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Rapid Accumulation of Motility-Activating Mutations in Resting Liquid Culture of Escherichia coli.

ABSTRACT: Expression of motility genes is a potentially beneficial but costly process in bacteria. Interestingly, many isolate strains of Escherichia coli possess motility genes but have lost the ability to activate them under conditions in which motility is advantageous, raising the question of how they respond to these situations. Through transcriptome profiling of strains in the E. coli single-gene knockout Keio collection, we noticed drastic upregulation of motility genes in many of the deletion strains compared to levels in their weakly motile parent strain (BW25113). We show that this switch to a motile phenotype is not a direct consequence of the genes deleted but is instead due to a variety of secondary mutations that increase the expression of the major motility regulator, FlhDC. Importantly, we find that this switch can be reproduced by growing poorly motile E. coli strains in nonshaking liquid medium overnight but not in shaking liquid medium. Individual isolates after the nonshaking overnight incubations acquired distinct mutations upstream of the flhDC operon, including different insertion sequence (IS) elements and, to a lesser extent, point mutations. The rapidity with which genetic changes sweep through the populations grown without shaking shows that poorly motile strains can quickly adapt to a motile lifestyle by genetic rewiring.IMPORTANCE The ability to tune gene expression in times of need outside preordained regulatory networks is an essential evolutionary process that allows organisms to survive and compete. Here, we show that upon overnight incubation in liquid medium without shaking, populations of largely nonmotile Escherichia coli bacteria can rapidly accumulate mutants that have constitutive motility. This effect contributes to widespread secondary mutations in the single-gene knockout library, the Keio collection. As a result, 49/71 (69%) of the Keio strains tested exhibited various degrees of motility, whereas their parental strain is poorly motile. These observations highlight the plasticity of gene expression even in the absence of preexisting regulatory programs and should raise awareness of procedures for handling laboratory strains of E. coli.

SUBMITTER: Parker DJ

PROVIDER: S-EPMC6755740 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Rapid Accumulation of Motility-Activating Mutations in Resting Liquid Culture of Escherichia coli.

Parker Darren J DJ Demetci Pınar P Li Gene-Wei GW

Journal of bacteriology 20190906 19

Expression of motility genes is a potentially beneficial but costly process in bacteria. Interestingly, many isolate strains of <i>Escherichia coli</i> possess motility genes but have lost the ability to activate them under conditions in which motility is advantageous, raising the question of how they respond to these situations. Through transcriptome profiling of strains in the <i>E. coli</i> single-gene knockout Keio collection, we noticed drastic upregulation of motility genes in many of the ...[more]

PMID: 31285239

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Project description:Many neutralophilic bacterial species try to evade acid stress with an escape strategy, which is reflected in the increased expression of genes coding for flagellar components. Extremely acid-tolerant bacteria, such as Escherichia coli, survive the strong acid stress, e.g., in the stomach of vertebrates. Recently, we were able to show that the induction of motility genes in E. coli is strictly dependent on the degree of acid stress, i.e., they are induced under mild acid stress but not under severe acid stress. However, it was not known to what extent fine-tuned expression of motility genes is related to fitness and the ability to survive periods of acid shock. In this study, we demonstrate that the expression of FlhDC, the master regulator of flagellation, is inversely correlated with the acid shock survival of E. coli. We encountered this phenomenon when analyzing mutants from the Keio collection, in which the expression of flhDC was altered by an insertion sequence element. These results suggest a fitness trade-off between acid tolerance and motility.IMPORTANCEEscherichia coli is extremely acid-resistant, which is crucial for survival in the gastrointestinal tract of vertebrates. Recently, we systematically studied the response of E. coli to mild and severe acidic conditions using Ribo-Seq and RNA-Seq. We found that motility genes are induced at pH 5.8 but not at pH 4.4, indicating stress-dependent synthesis of flagellar components. In this study, we demonstrate that motility-activating mutations upstream of flhDC, encoding the master regulator of flagella genes, reduce the ability of E. coli to survive periods of acid shock. Furthermore, we show an inverse correlation between motility and acid survival using a chromosomal isopropyl β-D-thio-galactopyranoside (IPTG)-inducible flhDC promoter and by sampling differentially motile subpopulations from swim agar plates. These results reveal a previously undiscovered trade-off between motility and acid tolerance and suggest a differentiation of E. coli into motile and acid-tolerant subpopulations, driven by the integration of insertion sequence elements.

Dataset Information

Rapid Accumulation of Motility-Activating Mutations in Resting Liquid Culture of Escherichia coli.

Publications

Rapid Accumulation of Motility-Activating Mutations in Resting Liquid Culture of Escherichia coli.

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