Cross talk in promoter recognition between six NarL‐family response regulators of <i>Escherichia coli</i> two‐component system

Yoshida, Masahito; Ishihama, Akira

doi:10.1111/gtc.12251

Cited by 14 publications

(9 citation statements)

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“…While there have been 30 or more paired two-component systems identified in E. coli and other well-studied model organisms and pathogens (Yoshida et al, 2015), very few TCS genes have been identified in the non-model organism Francisella . The two-component systems that are currently known in the genus Francisella are summarized in Table 1.…”

Section: Tcs Genes Present In the Genus Francisellamentioning

confidence: 99%

“…Although it is thought that SKs of paired TCSs will typically or preferentially phosphorylate their cognate RR, it is known that “promiscuity” between SKs and RRs can occur, in which they can “cross-talk” between different SKs and RRs (Yoshida et al, 2015; Groisman, 2016). Especially for organisms with very limited TCS genes and several orphan TCS genes, such as is observed in Francisella , it seems likely that promiscuous cross-phosphorylation could occur (Murch et al, 2017).…”

Section: Cross-talk Between Tcs Proteinsmentioning

confidence: 99%

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Two-Component Systems in Francisella Species

Hoek

Hoang

2019

Front. Cell. Infect. Microbiol.

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Bacteria alter gene expression in response to changes in their environment through various mechanisms that include signal transduction systems. These signal transduction systems use membrane histidine kinase with sensing domains to mediate phosphotransfer to DNA-binding proteins that alter the level of gene expression. Such regulators are called two-component systems (TCSs). TCSs integrate external signals and information from stress pathways, central metabolism and other global regulators, thus playing an important role as part of the overall regulatory network. This review will focus on the knowledge of TCSs in the Gram-negative bacterium, Francisella tularensis , a biothreat agent with a wide range of potential hosts and a significant ability to cause disease. While TCSs have been well-studied in several bacterial pathogens, they have not been well-studied in non-model organisms, such as F. tularensis and its subspecies, whose canonical TCS content surprisingly ranges from few to none. Additionally, of those TCS genes present, many are orphan components, including KdpDE, QseC, QseB/PmrA, and an unnamed two-component system (FTN_1452/FTN_1453). We discuss recent advances in this field related to the role of TCSs in Francisella physiology and pathogenesis and compare the TCS genes present in human virulent versus. environmental species and subspecies of Francisella .

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Section: Tcs Genes Present In the Genus Francisellamentioning

confidence: 99%

Section: Cross-talk Between Tcs Proteinsmentioning

confidence: 99%

Two-Component Systems in Francisella Species

Hoek

Hoang

2019

Front. Cell. Infect. Microbiol.

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“…The phosphoryl group is subsequently transferred to an aspartate residue in the RR, which induces a conformational change enabling the RR to function as a DNA binding transcriptional regulator. Although most bacterial TCSs are highly specific, cross talk between similar is observed in rare instances systems (19)(20)(21)(22). The bacterial response to the environmental signal is itself tightly regulated.…”

mentioning

confidence: 99%

The ChrSA and HrrSA Two-Component Systems Are Required for Transcriptional Regulation of the hemA Promoter in Corynebacterium diphtheriae

