Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.

Quorum sensing is a chemical communication process that bacteria use to coordinate group behaviors. In the global pathogen Vibrio cholerae, one quorum-sensing receptor and transcription factor, called VqmA (VqmAVc), activates expression of the vqmR gene encoding the small regulatory RNA VqmR, which...

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Autores principales:	Olivia P Duddy, Xiuliang Huang, Justin E Silpe, Bonnie L Bassler
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/3cef38b98f93460a8ad8b57666e62e57
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spelling	oai:doaj.org-article:3cef38b98f93460a8ad8b57666e62e572021-12-02T20:02:46ZMechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.1553-73901553-740410.1371/journal.pgen.1009550https://doaj.org/article/3cef38b98f93460a8ad8b57666e62e572021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009550https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Quorum sensing is a chemical communication process that bacteria use to coordinate group behaviors. In the global pathogen Vibrio cholerae, one quorum-sensing receptor and transcription factor, called VqmA (VqmAVc), activates expression of the vqmR gene encoding the small regulatory RNA VqmR, which represses genes involved in virulence and biofilm formation. Vibriophage VP882 encodes a VqmA homolog called VqmAPhage that activates transcription of the phage gene qtip, and Qtip launches the phage lytic program. Curiously, VqmAPhage can activate vqmR expression but VqmAVc cannot activate expression of qtip. Here, we investigate the mechanism underlying this asymmetry. We find that promoter selectivity is driven by each VqmA DNA-binding domain and key DNA sequences in the vqmR and qtip promoters are required to maintain specificity. A protein sequence-guided mutagenesis approach revealed that the residue E194 of VqmAPhage and A192, the equivalent residue in VqmAVc, in the helix-turn-helix motifs contribute to promoter-binding specificity. A genetic screen to identify VqmAPhage mutants that are incapable of binding the qtip promoter but maintain binding to the vqmR promoter delivered additional VqmAPhage residues located immediately C-terminal to the helix-turn-helix motif as required for binding the qtip promoter. Surprisingly, these residues are conserved between VqmAPhage and VqmAVc. A second, targeted genetic screen revealed a region located in the VqmAVc DNA-binding domain that is necessary to prevent VqmAVc from binding the qtip promoter, thus restricting DNA binding to the vqmR promoter. We propose that the VqmAVc helix-turn-helix motif and the C-terminal flanking residues function together to prohibit VqmAVc from binding the qtip promoter.Olivia P DuddyXiuliang HuangJustin E SilpeBonnie L BasslerPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009550 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Olivia P Duddy Xiuliang Huang Justin E Silpe Bonnie L Bassler Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.
description	Quorum sensing is a chemical communication process that bacteria use to coordinate group behaviors. In the global pathogen Vibrio cholerae, one quorum-sensing receptor and transcription factor, called VqmA (VqmAVc), activates expression of the vqmR gene encoding the small regulatory RNA VqmR, which represses genes involved in virulence and biofilm formation. Vibriophage VP882 encodes a VqmA homolog called VqmAPhage that activates transcription of the phage gene qtip, and Qtip launches the phage lytic program. Curiously, VqmAPhage can activate vqmR expression but VqmAVc cannot activate expression of qtip. Here, we investigate the mechanism underlying this asymmetry. We find that promoter selectivity is driven by each VqmA DNA-binding domain and key DNA sequences in the vqmR and qtip promoters are required to maintain specificity. A protein sequence-guided mutagenesis approach revealed that the residue E194 of VqmAPhage and A192, the equivalent residue in VqmAVc, in the helix-turn-helix motifs contribute to promoter-binding specificity. A genetic screen to identify VqmAPhage mutants that are incapable of binding the qtip promoter but maintain binding to the vqmR promoter delivered additional VqmAPhage residues located immediately C-terminal to the helix-turn-helix motif as required for binding the qtip promoter. Surprisingly, these residues are conserved between VqmAPhage and VqmAVc. A second, targeted genetic screen revealed a region located in the VqmAVc DNA-binding domain that is necessary to prevent VqmAVc from binding the qtip promoter, thus restricting DNA binding to the vqmR promoter. We propose that the VqmAVc helix-turn-helix motif and the C-terminal flanking residues function together to prohibit VqmAVc from binding the qtip promoter.
format	article
author	Olivia P Duddy Xiuliang Huang Justin E Silpe Bonnie L Bassler
author_facet	Olivia P Duddy Xiuliang Huang Justin E Silpe Bonnie L Bassler
author_sort	Olivia P Duddy
title	Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.
title_short	Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.
title_full	Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.
title_fullStr	Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.
title_full_unstemmed	Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.
title_sort	mechanism underlying the dna-binding preferences of the vibrio cholerae and vibriophage vp882 vqma quorum-sensing receptors.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/3cef38b98f93460a8ad8b57666e62e57
work_keys_str_mv	AT oliviapduddy mechanismunderlyingthednabindingpreferencesofthevibriocholeraeandvibriophagevp882vqmaquorumsensingreceptors AT xiulianghuang mechanismunderlyingthednabindingpreferencesofthevibriocholeraeandvibriophagevp882vqmaquorumsensingreceptors AT justinesilpe mechanismunderlyingthednabindingpreferencesofthevibriocholeraeandvibriophagevp882vqmaquorumsensingreceptors AT bonnielbassler mechanismunderlyingthednabindingpreferencesofthevibriocholeraeandvibriophagevp882vqmaquorumsensingreceptors
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Mechanism underlying the DNA-binding preferences of the Vibrio cholerae and vibriophage VP882 VqmA quorum-sensing receptors.

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