Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds

Autores
Juarez, Guillermo Esteban; Mateyca, Andrea Celeste; Galvan, Estela Maria
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Klebsiella pneumoniae and Proteus mirabilis form mixed biofilms in catheter-associated urinary tract infections. However, co-inoculation of P. mirabilis with K. pneumoniae in artificial urine medium (AUM) resulted in a drastic reduction of K. pneumoniae cells in both biofilm and planktonic growth. Here, the mechanism behind this competitive interaction was studied. Both pH and aqueous ammonia (NH3aq) increased in mixed cultures (to 9.3 and 150 mM, respectively), while K. pneumoniae viable cells dramatically diminished over time (>6-log reduction, p < 0.05). Mixed cultures developed in either 2-(N-morpholino) ethanesulfonic acid (MES)-buffered AUM (pH 6.5) or AUM without urea did not show bacterial competition, evidencing that the increase in pH and/or NH3aq concentration play a role in the competitive interaction. Viability of K. pneumoniae single-species cultures decreased 1.5-log in alkaline AUM containing 150 mM NH3aq after 24 h inoculation, suggesting that ammonia is involved in this inter-species competition. Besides NH3aq, additional antimicrobials should be present to get the whole competitive effect. Supernatants from P. mirabilis-containing cultures significantly diminished K. pneumoniae viability in planktonic cultures and affected biofilm biomass (p < 0.05). When subjected to evaporation, these supernatants lost their antimicrobial activity suggesting the volatile nature of the antimicrobial compounds. Exposure of K. pneumoniae to volatile compounds released by P. mirabilis significantly decreased cell viability in both planktonic and biofilm cultures (p < 0.05). The current investigation also evidenced a similar bactericidal effect of P. mirabilis volatiles over Escherichia coli and Morganella morganii. Altogether, these results evidence the secretion of ammonia and other volatile compounds by P. mirabilis, with antimicrobial activity against gram-negative uropathogens including K. pneumoniae. This investigation provides novel insight into competitive inter-species interactions that are mediated by production of volatile molecules.
Fil: Juarez, Guillermo Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Maimónides. Centro de Estudios Biomédicos, Básicos, Aplicados y Desarrollo. Departamento de Ciencias Biológicas y Biomédicas; Argentina
Fil: Mateyca, Andrea Celeste. 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: Galvan, Estela Maria. Universidad Maimónides. Área de Investigaciones Biomédicas y Biotecnológicas. Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y de Diagnóstico; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
ARTIFICIAL URINE MEDIUM
BACTERIA
BIOFILMS
DUAL-SPECIES COMPETITION
KLEBSIELLA PNEUMONIAE
METABOLITE
MICROBIOLOGY
PROTEUS MIRABILIS
VOLATILE COMPOUNDS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/131037
Acceder
id CONICETDig_7df447890514c609c14f37a6bda6259d
oai_identifier_str oai:ri.conicet.gov.ar:11336/131037
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compoundsJuarez, Guillermo EstebanMateyca, Andrea CelesteGalvan, Estela MariaARTIFICIAL URINE MEDIUMBACTERIABIOFILMSDUAL-SPECIES COMPETITIONKLEBSIELLA PNEUMONIAEMETABOLITEMICROBIOLOGYPROTEUS MIRABILISVOLATILE COMPOUNDShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Klebsiella pneumoniae and Proteus mirabilis form mixed biofilms in catheter-associated urinary tract infections. However, co-inoculation of P. mirabilis with K. pneumoniae in artificial urine medium (AUM) resulted in a drastic reduction of K. pneumoniae cells in both biofilm and planktonic growth. Here, the mechanism behind this competitive interaction was studied. Both pH and aqueous ammonia (NH3aq) increased in mixed cultures (to 9.3 and 150 mM, respectively), while K. pneumoniae viable cells dramatically diminished over time (>6-log reduction, p < 0.05). Mixed cultures developed in either 2-(N-morpholino) ethanesulfonic acid (MES)-buffered AUM (pH 6.5) or AUM without urea did not show bacterial competition, evidencing that the increase in pH and/or NH3aq concentration play a role in the competitive interaction. Viability of K. pneumoniae single-species cultures decreased 1.5-log in alkaline AUM containing 150 mM NH3aq after 24 h inoculation, suggesting that ammonia is involved in this inter-species competition. Besides NH3aq, additional antimicrobials should be present to get the whole competitive effect. Supernatants from P. mirabilis-containing cultures significantly diminished K. pneumoniae viability in planktonic cultures and affected biofilm biomass (p < 0.05). When subjected to evaporation, these supernatants lost their antimicrobial activity suggesting the volatile nature of the antimicrobial compounds. Exposure of K. pneumoniae to volatile compounds released by P. mirabilis significantly decreased cell viability in both planktonic and biofilm cultures (p < 0.05). The current investigation also evidenced a similar bactericidal effect of P. mirabilis volatiles over Escherichia coli and Morganella morganii. Altogether, these results evidence the secretion of ammonia and other volatile compounds by P. mirabilis, with antimicrobial activity against gram-negative uropathogens including K. pneumoniae. This investigation provides novel insight into competitive inter-species interactions that are mediated by production of volatile molecules.Fil: Juarez, Guillermo Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Maimónides. Centro de Estudios Biomédicos, Básicos, Aplicados y Desarrollo. Departamento de Ciencias Biológicas y Biomédicas; ArgentinaFil: Mateyca, Andrea Celeste. 