Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection

Autores
Tuttobene, Marisel Romina; Arango Gil, Brayan Stiven; Di Venanzio, Gisela Andrea; Mariscotti, Javier Fernando; Sieira, Rodrigo; Feldman, Mario F.; Ramirez, María Soledad; Garcia Vescovi, Eleonora
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Serratia marcescens, a member of the Enterobacteriaceae family, is an opportunistic human pathogen and a frequent cause of urinary tract infections. Clinical isolates often exhibit resistance to multiple antibiotics, posing challenges for successful treatment. Understanding its pathogenic mechanisms is crucial for elucidating new potential targets to develop effective therapeutic interventions and manage S. marcescens infections. This work identifies urea-induced lactonase of Serratia (UilS), a lactonase encoded in the S. marcescens RM66262 strain isolated from a patient with a urinary tract infection. The study explores the bacterium´s response to urea, a major component of urine, and its impact on uilS expression. We found that UilS degrades acyl-homoserine lactones (AHL) autoinducers traditionally associated with quorum sensing mechanisms. Surprisingly, UilS is able to degrade self and non-self AHL, exhibiting quorum-quenching activity toward Pseudomonas aeruginosa. We found that LuxR regulates uilS expression that is enhanced in the presence of AHL. In addition, urea-dependent induction of UilS expression is controlled by the transcriptional response regulator CpxR. UilS confers fitness advantage to S. marcescens, especially in the presence of urea, emphasizing the adaptive plasticity of strains to modulate gene expression based on environmental signals and population density. We also discovered a novel bacterial killing capacity of S. marcescens that involves UilS, indicating its importance in the interspecies interaction of Serratia. Finally, we found that a uilS mutant strain displays attenuated colonization in a mouse model of catheter-associated urinary tract infection. uilS is present in clinical but absent in environmental isolates, suggesting an evolutionary adaptation to host-specific selective pressures.
Fil: Tuttobene, Marisel Romina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Arango Gil, Brayan Stiven. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Di Venanzio, Gisela Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. University of Washington; Estados Unidos
Fil: Mariscotti, Javier Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Sieira, Rodrigo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Feldman, Mario F.. University of Washington; Estados Unidos
Fil: Ramirez, María Soledad. California State University; Estados Unidos
Fil: Garcia Vescovi, Eleonora. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Materia
Serratia
Quorum quenching
Lactonase
Pathogenesis
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/266223
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/266223
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infectionTuttobene, Marisel RominaArango Gil, Brayan StivenDi Venanzio, Gisela AndreaMariscotti, Javier FernandoSieira, RodrigoFeldman, Mario F.Ramirez, María SoledadGarcia Vescovi, EleonoraSerratiaQuorum quenchingLactonasePathogenesishttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Serratia marcescens, a member of the Enterobacteriaceae family, is an opportunistic human pathogen and a frequent cause of urinary tract infections. Clinical isolates often exhibit resistance to multiple antibiotics, posing challenges for successful treatment. Understanding its pathogenic mechanisms is crucial for elucidating new potential targets to develop effective therapeutic interventions and manage S. marcescens infections. This work identifies urea-induced lactonase of Serratia (UilS), a lactonase encoded in the S. marcescens RM66262 strain isolated from a patient with a urinary tract infection. The study explores the bacterium´s response to urea, a major component of urine, and its impact on uilS expression. We found that UilS degrades acyl-homoserine lactones (AHL) autoinducers traditionally associated with quorum sensing mechanisms. Surprisingly, UilS is able to degrade self and non-self AHL, exhibiting quorum-quenching activity toward Pseudomonas aeruginosa. We found that LuxR regulates uilS expression that is enhanced in the presence of AHL. In addition, urea-dependent induction of UilS expression is controlled by the transcriptional response regulator CpxR. UilS confers fitness advantage to S. marcescens, especially in the presence of urea, emphasizing the adaptive plasticity of strains to modulate gene expression based on environmental signals and population density. We also discovered a novel bacterial killing capacity of S. marcescens that involves UilS, indicating its importance in the interspecies interaction of Serratia. Finally, we found that a uilS mutant strain displays attenuated colonization in a mouse model of catheter-associated urinary tract infection. uilS is present in clinical but absent in environmental isolates, suggesting an evolutionary adaptation to host-specific selective pressures.Fil: Tuttobene, Marisel Romina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Arango Gil, Brayan Stiven. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Di Venanzio, Gisela Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. University of Washington; Estados UnidosFil: Mariscotti, Javier Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Sieira, Rodrigo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Feldman, Mario F.. University of Washington; Estados UnidosFil: Ramirez, María Soledad. California State University; Estados UnidosFil: Garcia Vescovi, Eleonora. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaAmerican Society for Microbiology2024-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/266223Tuttobene, Marisel Romina; Arango Gil, Brayan Stiven; Di Venanzio, Gisela Andrea; Mariscotti, Javier Fernando; Sieira, Rodrigo; et al.; Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection; American Society for Microbiology; mBio; 15; 12; 10-2024; 1-232150-7511CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://journals.asm.org/doi/10.1128/mbio.02505-24info:eu-repo/semantics/altIdentifier/doi/10.1128/mbio.02505-24info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:10:38Zoai:ri.conicet.gov.ar:11336/266223instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 10:10:38.875CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
title Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
spellingShingle Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
Tuttobene, Marisel Romina
Serratia
Quorum quenching
Lactonase
Pathogenesis
title_short Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
title_full Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
title_fullStr Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
title_full_unstemmed Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
title_sort Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection
dc.creator.none.fl_str_mv Tuttobene, Marisel Romina
Arango Gil, Brayan Stiven
Di Venanzio, Gisela Andrea
Mariscotti, Javier Fernando
Sieira, Rodrigo
Feldman, Mario F.
