Structural basis of H-NS-mediated temperature-dependent stimulation of initial growth in Escherichia coli

Bacteria rapidly initiate growth when entering warm-blooded hosts to ensure reproductive success. We investigated the temperature-dependent stimulation of the specific growth rate at the onset of the logarithmic phase (defined as μ at ODratio = 0.2) in Escherichia coli. High-frequency automated monitoring revealed that this stimulation peaks near 37°C and is strain-specific. Comparative analysis between MG1655 and W3110 type A identified the Rac prophage as a primary genomic determinant for this acceleration. However, growth stimulation is uniquely dependent on H-NS, which we redefine as a nucleoid structural organizer. Genetic complementation and comparative analysis of nucleoid-associated proteins (NAPs), and single-cell nucleoid imaging confirmed that H-NS provides a mandatory physical scaffold specifically at host temperatures. We propose that H-NS undergoes a conformational switch to a parallel dimer form around 37°C, enabling the nucleoid to adopt the highly condensed state required for managing replication-transcription conflicts during rapid growth bursts. Notably, while MG1655 relies primarily on H-NS for this stimulation, W3110 type A requires a distributed network of NAPs, including HU and StpA, to maintain its growth velocity. This effect is environment-specific, becoming particularly significant under minimal media conditions where metabolic and structural coordination requirements are more stringent, but less pronounced in nutrient-rich conditions. These findings resolve the silencing paradox: hns-deficient mutants grow slowly at 37°C because they lack the structural infrastructure required to physically coordinate the rapid onset of growth, regardless of the de-repression of growth-promoting genes. We conclude that H-NS-mediated physical organization of the genome is a fundamental prerequisite for temperature-dependent growth adaptation and successful host colonization.

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Publication Details

Journal
PLoS ONE
Published
2026-10-28
DOI
https://doi.org/10.1371/journal.pone.0346655
Primary Topic
Bacterial Genetics and Biotechnology
Type
article
Field-Weighted Citation Impact
0.00

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article

Structural basis of H-NS-mediated temperature-dependent stimulation of initial growth in Escherichia coli

Yukari Miyake, Kaneyoshi Yamamoto, Erika Yamauchi, Hayato Fujita
PLoS ONE
Bacterial Genetics and Biotechnology
article

Structural basis of H-NS-mediated temperature-dependent stimulation of initial growth in Escherichia coli

Yukari Miyake, Kaneyoshi Yamamoto, Erika Yamauchi, Hayato Fujita
article en

Abstract

Bacteria rapidly initiate growth when entering warm-blooded hosts to ensure reproductive success. We investigated the temperature-dependent stimulation of the specific growth rate at the onset of the logarithmic phase (defined as μ at ODratio = 0.2) in Escherichia coli. High-frequency automated monitoring revealed that this stimulation peaks near 37°C and is strain-specific. Comparative analysis between MG1655 and W3110 type A identified the Rac prophage as a primary genomic determinant for this acceleration. However, growth stimulation is uniquely dependent on H-NS, which we redefine as a nucleoid structural organizer. Genetic complementation and comparative analysis of nucleoid-associated proteins (NAPs), and single-cell nucleoid imaging confirmed that H-NS provides a mandatory physical scaffold specifically at host temperatures. We propose that H-NS undergoes a conformational switch to a parallel dimer form around 37°C, enabling the nucleoid to adopt the highly condensed state required for managing replication-transcription conflicts during rapid growth bursts. Notably, while MG1655 relies primarily on H-NS for this stimulation, W3110 type A requires a distributed network of NAPs, including HU and StpA, to maintain its growth velocity. This effect is environment-specific, becoming particularly significant under minimal media conditions where metabolic and structural coordination requirements are more stringent, but less pronounced in nutrient-rich conditions. These findings resolve the silencing paradox: hns-deficient mutants grow slowly at 37°C because they lack the structural infrastructure required to physically coordinate the rapid onset of growth, regardless of the de-repression of growth-promoting genes. We conclude that H-NS-mediated physical organization of the genome is a fundamental prerequisite for temperature-dependent growth adaptation and successful host colonization.

PLoS ONEVol. 21(10)
Hosei University (JP)
Takahashi Industrial and Economic Research Foundation, Ministry of Education, Culture, Sports, Science and Technology, JKA Foundation
Openalex Percentile: Top 15%
Bacterial Genetics and Biotechnology
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