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IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way.

ABSTRACT: Mutation rates may be influenced by the environment. Here, we demonstrate that insertion sequence IS5 in Escherichia coli inserts into the upstream region of the flhDC operon in a manner that depends on whether the environment permits motility; this operon encodes the master regulator of cell motility, FlhDC, and the IS5 insertion increases motility. IS5 inserts upstream of flhD(+) when cells are grown on soft-agar plates that permit swimming motility, but does not insert upstream of this locus on hard-agar plates that do not permit swimming motility or in planktonic cultures. Furthermore, there was only one IS5 insertion event on soft-agar plates, indicating insertion of IS5 into flhDC is not due to general elevated IS5 transposition throughout the whole genome. We also show that the highly motile cells with IS5 upstream of flhD(+) have greater biofilm formation, although there is a growth cost due to the energetic burden of the enhanced motility as these highly motile cells have a lower yield in rich medium and reduced growth rate. Functional flagella are required for IS5 insertion upstream of flhD(+) as there was no IS5 insertion upstream of flhD(+) for flhD, flgK and motA mutants, and the mutation is stable. Additionally, the IS5 mutation occurs during biofilm formation, which creates genetic and phenotypic diversity. Hence, the cells appear to 'sense' whether motility is feasible before a sub-population undergoes a mutation to become hypermotile; this sensing appears related to the master transcription regulator, FlhDC.

SUBMITTER: Wang X

PROVIDER: S-EPMC3160685 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way.

Wang Xiaoxue X Wood Thomas K TK

The ISME journal 20110310 9

Mutation rates may be influenced by the environment. Here, we demonstrate that insertion sequence IS5 in Escherichia coli inserts into the upstream region of the flhDC operon in a manner that depends on whether the environment permits motility; this operon encodes the master regulator of cell motility, FlhDC, and the IS5 insertion increases motility. IS5 inserts upstream of flhD(+) when cells are grown on soft-agar plates that permit swimming motility, but does not insert upstream of this locus ...[more]

PMID: 21390082

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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

IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way.

Publications

IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way.

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