Burgos

Schmitt

2016

J Bacteriol

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Corynebacterium diphtheriae utilizes heme and hemoglobin (Hb) as iron sources for growth in low-iron environments. In C. diphtheriae, the two-component signal transduction systems (TCSs) ChrSA and HrrSA are responsive to Hb levels and regulate the transcription of promoters for hmuO, hrtAB, and hemA. ChrSA and HrrSA activate transcription at the hmuO promoter and repress transcription at hemA in an Hb-dependent manner. In this study, we show that HrrSA is the predominant repressor at hemA and that its activity results in transcriptional repression in the presence and absence of Hb, whereas repression of hemA by ChrSA is primarily responsive to Hb. DNA binding studies showed that both ChrA and HrrA bind to the hemA promoter region at virtually identical sequences. ChrA binding was enhanced by phosphorylation, while binding to DNA by HrrA was independent of its phosphorylation state. ChrA and HrrA are phosphorylated in vitro by the sensor kinase ChrS, whereas no kinase activity was observed with HrrS in vitro. Phosphorylated ChrA was not observed in vivo, even in the presence of Hb, which is likely due to the instability of the phosphate moiety on ChrA. However, phosphorylation of HrrA was observed in vivo regardless of the presence of the Hb inducer, and genetic analysis indicates that ChrS is responsible for most of the phosphorylation of HrrA in vivo. Phosphorylation studies strongly suggest that HrrS functions primarily as a phosphatase and has only minimal kinase activity. These findings collectively show a complex mechanism of regulation at the hemA promoter, where both two-component systems act in concert to optimize expression of heme biosynthetic enzymes. IMPORTANCEUnderstanding the mechanism by which two-component signal transduction systems function to respond to environmental stimuli is critical to the study of bacterial pathogenesis. The current study expands on the previous analyses of the ChrSA and HrrSA TCSs in the human pathogen C. diphtheriae. The findings here underscore the complex interactions between the ChrSA and HrrSA systems in the regulation of the hemA promoter and demonstrate how the two systems complement one another to refine and control transcription in the presence and absence of Hb.C orynebacterium diphtheriae, a strict human pathogen, is the etiologic agent of diphtheria (1-3). After colonizing the upper respiratory tract, actively dividing cells secrete the potent diphtheria toxin (DT), which disseminates throughout the host and elicits the major clinical symptoms of the disease (1-3). Expression of DT is negatively regulated at the transcriptional level by iron and the diphtheria toxin repressor protein DtxR (3, 4). Although essential for bacterial physiology, iron is not readily available for invading pathogens since much of it is sequestered by host proteins such as transferrin, lactoferrin, and hemoglobin (Hb) (5-7).To thrive in such a stringent environment, bacteria utilize a variety of tightly regulated iron-and heme-scavenging systems (7,8). C. diphtheriae, in part...

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“…In TCS signal transduction, crosstalk takes place at all three stages: recognition of external signal by the sensor kinase, phosphorylation of the response regulator by the sensor kinase, and recognition of regulatory targets by the response regulator (Yoshida et al, 2015;Yamamoto et al, 2018). Previously, we identified that CusR is phosphorylated by not only CusS, the cognate pairing sensor kinase, but also other TCS sensor kinases, including UhpB (the sensor kinase of UhpAB TCS) and HprS (the sensor kinase of HprSR TCS) (Yamamoto et al, 2005;Urano et al, 2017).…”

Section: Conditional Type-a Single-target Tfsmentioning

confidence: 99%

Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12

et al. 2021

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The identification of regulatory targets of all transcription factors (TFs) is critical for understanding the entire network of genome regulation. A total of approximately 300 TFs exist in the model prokaryote Escherichia coli K-12, but the identification of whole sets of their direct targets is impossible with use of in vivo approaches. For this end, the most direct and quick approach is to identify the TF-binding sites in vitro on the genome. We then developed and utilized the gSELEX screening system in vitro for identification of more than 150 E. coli TF-binding sites along the E. coli genome. Based on the number of predicted regulatory targets, we classified E. coli K-12 TFs into four groups, altogether forming a hierarchy ranging from a single-target TF (ST-TF) to local TFs, global TFs, and nucleoid-associated TFs controlling as many as 1,000 targets. Using the collection of purified TFs and a library of genome DNA segments from a single and the same E. coli K-12, we identified here a total of 11 novel ST-TFs, CsqR, CusR, HprR, NorR, PepA, PutA, QseA, RspR, UvrY, ZraR, and YqhC. The regulation of single-target promoters was analyzed in details for the hitherto uncharacterized QseA and RspR. In most cases, the ST-TF gene and its regulatory target genes are adjacently located on the E. coli K-12 genome, implying their simultaneous transfer in the course of genome evolution. The newly identified 11 ST-TFs and the total of 13 hitherto identified altogether constitute the minority group of TFs in E. coli K-12.

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Cross talk in promoter recognition between six NarL‐family response regulators of Escherichia coli two‐component system

Cited by 14 publications

References 67 publications

Two-Component Systems in Francisella Species

Two-Component Systems in Francisella Species

The ChrSA and HrrSA Two-Component Systems Are Required for Transcriptional Regulation of the hemA Promoter in Corynebacterium diphtheriae

Single-Target Regulators Constitute the Minority Group of Transcription Factors in Escherichia coli K-12

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