ChiS is a noncanonical DNA-binding hybrid sensor kinase that directly regulates the chitin utilization program in
            <i>Vibrio cholerae</i>

Klancher, Catherine A.; Yamamoto, Shouji; Dalia, Triana N.; Dalia, Ankur B.

doi:10.1073/pnas.2001768117

Cited by 23 publications

(40 citation statements)

References 57 publications

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“…Previous work from our group demonstrated that ChiS is a noncanonical hybrid histidine kinase that contains a DBD at its C terminus ( Fig. 1A ) ( 5 ). In that study, we found that the C-terminal 106 amino acids of ChiS (ChiS 1024–1129 ) were necessary and sufficient to bind to the chb promoter in vivo .…”

Section: Resultsmentioning

confidence: 91%

“…Chitin is sensed in V. cholerae by the hybrid histidine kinase ChiS ( 5 – 7 ). In response to chitin, ChiS activates the expression of the chitin utilization program.…”

Section: Introductionmentioning

confidence: 99%

“…This regulon includes the chb operon, which is required for the uptake and degradation of the chitin disaccharide chitobiose. In a recent study, we showed that unlike most histidine kinases, ChiS is capable of directly binding to DNA to regulate the expression of the chb operon ( 5 ). This finding was particularly surprising because ChiS is not predicted to contain a DNA-binding domain via primary sequence homology (BLAST [ 8 ]) or structural predictions (Phyre2 [ 9 ]).…”

Section: Introductionmentioning

confidence: 99%

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The ChiS-Family DNA-Binding Domain Contains a Cryptic Helix-Turn-Helix Variant

Klancher

Minasov

Podicheti

et al. 2021

mBio

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Sequence-specific DNA-binding domains (DBDs) are conserved in all domains of life. These proteins carry out a variety of cellular functions, and there are a number of distinct structural domains already described that allow for sequence-specific DNA binding, including the ubiquitous helix-turn-helix (HTH) domain. In the facultative pathogen Vibrio cholerae, the chitin sensor ChiS is a transcriptional regulator that is critical for the survival of this organism in its marine reservoir. We recently showed that ChiS contains a cryptic DBD in its C terminus. This domain is not homologous to any known DBD, but it is a conserved domain present in other bacterial proteins. Here, we present the crystal structure of the ChiS DBD at a resolution of 1.28 Å. We find that the ChiS DBD contains an HTH domain that is structurally similar to those found in other DNA-binding proteins, like the LacI repressor. However, one striking difference observed in the ChiS DBD is that the canonical tight turn of the HTH is replaced with an insertion containing a β-sheet, a variant which we term the helix-sheet-helix. Through systematic mutagenesis of all positively charged residues within the ChiS DBD, we show that residues within and proximal to the ChiS helix-sheet-helix are critical for DNA binding. Finally, through phylogenetic analyses we show that the ChiS DBD is found in diverse proteobacterial proteins that exhibit distinct domain architectures. Together, these results suggest that the structure described here represents the prototypical member of the ChiS-family of DBDs. IMPORTANCE Regulating gene expression is essential in all domains of life. This process is commonly facilitated by the activity of DNA-binding transcription factors. There are diverse structural domains that allow proteins to bind to specific DNA sequences. The structural basis underlying how some proteins bind to DNA, however, remains unclear. Previously, we showed that in the major human pathogen Vibrio cholerae, the transcription factor ChiS directly regulates gene expression through a cryptic DNA-binding domain. This domain lacked homology to any known DNA-binding protein. In the current study, we determined the structure of the ChiS DNA-binding domain (DBD) and found that the ChiS-family DBD is a cryptic variant of the ubiquitous helix-turn-helix (HTH) domain. We further demonstrate that this domain is conserved in diverse proteins that may represent a novel group of transcriptional regulators.

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Section: Resultsmentioning

confidence: 91%

“…Chitin is sensed in V. cholerae by the hybrid histidine kinase ChiS ( 5 – 7 ). In response to chitin, ChiS activates the expression of the chitin utilization program.…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The ChiS-Family DNA-Binding Domain Contains a Cryptic Helix-Turn-Helix Variant

Klancher

Minasov

Podicheti

et al. 2021

mBio

Self Cite

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“…Analytical ultracentrifugation studies also showed that TMAO binding to apoTorT increases its affinity for TorS-LBD, a finding that was also reflected in decreased atomic mobility at the TorS-LBD/TorT interface. In a similar way, the CBP SBP interacts with the non-canonical DNA binding sensor kinase ChiS to repress its activity, and the binding of chitin oligosaccharides by the CBP/ChiS complex activates ChiS without triggering the dissociation of the complex [58] . Of note is that these findings do not agree with a previous publication that suggested a ligand-induced dissociation of CBP from ChiS [59] .…”

Section: Sensor Kinases Diguanylate Cyclases/phosphodiesterases and Ser/thr Kinasesmentioning

confidence: 99%

The role of solute binding proteins in signal transduction

Matilla

Ortega

Krell

2021

Computational and Structural Biotechnology Journal

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“…Via secreted chitinases, V. cholerae breaks down the chitin polymers and use the oligomers, detected by the HK ChiS, as their sole source of carbon and nitrogen. 28 – 30 …”

Section: Navigating the Aquatic Environment: Watch And Roll With The mentioning

confidence: 99%

On or Off: Life-Changing Decisions Made by Vibrio cholerae Under Stress

Zhou

Lee

Zhu

2020

Infectious Microbes and Diseases

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Vibrio cholerae , the causative agent of the infectious disease, cholera, is commonly found in brackish waters and infects human hosts via the fecal-oral route. V. cholerae is a master of stress resistance as V. cholerae's dynamic lifestyle across different physical environments constantly exposes it to diverse stressful circumstances. Specifically, V. cholerae has dedicated genetic regulatory networks to sense different environmental cues and respond to these signals. With frequent outbreaks costing a tremendous amount of lives and increased global water temperatures providing more suitable aquatic habitats for V. cholerae , cholera pandemics remain a probable catastrophic threat to humanity. Understanding how V. cholerae copes with different environmental stresses broadens our repertoire of measures against infectious diseases and expands our general knowledge of prokaryotic stress responses. In this review, we summarize the regulatory mechanisms of how V. cholerae fights against stresses in vivo and in vitro.

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ChiS is a noncanonical DNA-binding hybrid sensor kinase that directly regulates the chitin utilization program in Vibrio cholerae

Cited by 23 publications

References 57 publications

The ChiS-Family DNA-Binding Domain Contains a Cryptic Helix-Turn-Helix Variant

The ChiS-Family DNA-Binding Domain Contains a Cryptic Helix-Turn-Helix Variant

The role of solute binding proteins in signal transduction

On or Off: Life-Changing Decisions Made by Vibrio cholerae Under Stress

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