<i>Escherichia coli</i> transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA)

Zhang, Xue Song; García‐Contreras, Rodolfo; Wood, Thomas K.

doi:10.1038/ismej.2008.24

Cited by 69 publications

(92 citation statements)

References 81 publications

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“…Glucose equivalents in the EPS samples were quantified by using a calibration curve with a glucose standard solution (GAHK20; Sigma-Aldrich Corp.) from 10 to 80 g/ml, and the values were normalized by cell turbidity at 600 nm. Colanic acid from the same samples was assayed by measuring fucose (49). An L-fucose (Acros Organics, Morris Plains, NJ) calibration curve from 10 to 60 g/ml was used to determine the fucose concentration, and these values were normalized by the cell turbidity at 600 nm.…”

Section: Methodsmentioning

confidence: 99%

Toxin-Antitoxin Systems in Escherichia coli Influence Biofilm Formation through YjgK (TabA) and Fimbriae

Kim¹,

Wang²,

Ma³

et al. 2009

J Bacteriol

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163

147

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The roles of toxin-antitoxin (TA) systems in bacteria have been debated. Here, the role of five TA systems in regard to biofilm development was investigated (listed as toxin/antitoxin: MazF/MazE, RelE/RelB, ChpB, YoeB/YefM, and YafQ/DinJ). Although these multiple TA systems were reported previously to not impact bacterial fitness, we found that deletion of the five TA systems decreased biofilm formation initially (8 h) on three different surfaces and then increased biofilm formation (24 h) by decreasing biofilm dispersal. Wholetranscriptome profiling revealed that the deletion of the five TA systems induced expression of a single gene, yjgK, which encodes an uncharacterized protein; quantitative real-time PCR (qRT-PCR) confirmed consistent induction of this gene (at 8, 15, and 24 h). Corroborating the complex phenotype seen upon deleting the TA systems, overexpression of YjgK decreased biofilm formation at 8 h and increased biofilm formation at 24 h; deletion of yjgK also affected biofilm formation in the expected manner by increasing biofilm formation after 8 h and decreasing biofilm formation after 24 h. In addition, YjgK significantly reduced biofilm dispersal. Whole-transcriptome profiling revealed YjgK represses fimbria genes at 8 h (corroborated by qRT-PCR and a yeast agglutination assay), which agrees with the decrease in biofilm formation upon deleting the five TA systems at 8 h, as well as that seen upon overexpressing YjgK. Sand column assays confirmed that deleting the five TA systems reduced cell attachment. Furthermore, deletion of each of the five toxins increased biofilm formation at 8 h, and overexpression of the five toxins repressed biofilm formation at 8 h, a result that is opposite that of deleting all five TA systems; this suggests that complex regulation occurs involving the antitoxins. Also, the ability of the global regulator Hha to reduce biofilm formation was dependent on the presence of these TA systems. Hence, we suggest that one role of TA systems is to influence biofilm formation.

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Section: Methodsmentioning

confidence: 99%

Toxin-Antitoxin Systems in Escherichia coli Influence Biofilm Formation through YjgK (TabA) and Fimbriae

Kim¹,

Wang²,

Ma³

et al. 2009

J Bacteriol

Self Cite

163

147

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“…In another study by the same research group, the toxicity of MqsR was reported and deletion of the nearby ygiV gene was shown to reduce this toxicity in MG1655 (59). Therefore, we studied the effect of ectopic expression of MqsR in MG1655 and found that this strain is indeed less toxic than HM21 (see Fig.…”

Section: Vol 192 2010mentioning

confidence: 99%

The Escherichia coli mqsR and ygiT Genes Encode a New Toxin-Antitoxin Pair

et al. 2010

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Toxin-antitoxin (TA) systems are plasmid-or chromosome-encoded protein complexes composed of a stable toxin and a short-lived inhibitor of the toxin. In cultures of Escherichia coli, transcription of toxin-antitoxin genes was induced in a nondividing subpopulation of bacteria that was tolerant to bactericidal antibiotics. Along with transcription of known toxin-antitoxin operons, transcription of mqsR and ygiT, two adjacent genes with multiple TA-like features, was induced in this cell population. Here we show that mqsR and ygiT encode a toxin-antitoxin system belonging to a completely new family which is represented in several groups of bacteria. The mqsR gene encodes a toxin, and ectopic expression of this gene inhibits growth and induces rapid shutdown of protein synthesis in vivo. ygiT encodes an antitoxin, which protects cells from the effects of MqsR. These two genes constitute a single operon which is transcriptionally repressed by the product of ygiT. We confirmed that transcription of this operon is induced in the ampicillin-tolerant fraction of a growing population of E. coli and in response to activation of the HipA toxin. Expression of the MqsR toxin does not kill bacteria but causes reversible growth inhibition and elongation of cells.Bacterial toxin-antitoxin (TA) systems (for reviews, see references 16 and 54) are complexes consisting of a stable toxin component and a short-lived antitoxin. Toxins of TA systems are autotoxic; they target vital functions of the producing bacterium itself. TA complexes were discovered because they are plasmid-stabilizing entities. When a bacterium carries a plasmid which encodes a toxin and an antitoxin, both molecules are produced continuously and have no effect on the activities of the cell. When the plasmid is lost during cell division, the toxin is released and kills or inhibits the cell, because the unstable antitoxin is degraded faster. Chromosomal TA systems were found later (36), and comparative studies determined that they are widespread in free-living bacteria (35, 41).There are two different types of bacterial TA systems, which depend on the nature of the antitoxin. In type I TA systems, the antitoxin is a small regulatory RNA (15, 18). In type II TA systems, which are relevant to this study, both the toxin and the antitoxin are proteins. Protein antitoxins neutralize toxins by direct interaction, forming catalytically inactive complexes. All known TA genes are organized as operons. The antitoxin is usually encoded by the first gene and always acts as a transcriptional autorepressor of the operon either alone or in a complex with the toxin molecule. Thus, antitoxins control toxin activity in two ways: through direct binding and through transcriptional regulation (17).The toxins of type II systems attack essential functions of a bacterial cell, either protein synthesis through cleavage of free or ribosome-bound mRNA (e.g., RelE, MazF, HigB, and HicA) (10,11,25,43) or the replication and integrity of DNA through interference with DNA gyrase (e.g., CcdB and ...

