A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals

Stenotrophomonas maltophilia is an environmental bacterium as well as an emerging opportunistic multidrug-resistant pathogen. They use the endogenous diffusible signal factor (DSF) quorum sensing (QS) system to coordinate population behavior and regulate virulence processes but can also respond to e...

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Autores: Coves, Xavier, Bravo, Marc, Huedo, Pol, Conchillo-Solé, Òscar, Gómez, Andromeda-Celeste, Esteve-Codina, Anna, Dabad, Marc, Gut, Marta, Daura, Xavier, Yero, Daniel, Gibert, Isidre
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/57837
Acesso em linha:http://hdl.handle.net/10230/57837
http://dx.doi.org/10.1128/aem.00635-23
Access Level:acceso abierto
Palavra-chave:DSF
N-acyl homoserine lactones
Stenotrophomonas
TetR-like regulator
Fatty acid metabolism
Quorum sensing
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repository_id_str
spelling A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signalsCoves, XavierBravo, MarcHuedo, PolConchillo-Solé, ÒscarGómez, Andromeda-CelesteEsteve-Codina, AnnaDabad, MarcGut, MartaDaura, XavierYero, DanielGibert, IsidreDSFN-acyl homoserine lactonesStenotrophomonasTetR-like regulatorFatty acid metabolismQuorum sensingStenotrophomonas maltophilia is an environmental bacterium as well as an emerging opportunistic multidrug-resistant pathogen. They use the endogenous diffusible signal factor (DSF) quorum sensing (QS) system to coordinate population behavior and regulate virulence processes but can also respond to exogenous N-acyl-homoserine lactone (AHL) signals produced by neighboring bacteria. The effect of these QS signals on the global gene expression of this species remains, however, unknown. Whole-transcriptome sequencing analyses were performed for exponential cultures of S. maltophilia K279a treated with exogenous DSF or AHLs. Addition of DSF and AHLs signals resulted in changes in expression of at least 2-fold for 28 and 82 genes, respectively. Interestingly, 22 of these genes were found upregulated by both QS signals, 14 of which were shown to also be induced during the stationary phase. Gene functions regulated by all conditions included lipid and amino acid metabolism, stress response and signal transduction, nitrogen and iron metabolism, and adaptation to microoxic conditions. Among the common top upregulated QS core genes, a putative TetR-like regulator (locus tag SMLT2053) was selected for functional characterization. This regulator controls its own β-oxidation operon (Smlt2053-Smlt2051), and it is found to sense long-chain fatty acids (FAs), including the QS signal DSF. Gene knockout experiments reveal that operon Smlt2053-Smlt2051 is involved in biofilm formation. Overall, our findings provide clues on the effect that QS signals have in S. maltophilia QS-related phenotypes and the transition from the exponential to the stationary phase and bacterial fitness under high-density growth. IMPORTANCE The quorum sensing system in Stenotrophomonas maltophilia, in addition to coordinating the bacterial population, controls virulence-associated phenotypes, such as biofilm formation, motility, protease production, and antibiotic resistance mechanisms. Biofilm formation is frequently associated with the persistence and chronic nature of nosocomial infections. In addition, biofilms exhibit high resistance to antibiotics, making treatment of these infections extremely difficult. The importance of studying the metabolic and regulatory systems controlled by quorum sensing autoinducers will make it possible to discover new targets to control pathogenicity mechanisms in S. maltophilia.This work was funded by the Spanish MICINN (PID2019-111364RB-I00). Research at CNAG-CRG was funded by the Instituto de Salud Carlos III Spain (reference PT17/0009/0019) and cofunded by FEDER funds (European Regional Development Fund).American Society for Microbiology202320232023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/57837http://dx.doi.org/10.1128/aem.00635-23reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésAppl Environ Microbiol. 2023 Jun 28;89(6):e0063523info:eu-repo/grantAgreement/ES/2PE/PID2019-111364RB-I00© 2023 Coves et al. This is an openaccess article distributed under the terms of the Creative Commons Attribution 4.0 International license.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/578372026-06-12T07:21:37Z
