pavlou, Eugenio Cinquemani, Corinne Pinel, Nils Giordano, Van Melle-Gateau Mathilde, Irina Mihalcescu, Johannes Geiselmann, Hidde de Jong
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55394-5
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author Antrea Pavlou
Eugenio Cinquemani
Corinne Pinel
Nils Giordano
Van Melle-Gateau Mathilde
Irina Mihalcescu
Johannes Geiselmann
Hidde de Jong
author_facet Antrea Pavlou
Eugenio Cinquemani
Corinne Pinel
Nils Giordano
Van Melle-Gateau Mathilde
Irina Mihalcescu
Johannes Geiselmann
Hidde de Jong
author_sort Antrea Pavlou
collection DOAJ
description Abstract Ribosomes are responsible for the synthesis of proteins, the major component of cellular biomass. Classical experiments have established a linear relationship between the fraction of resources invested in ribosomal proteins and the rate of balanced growth of a microbial population. Very little is known, however, about how the investment in ribosomes varies over individual cells in a population. We therefore extended the study of ribosomal resource allocation from populations to single cells, using a combination of time-lapse fluorescence microscopy and statistical inference. We found a large variability of ribosome concentrations and growth rates in conditions of balanced growth of the model bacterium Escherichia coli in a given medium, which cannot be accounted for by the population-level growth law. A large variability in the allocation of resources to ribosomes was also found during the transition of the bacteria from a poor to a rich growth medium. While some cells immediately adapt their ribosome synthesis rate to the new environment, others do so only gradually. Our results thus reveal a range of strategies for investing resources in the molecular machines at the heart of cellular self-replication. This raises the fundamental question whether the observed variability is an intrinsic consequence of the stochastic nature of the underlying biochemical processes or whether it improves the fitness of Escherichia coli in its natural environment.
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spelling doaj-art-bdc64d4654784be693106f9f0d4fd6f22025-01-05T12:37:04ZengNature PortfolioNature Communications2041-17232025-01-0116111610.1038/s41467-024-55394-5Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial populationAntrea Pavlou0Eugenio Cinquemani1Corinne Pinel2Nils Giordano3Van Melle-Gateau Mathilde4Irina Mihalcescu5Johannes Geiselmann6Hidde de Jong7Univ. Grenoble Alpes, InriaUniv. Grenoble Alpes, InriaUniv. Grenoble Alpes, InriaNantes Université, INSERM, CNRS, Université d’Angers, CRCI2NAUniv. Grenoble Alpes, CNRS, LIPhyUniv. Grenoble Alpes, CNRS, LIPhyUniv. Grenoble Alpes, InriaUniv. Grenoble Alpes, InriaAbstract Ribosomes are responsible for the synthesis of proteins, the major component of cellular biomass. Classical experiments have established a linear relationship between the fraction of resources invested in ribosomal proteins and the rate of balanced growth of a microbial population. Very little is known, however, about how the investment in ribosomes varies over individual cells in a population. We therefore extended the study of ribosomal resource allocation from populations to single cells, using a combination of time-lapse fluorescence microscopy and statistical inference. We found a large variability of ribosome concentrations and growth rates in conditions of balanced growth of the model bacterium Escherichia coli in a given medium, which cannot be accounted for by the population-level growth law. A large variability in the allocation of resources to ribosomes was also found during the transition of the bacteria from a poor to a rich growth medium. While some cells immediately adapt their ribosome synthesis rate to the new environment, others do so only gradually. Our results thus reveal a range of strategies for investing resources in the molecular machines at the heart of cellular self-replication. This raises the fundamental question whether the observed variability is an intrinsic consequence of the stochastic nature of the underlying biochemical processes or whether it improves the fitness of Escherichia coli in its natural environment.https://doi.org/10.1038/s41467-024-55394-5
spellingShingle Antrea Pavlou
Eugenio Cinquemani
Corinne Pinel
Nils Giordano
Van Melle-Gateau Mathilde
Irina Mihalcescu
Johannes Geiselmann
Hidde de Jong
Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population
Nature Communications
title Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population
title_full Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population
title_fullStr Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population
title_full_unstemmed Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population
title_short Single-cell data reveal heterogeneity of investment in ribosomes across a bacterial population
title_sort single cell data reveal heterogeneity of investment in ribosomes across a bacterial population
url https://doi.org/10.1038/s41467-024-55394-5
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