Genomic SELEX Reveals Pervasive Role of the Flagella Master Regulator FlhDC in Carbon Metabolism

Takada, Hiraku; Kijima, Kaede; Ishiguro, Akira; Ishihama, Akira; Shimada, Tomohiro

doi:10.3390/ijms24043696

Cited by 3 publications

(3 citation statements)

References 38 publications

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“…Specifically, deletion of these factors has been observed to diminish E. coli's motility 60,61 Furthermore, FlhD and FlhC proteins, both transcriptional factors, play roles in glucose and fructose uptake and metabolism, as well as other carbon metabolic pathways 65 . A knockout of these genes indeed led to growth retardation, coupled with increased ATP and NADPH production, shifting carbon flux towards the TCA cycle and pentose phosphate pathways 66 .…”

Section: Whole-genome Sequencing Reveal Mutations Related To Motility...mentioning

confidence: 99%

Quantifying the intra- and inter-species community interaction in a microbiome by dynamic covariance mapping

Serohijos,

Gencel,

Hui

et al. 2024

Preprint

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A microbiome’s composition, stability, and response to perturbations is dictated by the community interaction matrix 1-10 that is commonly assayed by pair-wise species competition. In their natural environment however, microbes concurrently experience multiple species, face conditions that may be difficult to mimic in vitro, and have members that are impractical to isolate. Additionally, due to overlapping of evolutionary and ecological timescales, the community interaction matrix is also influenced by intra-species diversity, but how and to what extent remains poorly understood 11-14. Here, we develop a general approach called Dynamic Covariance Mapping (DCM) to estimate the interaction matrix of multispecies microbiome community in its natural environment from abundance time-series data. Together with intra-species high-resolution lineage tracking via chromosomal barcoding, we quantify the inter- and intra-species community interaction matrix during E. coli colonization of mice gut microbiome with increasing complexity: germ-free, antibiotic-perturbed, and innate microbiota. With DCM, we differentiate three temporal phases of invasion in the susceptible communities: 1) initial loss of community stability as E. coli enters; 2) recolonization of some gut bacteria; and 3) recovery of stability with E. coli clones coexisting with resident bacteria in a quasi-steady state. These phases are influenced by specific interactions between E. coli sub-lineages with other species in the community. These results highlight the transient nature and time-dependence of community interaction networks in microbiomes driven by the persistent coupling of ecological and evolutionary dynamics. Our theoretical and experimental approach can be applied to characterize coupled ecological-evolutionary dynamics of bacterial communities in vitro and in situ.

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Section: Whole-genome Sequencing Reveal Mutations Related To Motility...mentioning

confidence: 99%

Quantifying the intra- and inter-species community interaction in a microbiome by dynamic covariance mapping

Serohijos,

Gencel,

Hui

et al. 2024

Preprint

View full text Add to dashboard Cite

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“…This is because virulence factors are not always expressed in microorganisms but are expressed in adaptation to a certain environment or a certain cellular condition [5][6][7]. Microorganisms are also often used to produce useful compounds, but metabolic pathways do not always maintain the same activity; they change their activities in response to changing environments or cellular conditions [8][9][10]. In short, organisms are often studied for specific functions for specific purposes but understanding them not only from the analysis of specific factors related to those purposes but also in terms of their roles for the organism, their cooperative relationships with cells, and their regulatory network mechanisms, will provide essential understanding and applications.…”

mentioning

confidence: 99%

“…However, the genome-wide transcriptional regulation of FlhDC was poorly understood. Takada et al attempted to re-examine the role of FlhDC, the master regulator of flagellum formation genes, in the entire E. coli genome regulatory network by using Genomic SELEX (gSELEX)-chip screening to uncover a direct set of target genes in vitro [8]. They identified novel target genes involved in the sugar utilization phosphotransferase system, sugar catabolic pathway of glycolysis, and other carbon source metabolic pathways in addition to the known flagella formation target genes.…”

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confidence: 99%

Overview of the Molecular Mechanism of Bacterial Environmental Adaptation by Comprehensive Analysis

Shimada

Yoshida

2023

IJMS

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Motility-activating mutations upstream of flhDC reduce acid shock survival of Escherichia coli

Schumacher,

Braun,

Kleigrewe

et al. 2024

Microbiol Spectr

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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. IMPORTANCE Escherichia 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.

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Genomic SELEX Reveals Pervasive Role of the Flagella Master Regulator FlhDC in Carbon Metabolism

Cited by 3 publications

References 38 publications

Quantifying the intra- and inter-species community interaction in a microbiome by dynamic covariance mapping

Quantifying the intra- and inter-species community interaction in a microbiome by dynamic covariance mapping

Overview of the Molecular Mechanism of Bacterial Environmental Adaptation by Comprehensive Analysis

Motility-activating mutations upstream of flhDC reduce acid shock survival of Escherichia coli

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