dc.title.none.fl_str_mv A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
title A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
spellingShingle A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
Coves, Xavier
DSF
N-acyl homoserine lactones
Stenotrophomonas
TetR-like regulator
Fatty acid metabolism
Quorum sensing
title_short A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
title_full A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
title_fullStr A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
title_full_unstemmed A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
title_sort A Stenotrophomonas maltophilia TetR-like transcriptional regulator involved in fatty acid metabolism is controlled by quorum sensing signals
dc.creator.none.fl_str_mv Coves, Xavier
Bravo, Marc
Huedo, Pol
Conchillo-Solé, Òscar
Gómez, Andromeda-Celeste
Esteve-Codina, Anna
Dabad, Marc
Gut, Marta
Daura, Xavier
Yero, Daniel
Gibert, Isidre
author Coves, Xavier
author_facet Coves, Xavier
Bravo, Marc
Huedo, Pol
Conchillo-Solé, Òscar
Gómez, Andromeda-Celeste
Esteve-Codina, Anna
Dabad, Marc
Gut, Marta
Daura, Xavier
Yero, Daniel
Gibert, Isidre
author_role author
author2 Bravo, Marc
Huedo, Pol
Conchillo-Solé, Òscar
Gómez, Andromeda-Celeste
Esteve-Codina, Anna
Dabad, Marc
Gut, Marta
Daura, Xavier
Yero, Daniel
Gibert, Isidre
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv DSF
N-acyl homoserine lactones
Stenotrophomonas
TetR-like regulator
Fatty acid metabolism
Quorum sensing
topic DSF
N-acyl homoserine lactones
Stenotrophomonas
TetR-like regulator
Fatty acid metabolism
Quorum sensing
description Stenotrophomonas maltophilia is an environmental bacterium as well as an emerging opportunistic multidrug-resistant pathogen. They use the endogenous diffusible signal factor (DSF) quorum sensing (QS) system to coordinate population behavior and regulate virulence processes but can also respond to exogenous N-acyl-homoserine lactone (AHL) signals produced by neighboring bacteria. The effect of these QS signals on the global gene expression of this species remains, however, unknown. Whole-transcriptome sequencing analyses were performed for exponential cultures of S. maltophilia K279a treated with exogenous DSF or AHLs. Addition of DSF and AHLs signals resulted in changes in expression of at least 2-fold for 28 and 82 genes, respectively. Interestingly, 22 of these genes were found upregulated by both QS signals, 14 of which were shown to also be induced during the stationary phase. Gene functions regulated by all conditions included lipid and amino acid metabolism, stress response and signal transduction, nitrogen and iron metabolism, and adaptation to microoxic conditions. Among the common top upregulated QS core genes, a putative TetR-like regulator (locus tag SMLT2053) was selected for functional characterization. This regulator controls its own β-oxidation operon (Smlt2053-Smlt2051), and it is found to sense long-chain fatty acids (FAs), including the QS signal DSF. Gene knockout experiments reveal that operon Smlt2053-Smlt2051 is involved in biofilm formation. Overall, our findings provide clues on the effect that QS signals have in S. maltophilia QS-related phenotypes and the transition from the exponential to the stationary phase and bacterial fitness under high-density growth. IMPORTANCE The quorum sensing system in Stenotrophomonas maltophilia, in addition to coordinating the bacterial population, controls virulence-associated phenotypes, such as biofilm formation, motility, protease production, and antibiotic resistance mechanisms. Biofilm formation is frequently associated with the persistence and chronic nature of nosocomial infections. In addition, biofilms exhibit high resistance to antibiotics, making treatment of these infections extremely difficult. The importance of studying the metabolic and regulatory systems controlled by quorum sensing autoinducers will make it possible to discover new targets to control pathogenicity mechanisms in S. maltophilia.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/57837
http://dx.doi.org/10.1128/aem.00635-23
url http://hdl.handle.net/10230/57837
http://dx.doi.org/10.1128/aem.00635-23
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Appl Environ Microbiol. 2023 Jun 28;89(6):e0063523
info:eu-repo/grantAgreement/ES/2PE/PID2019-111364RB-I00
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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