Ramirez, María Soledad
Garcia Vescovi, Eleonora
author Tuttobene, Marisel Romina
author_facet Tuttobene, Marisel Romina
Arango Gil, Brayan Stiven
Di Venanzio, Gisela Andrea
Mariscotti, Javier Fernando
Sieira, Rodrigo
Feldman, Mario F.
Ramirez, María Soledad
Garcia Vescovi, Eleonora
author_role author
author2 Arango Gil, Brayan Stiven
Di Venanzio, Gisela Andrea
Mariscotti, Javier Fernando
Sieira, Rodrigo
Feldman, Mario F.
Ramirez, María Soledad
Garcia Vescovi, Eleonora
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Serratia
Quorum quenching
Lactonase
Pathogenesis
topic Serratia
Quorum quenching
Lactonase
Pathogenesis
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Serratia marcescens, a member of the Enterobacteriaceae family, is an opportunistic human pathogen and a frequent cause of urinary tract infections. Clinical isolates often exhibit resistance to multiple antibiotics, posing challenges for successful treatment. Understanding its pathogenic mechanisms is crucial for elucidating new potential targets to develop effective therapeutic interventions and manage S. marcescens infections. This work identifies urea-induced lactonase of Serratia (UilS), a lactonase encoded in the S. marcescens RM66262 strain isolated from a patient with a urinary tract infection. The study explores the bacterium´s response to urea, a major component of urine, and its impact on uilS expression. We found that UilS degrades acyl-homoserine lactones (AHL) autoinducers traditionally associated with quorum sensing mechanisms. Surprisingly, UilS is able to degrade self and non-self AHL, exhibiting quorum-quenching activity toward Pseudomonas aeruginosa. We found that LuxR regulates uilS expression that is enhanced in the presence of AHL. In addition, urea-dependent induction of UilS expression is controlled by the transcriptional response regulator CpxR. UilS confers fitness advantage to S. marcescens, especially in the presence of urea, emphasizing the adaptive plasticity of strains to modulate gene expression based on environmental signals and population density. We also discovered a novel bacterial killing capacity of S. marcescens that involves UilS, indicating its importance in the interspecies interaction of Serratia. Finally, we found that a uilS mutant strain displays attenuated colonization in a mouse model of catheter-associated urinary tract infection. uilS is present in clinical but absent in environmental isolates, suggesting an evolutionary adaptation to host-specific selective pressures.
Fil: Tuttobene, Marisel Romina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Arango Gil, Brayan Stiven. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Di Venanzio, Gisela Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. University of Washington; Estados Unidos
Fil: Mariscotti, Javier Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Sieira, Rodrigo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Feldman, Mario F.. University of Washington; Estados Unidos
Fil: Ramirez, María Soledad. California State University; Estados Unidos
Fil: Garcia Vescovi, Eleonora. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
description Serratia marcescens, a member of the Enterobacteriaceae family, is an opportunistic human pathogen and a frequent cause of urinary tract infections. Clinical isolates often exhibit resistance to multiple antibiotics, posing challenges for successful treatment. Understanding its pathogenic mechanisms is crucial for elucidating new potential targets to develop effective therapeutic interventions and manage S. marcescens infections. This work identifies urea-induced lactonase of Serratia (UilS), a lactonase encoded in the S. marcescens RM66262 strain isolated from a patient with a urinary tract infection. The study explores the bacterium´s response to urea, a major component of urine, and its impact on uilS expression. We found that UilS degrades acyl-homoserine lactones (AHL) autoinducers traditionally associated with quorum sensing mechanisms. Surprisingly, UilS is able to degrade self and non-self AHL, exhibiting quorum-quenching activity toward Pseudomonas aeruginosa. We found that LuxR regulates uilS expression that is enhanced in the presence of AHL. In addition, urea-dependent induction of UilS expression is controlled by the transcriptional response regulator CpxR. UilS confers fitness advantage to S. marcescens, especially in the presence of urea, emphasizing the adaptive plasticity of strains to modulate gene expression based on environmental signals and population density. We also discovered a novel bacterial killing capacity of S. marcescens that involves UilS, indicating its importance in the interspecies interaction of Serratia. Finally, we found that a uilS mutant strain displays attenuated colonization in a mouse model of catheter-associated urinary tract infection. uilS is present in clinical but absent in environmental isolates, suggesting an evolutionary adaptation to host-specific selective pressures.
publishDate 2024
dc.date.none.fl_str_mv 2024-10
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/266223
Tuttobene, Marisel Romina; Arango Gil, Brayan Stiven; Di Venanzio, Gisela Andrea; Mariscotti, Javier Fernando; Sieira, Rodrigo; et al.; Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection; American Society for Microbiology; mBio; 15; 12; 10-2024; 1-23
2150-7511
CONICET Digital
CONICET
url http://hdl.handle.net/11336/266223
identifier_str_mv Tuttobene, Marisel Romina; Arango Gil, Brayan Stiven; Di Venanzio, Gisela Andrea; Mariscotti, Javier Fernando; Sieira, Rodrigo; et al.; Unraveling the role of UilS, a urea-induced acyl-homoserine lactonase that enhances Serratia marcescens fitness, interbacterial competition, and urinary tract infection; American Society for Microbiology; mBio; 15; 12; 10-2024; 1-23
2150-7511
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/doi/10.1128/mbio.02505-24
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
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:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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