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: Galvan, Estela Maria. Universidad Maimónides. Área de Investigaciones Biomédicas y Biotecnológicas. Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y de Diagnóstico; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaElsevier2020-02info: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/11336/131037Juarez, Guillermo Esteban; Mateyca, Andrea Celeste; Galvan, Estela Maria; Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds; Elsevier; Heliyon; 6; 2; 2-2020; 1-92405-8440CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S2405844020302061info:eu-repo/semantics/altIdentifier/doi/10.1016/j.heliyon.2020.e03361info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:09:42Zoai:ri.conicet.gov.ar:11336/131037instacron: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 10:09:43.119CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
title Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
spellingShingle Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
Juarez, Guillermo Esteban
ARTIFICIAL URINE MEDIUM
BACTERIA
BIOFILMS
DUAL-SPECIES COMPETITION
KLEBSIELLA PNEUMONIAE
METABOLITE
MICROBIOLOGY
PROTEUS MIRABILIS
VOLATILE COMPOUNDS
title_short Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
title_full Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
title_fullStr Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
title_full_unstemmed Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
title_sort Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds
dc.creator.none.fl_str_mv Juarez, Guillermo Esteban
Mateyca, Andrea Celeste
Galvan, Estela Maria
author Juarez, Guillermo Esteban
author_facet Juarez, Guillermo Esteban
Mateyca, Andrea Celeste
Galvan, Estela Maria
author_role author
author2 Mateyca, Andrea Celeste
Galvan, Estela Maria
author2_role author
author
dc.subject.none.fl_str_mv ARTIFICIAL URINE MEDIUM
BACTERIA
BIOFILMS
DUAL-SPECIES COMPETITION
KLEBSIELLA PNEUMONIAE
METABOLITE
MICROBIOLOGY
PROTEUS MIRABILIS
VOLATILE COMPOUNDS
topic ARTIFICIAL URINE MEDIUM
BACTERIA
BIOFILMS
DUAL-SPECIES COMPETITION
KLEBSIELLA PNEUMONIAE
METABOLITE
MICROBIOLOGY
PROTEUS MIRABILIS
VOLATILE COMPOUNDS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Klebsiella pneumoniae and Proteus mirabilis form mixed biofilms in catheter-associated urinary tract infections. However, co-inoculation of P. mirabilis with K. pneumoniae in artificial urine medium (AUM) resulted in a drastic reduction of K. pneumoniae cells in both biofilm and planktonic growth. Here, the mechanism behind this competitive interaction was studied. Both pH and aqueous ammonia (NH3aq) increased in mixed cultures (to 9.3 and 150 mM, respectively), while K. pneumoniae viable cells dramatically diminished over time (>6-log reduction, p < 0.05). Mixed cultures developed in either 2-(N-morpholino) ethanesulfonic acid (MES)-buffered AUM (pH 6.5) or AUM without urea did not show bacterial competition, evidencing that the increase in pH and/or NH3aq concentration play a role in the competitive interaction. Viability of K. pneumoniae single-species cultures decreased 1.5-log in alkaline AUM containing 150 mM NH3aq after 24 h inoculation, suggesting that ammonia is involved in this inter-species competition. Besides NH3aq, additional antimicrobials should be present to get the whole competitive effect. Supernatants from P. mirabilis-containing cultures significantly diminished K. pneumoniae viability in planktonic cultures and affected biofilm biomass (p < 0.05). When subjected to evaporation, these supernatants lost their antimicrobial activity suggesting the volatile nature of the antimicrobial compounds. Exposure of K. pneumoniae to volatile compounds released by P. mirabilis significantly decreased cell viability in both planktonic and biofilm cultures (p < 0.05). The current investigation also evidenced a similar bactericidal effect of P. mirabilis volatiles over Escherichia coli and Morganella morganii. Altogether, these results evidence the secretion of ammonia and other volatile compounds by P. mirabilis, with antimicrobial activity against gram-negative uropathogens including K. pneumoniae. This investigation provides novel insight into competitive inter-species interactions that are mediated by production of volatile molecules.
