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Growth rate-coordinated transcriptome reorganization in bacteria.

ABSTRACT: BACKGROUND: Cell growth rate reflects an organism's physiological state and largely relies on the ability of gene expression to respond to the environment. The relationship between cellular growth rate and gene expression remains unknown. RESULTS: Growth rate-coordinated changes in gene expression were discovered by analyzing exponentially growing Escherichia coli cells cultured under multiple defined environments, in which osmotic pressure, temperature and starvation status were varied. Gene expression analyses showed that all 3,740 genes in the genome could be simply divided into three clusters (C1, C2 and C3), which were accompanied by a generic trend in the growth rate that was coordinated with transcriptional changes. The direction of transcriptional change in C1 indicated environmental specificity, whereas those in C2 and C3 were correlated negatively and positively with growth rates, respectively. The three clusters exhibited differentiated gene functions and gene regulation task division. CONCLUSIONS: We identified three gene clusters, exhibiting differential gene functions and distinct directions in their correlations with growth rates. Reverses in the direction of the growth rate correlated transcriptional changes and the distinguished duties of the three clusters indicated how transcriptome homeostasis is maintained to balance the total expression cost for sustaining life in new habitats.

SUBMITTER: Matsumoto Y

PROVIDER: S-EPMC3840594 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Growth rate-coordinated transcriptome reorganization in bacteria.

Matsumoto Yuki Y Murakami Yoshie Y Tsuru Saburo S Ying Bei-Wen BW Yomo Tetsuya T

BMC genomics 20131120

<h4>Background</h4>Cell growth rate reflects an organism's physiological state and largely relies on the ability of gene expression to respond to the environment. The relationship between cellular growth rate and gene expression remains unknown.<h4>Results</h4>Growth rate-coordinated changes in gene expression were discovered by analyzing exponentially growing Escherichia coli cells cultured under multiple defined environments, in which osmotic pressure, temperature and starvation status were va ...[more]

PMID: 24252326

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Project description:The genomic, environmental, and evolutionary interruptions caused the changes in bacterial growth, which were stringently associated with changes in gene expression. The growth and gene expression changes remained unclear in response to these interruptions that occurred combinative. As a pilot study, whether and how bacterial growth was affected by the individual and dual interruptions of genome reduction, environmental stress, and adaptive evolution were investigated. Growth assay showed that the presence of the environmental stressors, i.e., threonine and chloramphenicol, significantly decreased the growth rate of the wild-type Escherichia coli, whereas not that of the reduced genome. It indicated a canceling effect in bacterial growth due to the dual interruption of the genomic and environmental changes. Experimental evolution of the reduced genome released the canceling effect by improving growth fitness. Intriguingly, the transcriptome architecture maintained a homeostatic chromosomal periodicity regardless of the genomic, environmental, and evolutionary interruptions. Negative epistasis in transcriptome reorganization was commonly observed in response to the dual interruptions, which might contribute to the canceling effect. It was supported by the changes in the numbers of differentially expressed genes (DEGs) and the enriched regulons and functions. Gene network analysis newly constructed 11 gene modules, one out of which was correlated to the growth rate. Enrichment of DEGs in these modules successfully categorized them into three types, i.e., conserved, responsive, and epistatic. Taken together, homeostasis in transcriptome architecture was essential to being alive, and it might be attributed to the negative epistasis in transcriptome reorganization and the functional differentiation in gene modules. The present study directly connected bacterial growth fitness with transcriptome reorganization and provided a global view of how microorganisms responded to genomic, environmental, and evolutionary interruptions for survival from wild nature.

Dataset Information

Growth rate-coordinated transcriptome reorganization in bacteria.

Publications

Growth rate-coordinated transcriptome reorganization in bacteria.

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