High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

ABSTRACT Histamine is a key biological signaling molecule. It acts as a neurotransmitter in the central and peripheral nervous systems and coordinates local inflammatory responses by modulating the activity of different immune cells. During inflammatory processes, including bacterial infections, neu...

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Autores principales:	Andrés Corral-Lugo, Miguel A. Matilla, David Martín-Mora, Hortencia Silva Jiménez, Noel Mesa Torres, Junichi Kato, Akiko Hida, Shota Oku, Mayte Conejero-Muriel, Jose A. Gavira, Tino Krell
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Pseudomonas aeruginosa chemotaxis histamine Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a9d5f6adc8fa4168882f343afc67f4e0
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spelling	oai:doaj.org-article:a9d5f6adc8fa4168882f343afc67f4e02021-11-15T15:52:19ZHigh-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>10.1128/mBio.01894-182150-7511https://doaj.org/article/a9d5f6adc8fa4168882f343afc67f4e02018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01894-18https://doaj.org/toc/2150-7511ABSTRACT Histamine is a key biological signaling molecule. It acts as a neurotransmitter in the central and peripheral nervous systems and coordinates local inflammatory responses by modulating the activity of different immune cells. During inflammatory processes, including bacterial infections, neutrophils stimulate the production and release of histamine. Here, we report that the opportunistic human pathogen Pseudomonas aeruginosa exhibits chemotaxis toward histamine. This chemotactic response is mediated by the concerted action of the TlpQ, PctA, and PctC chemoreceptors, which display differing sensitivities to histamine. Low concentrations of histamine were sufficient to activate TlpQ, which binds histamine with an affinity of 639 nM. To explore this binding, we resolved the high-resolution structure of the TlpQ ligand binding domain in complex with histamine. It has an unusually large dCACHE domain and binds histamine through a highly negatively charged pocket at its membrane distal module. Chemotaxis to histamine may play a role in the virulence of P. aeruginosa by recruiting cells at the infection site and consequently modulating the expression of quorum-sensing-dependent virulence genes. TlpQ is the first bacterial histamine receptor to be described and greatly differs from human histamine receptors, indicating that eukaryotes and bacteria have pursued different strategies for histamine recognition. IMPORTANCE Genome analyses indicate that many bacteria possess an elevated number of chemoreceptors, suggesting that these species are able to perform chemotaxis to a wide variety of compounds. The scientific community is now only beginning to explore this diversity and to elucidate the corresponding physiological relevance. The discovery of histamine chemotaxis in the human pathogen Pseudomonas aeruginosa provides insight into tactic movements that occur within the host. Since histamine is released in response to bacterial pathogens, histamine chemotaxis may permit bacterial migration and accumulation at infection sites, potentially modulating, in turn, quorum-sensing-mediated processes and the expression of virulence genes. As a consequence, the modulation of histamine chemotaxis by signal analogues may result in alterations of the bacterial virulence. As the first report of bacterial histamine chemotaxis, this study lays the foundation for the exploration of the physiological relevance of histamine chemotaxis and its role in pathogenicity.Andrés Corral-LugoMiguel A. MatillaDavid Martín-MoraHortencia Silva JiménezNoel Mesa TorresJunichi KatoAkiko HidaShota OkuMayte Conejero-MurielJose A. GaviraTino KrellAmerican Society for MicrobiologyarticlePseudomonas aeruginosachemotaxishistamineMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa chemotaxis histamine Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa chemotaxis histamine Microbiology QR1-502 Andrés Corral-Lugo Miguel A. Matilla David Martín-Mora Hortencia Silva Jiménez Noel Mesa Torres Junichi Kato Akiko Hida Shota Oku Mayte Conejero-Muriel Jose A. Gavira Tino Krell High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
description	ABSTRACT Histamine is a key biological signaling molecule. It acts as a neurotransmitter in the central and peripheral nervous systems and coordinates local inflammatory responses by modulating the activity of different immune cells. During inflammatory processes, including bacterial infections, neutrophils stimulate the production and release of histamine. Here, we report that the opportunistic human pathogen Pseudomonas aeruginosa exhibits chemotaxis toward histamine. This chemotactic response is mediated by the concerted action of the TlpQ, PctA, and PctC chemoreceptors, which display differing sensitivities to histamine. Low concentrations of histamine were sufficient to activate TlpQ, which binds histamine with an affinity of 639 nM. To explore this binding, we resolved the high-resolution structure of the TlpQ ligand binding domain in complex with histamine. It has an unusually large dCACHE domain and binds histamine through a highly negatively charged pocket at its membrane distal module. Chemotaxis to histamine may play a role in the virulence of P. aeruginosa by recruiting cells at the infection site and consequently modulating the expression of quorum-sensing-dependent virulence genes. TlpQ is the first bacterial histamine receptor to be described and greatly differs from human histamine receptors, indicating that eukaryotes and bacteria have pursued different strategies for histamine recognition. IMPORTANCE Genome analyses indicate that many bacteria possess an elevated number of chemoreceptors, suggesting that these species are able to perform chemotaxis to a wide variety of compounds. The scientific community is now only beginning to explore this diversity and to elucidate the corresponding physiological relevance. The discovery of histamine chemotaxis in the human pathogen Pseudomonas aeruginosa provides insight into tactic movements that occur within the host. Since histamine is released in response to bacterial pathogens, histamine chemotaxis may permit bacterial migration and accumulation at infection sites, potentially modulating, in turn, quorum-sensing-mediated processes and the expression of virulence genes. As a consequence, the modulation of histamine chemotaxis by signal analogues may result in alterations of the bacterial virulence. As the first report of bacterial histamine chemotaxis, this study lays the foundation for the exploration of the physiological relevance of histamine chemotaxis and its role in pathogenicity.
format	article
author	Andrés Corral-Lugo Miguel A. Matilla David Martín-Mora Hortencia Silva Jiménez Noel Mesa Torres Junichi Kato Akiko Hida Shota Oku Mayte Conejero-Muriel Jose A. Gavira Tino Krell
author_facet	Andrés Corral-Lugo Miguel A. Matilla David Martín-Mora Hortencia Silva Jiménez Noel Mesa Torres Junichi Kato Akiko Hida Shota Oku Mayte Conejero-Muriel Jose A. Gavira Tino Krell
author_sort	Andrés Corral-Lugo
title	High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_short	High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full	High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_fullStr	High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full_unstemmed	High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_sort	high-affinity chemotaxis to histamine mediated by the tlpq chemoreceptor of the human pathogen <named-content content-type="genus-species">pseudomonas aeruginosa</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/a9d5f6adc8fa4168882f343afc67f4e0
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High-Affinity Chemotaxis to Histamine Mediated by the TlpQ Chemoreceptor of the Human Pathogen <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

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