Fil: Juarez, Guillermo Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Maimónides. Centro de Estudios Biomédicos, Básicos, Aplicados y Desarrollo. Departamento de Ciencias Biológicas y Biomédicas; Argentina
Fil: Mateyca, Andrea Celeste. 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: Galvan, Estela Maria. Universidad Maimónides. Área de Investigaciones Biomédicas y Biotecnológicas. Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y de Diagnóstico; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Klebsiella pneumoniae and Proteus mirabilis form mixed biofilms in catheter-associated urinary tract infections. However, co-inoculation of P. mirabilis with K. pneumoniae in artificial urine medium (AUM) resulted in a drastic reduction of K. pneumoniae cells in both biofilm and planktonic growth. Here, the mechanism behind this competitive interaction was studied. Both pH and aqueous ammonia (NH3aq) increased in mixed cultures (to 9.3 and 150 mM, respectively), while K. pneumoniae viable cells dramatically diminished over time (>6-log reduction, p < 0.05). Mixed cultures developed in either 2-(N-morpholino) ethanesulfonic acid (MES)-buffered AUM (pH 6.5) or AUM without urea did not show bacterial competition, evidencing that the increase in pH and/or NH3aq concentration play a role in the competitive interaction. Viability of K. pneumoniae single-species cultures decreased 1.5-log in alkaline AUM containing 150 mM NH3aq after 24 h inoculation, suggesting that ammonia is involved in this inter-species competition. Besides NH3aq, additional antimicrobials should be present to get the whole competitive effect. Supernatants from P. mirabilis-containing cultures significantly diminished K. pneumoniae viability in planktonic cultures and affected biofilm biomass (p < 0.05). When subjected to evaporation, these supernatants lost their antimicrobial activity suggesting the volatile nature of the antimicrobial compounds. Exposure of K. pneumoniae to volatile compounds released by P. mirabilis significantly decreased cell viability in both planktonic and biofilm cultures (p < 0.05). The current investigation also evidenced a similar bactericidal effect of P. mirabilis volatiles over Escherichia coli and Morganella morganii. Altogether, these results evidence the secretion of ammonia and other volatile compounds by P. mirabilis, with antimicrobial activity against gram-negative uropathogens including K. pneumoniae. This investigation provides novel insight into competitive inter-species interactions that are mediated by production of volatile molecules.
publishDate 2020
dc.date.none.fl_str_mv 2020-02
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/11336/131037
Juarez, Guillermo Esteban; Mateyca, Andrea Celeste; Galvan, Estela Maria; Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds; Elsevier; Heliyon; 6; 2; 2-2020; 1-9
2405-8440
CONICET Digital
CONICET
url http://hdl.handle.net/11336/131037
identifier_str_mv Juarez, Guillermo Esteban; Mateyca, Andrea Celeste; Galvan, Estela Maria; Proteus mirabilis outcompetes Klebsiella pneumoniae in artificial urine medium through secretion of ammonia and other volatile compounds; Elsevier; Heliyon; 6; 2; 2-2020; 1-9
2405-8440
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S2405844020302061
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.heliyon.2020.e03361
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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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score 13.13397

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