Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations

ABSTRACT Bacillus subtilis and Escherichia coli are evolutionarily divergent model organisms whose analysis has enabled elucidation of fundamental differences between Gram-positive and Gram-negative bacteria, respectively. Despite their differences in cell cycle control at the molecular level, the t...

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Autores principales: John T. Sauls, Sarah E. Cox, Quynh Do, Victoria Castillo, Zulfar Ghulam-Jelani, Suckjoon Jun
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:017149128f8447b3b69ea09929c355a82021-11-15T15:54:45ZControl of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations10.1128/mBio.02205-192150-7511https://doaj.org/article/017149128f8447b3b69ea09929c355a82019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02205-19https://doaj.org/toc/2150-7511ABSTRACT Bacillus subtilis and Escherichia coli are evolutionarily divergent model organisms whose analysis has enabled elucidation of fundamental differences between Gram-positive and Gram-negative bacteria, respectively. Despite their differences in cell cycle control at the molecular level, the two organisms follow the same phenomenological principle, known as the adder principle, for cell size homeostasis. We thus asked to what extent B. subtilis and E. coli share common physiological principles in coordinating growth and the cell cycle. We measured physiological parameters of B. subtilis under various steady-state growth conditions with and without translation inhibition at both the population and single-cell levels. These experiments revealed core physiological principles shared between B. subtilis and E. coli. Specifically, both organisms maintain an invariant cell size per replication origin at initiation, under all steady-state conditions, and even during nutrient shifts at the single-cell level. Furthermore, the two organisms also inherit the same “hierarchy” of physiological parameters. On the basis of these findings, we suggest that the basic principles of coordination between growth and the cell cycle in bacteria may have been established early in evolutionary history. IMPORTANCE High-throughput, quantitative approaches have enabled the discovery of fundamental principles describing bacterial physiology. These principles provide a foundation for predicting the behavior of biological systems, a widely held aspiration. However, these approaches are often exclusively applied to the best-known model organism, E. coli. In this report, we investigate to what extent quantitative principles discovered in Gram-negative E. coli are applicable to Gram-positive B. subtilis. We found that these two extremely divergent bacterial species employ deeply similar strategies in order to coordinate growth, cell size, and the cell cycle. These similarities mean that the quantitative physiological principles described here can likely provide a beachhead for others who wish to understand additional, less-studied prokaryotes.John T. SaulsSarah E. CoxQuynh DoVictoria CastilloZulfar Ghulam-JelaniSuckjoon JunAmerican Society for Microbiologyarticlecell cyclecell sizereplication initiationsingle cellMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution DOAJ
collection DOAJ
language EN
topic cell cycle
cell size
replication initiation
single cell
Microbiology
QR1-502
spellingShingle cell cycle
cell size
replication initiation
single cell
Microbiology
QR1-502
John T. Sauls
Sarah E. Cox
Quynh Do
Victoria Castillo
Zulfar Ghulam-Jelani
Suckjoon Jun
Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations
description ABSTRACT Bacillus subtilis and Escherichia coli are evolutionarily divergent model organisms whose analysis has enabled elucidation of fundamental differences between Gram-positive and Gram-negative bacteria, respectively. Despite their differences in cell cycle control at the molecular level, the two organisms follow the same phenomenological principle, known as the adder principle, for cell size homeostasis. We thus asked to what extent B. subtilis and E. coli share common physiological principles in coordinating growth and the cell cycle. We measured physiological parameters of B. subtilis under various steady-state growth conditions with and without translation inhibition at both the population and single-cell levels. These experiments revealed core physiological principles shared between B. subtilis and E. coli. Specifically, both organisms maintain an invariant cell size per replication origin at initiation, under all steady-state conditions, and even during nutrient shifts at the single-cell level. Furthermore, the two organisms also inherit the same “hierarchy” of physiological parameters. On the basis of these findings, we suggest that the basic principles of coordination between growth and the cell cycle in bacteria may have been established early in evolutionary history. IMPORTANCE High-throughput, quantitative approaches have enabled the discovery of fundamental principles describing bacterial physiology. These principles provide a foundation for predicting the behavior of biological systems, a widely held aspiration. However, these approaches are often exclusively applied to the best-known model organism, E. coli. In this report, we investigate to what extent quantitative principles discovered in Gram-negative E. coli are applicable to Gram-positive B. subtilis. We found that these two extremely divergent bacterial species employ deeply similar strategies in order to coordinate growth, cell size, and the cell cycle. These similarities mean that the quantitative physiological principles described here can likely provide a beachhead for others who wish to understand additional, less-studied prokaryotes.
format article
author John T. Sauls
Sarah E. Cox
Quynh Do
Victoria Castillo
Zulfar Ghulam-Jelani
Suckjoon Jun
author_facet John T. Sauls
Sarah E. Cox
Quynh Do
Victoria Castillo
Zulfar Ghulam-Jelani
Suckjoon Jun
author_sort John T. Sauls
title Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations
title_short Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations
title_full Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations
title_fullStr Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations
title_full_unstemmed Control of <named-content content-type="genus-species">Bacillus subtilis</named-content> Replication Initiation during Physiological Transitions and Perturbations
title_sort control of <named-content content-type="genus-species">bacillus subtilis</named-content> replication initiation during physiological transitions and perturbations
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/017149128f8447b3b69ea09929c355a8
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