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“…In contrast, increased expression was identified for several TFs such as HdfR, McbR and NadR (Table 1). HdfR is a repressor of the genes encoding the flagellar master regulator FlhDC (Ko & Park, 2000) while McbR is a sensor of quorum sensing (QS) signal AI-2, and regulates biofilm formation and mucoidity by repressing expression of mcbA (Zhang et al, 2008). Together these two TFs participate in switching of the genomic programme from planktonic growth to biofilm formation.…”

Section: Expression Levels Of Tfs Under Aerobic Conditionsmentioning

confidence: 99%

“…McbR is a sensor of QS signal AI-2, and regulates biofilm formation and mucoidity by repressing expression of mcbA (Zhang et al, 2008). McbA is involved in cell-cell contact and biofilm modulation.…”

Section: Expression Levels Of Tfs Under Anaerobic Growth Conditionsmentioning

confidence: 99%

Expression levels of transcription factors in Escherichia coli: growth phase- and growth condition-dependent variation of 90 regulators from six families

Watanabe

Ishihama

2014

Microbiology

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The expression pattern of the genome in Escherichia coli is controlled by regulating the utilization of a limited number of RNA polymerases between a total of 4600 genes on its genome. The distribution pattern of RNA polymerase on the genome changes after two steps of protein-protein interaction with seven sigma subunits and about 300 transcription factors (TFs). Based on a systematic search for the regulation target promoters recognized by each TF, we propose two novel concepts: each TF regulates a number of target promoters; and each promoter is regulated by many TFs. In parallel, attempts have been made to determine the intracellular concentrations of all TFs using two systems: quantitative immunoblot analysis using TF-specific antibodies; and reporter assay of TF promoter activities. The direct measurement of TF protein level has so far been published for a set of 60 regulators with known functions. This study describes the determination of growth phase-dependent expression levels of 90 TFs using the reporter assay system. The translational fusion vector was constructed from the TF promoter sequence including an N-terminal proximal TF segment and the reporter GFP. At the beginning of cell growth, highlevel expression was observed only for a small number of TFs. In the exponential phase, approximately 80 % TFs are expressed, but the expressed TF species change upon transfer to the stationary phase. Significant changes in the pattern of TF expression were observed between aerobic and anaerobic conditions. The list of intracellular levels of TFs provides further understanding to the transcription regulation of the E. coli genome under various stressful conditions. INTRODUCTIONSingle-cell bacteria are directly exposed to frequently changing environments in nature and thus carry sophisticated genetic systems for adaptation to environmental changes (Ishihama, 2010(Ishihama, , 2012Yamamoto, 2014). On the basis of the complete genome sequence of several model Escherichia coli strains, the whole set of about 4600 genes has been predicted to exist in E. coli K-12 (Hayashi et al., 2006;Riley et al., 2006). In growing E. coli cells under laboratory culture conditions, only one-quarter to one-third of the genes on its genome are expressed, the others remaining silent. The majority of these uncharacterized silent genes must be expressed and utilized for adaptation and survival of E. coli under stressful conditions. Thus, even for this well-characterized model organism, the gene functions remain unidentified or unpredicted for approximately one-quarter because expression conditions of these silent genes have not yet been established.As the total number of RNA polymerases (RNAPs) in E. coli K-12 is less than the total number of genes on its genome (Ishihama, 2000), we proposed a model in which the change in genome transcription pattern takes place mainly through controlling the utilization of this limited number of transcription apparatuses between 4600 genes on the genome (Ishihama, 2010(Ishihama, , 2012. Two groups of reg...

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Escherichia coli transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA)

Cited by 69 publications

References 81 publications

Toxin-Antitoxin Systems in Escherichia coli Influence Biofilm Formation through YjgK (TabA) and Fimbriae

Toxin-Antitoxin Systems in Escherichia coli Influence Biofilm Formation through YjgK (TabA) and Fimbriae

The Escherichia coli mqsR and ygiT Genes Encode a New Toxin-Antitoxin Pair

Expression levels of transcription factors in Escherichia coli: growth phase- and growth condition-dependent variation of 90 regulators from six families

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