The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation

Autores
Guragain, Manita; Jennings-Gee, Jamie; Cattelan, Natalia; Finger, Mary; Conover, Matt S.; Hollis, Thomas; Deora, Rajendar
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Many of the pathogenic species of the genus Bordetella have an absolute requirement for nicotinic acid (NA) for laboratory growth. These Gram-negative bacteria also harbor a gene cluster homologous to the nic cluster of Pseudomonas putida which is involved in the aerobic degradation of NA and its transcriptional control. We report here that BpsR, a negative regulator of biofilm formation and Bps polysaccharide production, controls the growth of Bordetella bronchiseptica by repressing the expression of nic genes. The severe growth defect of the ΔbpsR strain in Stainer-Scholte medium was restored by supplementation with NA, which also functioned as an inducer of nic genes at low micromolar concentrations that are usually present in animals and humans. Purified BpsR protein bound to the nic promoter region, and its DNA binding activity was inhibited by 6-hydroxynicotinic acid (6-HNA), the first metabolite of the NA degradative pathway. Reporter assays with the isogenic mutant derivative of the wild-type (WT) strain harboring deletion in nicA, which encodes a putative nicotinic acid hydroxylase responsible for conversion of NA to 6-HNA, showed that 6-HNA is the actual inducer of the nic genes in the bacterial cell. Gene expression profiling further showed that BpsR dually activated and repressed the expression of genes associated with pathogenesis, transcriptional regulation, metabolism, and other cellular processes. We discuss the implications of these findings with respect to the selection of pyridines such as NA and quinolinic acid for optimum bacterial growth depending on the ecological niche.
Centro de Investigación y Desarrollo en Fermentaciones Industriales
Materia
Ciencias Exactas
Bordetella
metabolism
transcriptional regulation
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
SEDICI (UNLP)
Institución
Universidad Nacional de La Plata
OAI Identificador
oai:sedici.unlp.edu.ar:10915/107997
Acceder
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network_acronym_str SEDICI
repository_id_str 1329
network_name_str SEDICI (UNLP)
spelling The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid DegradationGuragain, ManitaJennings-Gee, JamieCattelan, NataliaFinger, MaryConover, Matt S.Hollis, ThomasDeora, RajendarCiencias ExactasBordetellametabolismtranscriptional regulationMany of the pathogenic species of the genus Bordetella have an absolute requirement for nicotinic acid (NA) for laboratory growth. These Gram-negative bacteria also harbor a gene cluster homologous to the nic cluster of Pseudomonas putida which is involved in the aerobic degradation of NA and its transcriptional control. We report here that BpsR, a negative regulator of biofilm formation and Bps polysaccharide production, controls the growth of Bordetella bronchiseptica by repressing the expression of nic genes. The severe growth defect of the ΔbpsR strain in Stainer-Scholte medium was restored by supplementation with NA, which also functioned as an inducer of nic genes at low micromolar concentrations that are usually present in animals and humans. Purified BpsR protein bound to the nic promoter region, and its DNA binding activity was inhibited by 6-hydroxynicotinic acid (6-HNA), the first metabolite of the NA degradative pathway. Reporter assays with the isogenic mutant derivative of the wild-type (WT) strain harboring deletion in nicA, which encodes a putative nicotinic acid hydroxylase responsible for conversion of NA to 6-HNA, showed that 6-HNA is the actual inducer of the nic genes in the bacterial cell. Gene expression profiling further showed that BpsR dually activated and repressed the expression of genes associated with pathogenesis, transcriptional regulation, metabolism, and other cellular processes. We discuss the implications of these findings with respect to the selection of pyridines such as NA and quinolinic acid for optimum bacterial growth depending on the ecological niche.Centro de Investigación y Desarrollo en Fermentaciones Industriales2018info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionArticulohttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://sedici.unlp.edu.ar/handle/10915/107997enginfo:eu-repo/semantics/altIdentifier/url/http://europepmc.org/backend/ptpmcrender.fcgi?accid=PMC5971473&blobtype=pdfinfo:eu-repo/semantics/altIdentifier/issn/1098-5530info:eu-repo/semantics/altIdentifier/pmid/29581411info:eu-repo/semantics/altIdentifier/doi/10.1128/jb.00712-17info:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)reponame:SEDICI (UNLP)instname:Universidad Nacional de La Platainstacron:UNLP2025-09-29T11:23:52Zoai:sedici.unlp.edu.ar:10915/107997Institucionalhttp://sedici.unlp.edu.ar/Universidad públicaNo correspondehttp://sedici.unlp.edu.ar/oai/snrdalira@sedici.unlp.edu.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:13292025-09-29 11:23:53.105SEDICI (UNLP) - Universidad Nacional de La Platafalse
dc.title.none.fl_str_mv The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
title The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
spellingShingle The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
Guragain, Manita
Ciencias Exactas
Bordetella
metabolism
transcriptional regulation
title_short The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
title_full The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
title_fullStr The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
title_full_unstemmed The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
title_sort The Transcriptional Regulator BpsR Controls the Growth of <i>Bordetella bronchiseptica</i> by Repressing Genes Involved in Nicotinic Acid Degradation
dc.creator.none.fl_str_mv Guragain, Manita
Jennings-Gee, Jamie
Cattelan, Natalia
Finger, Mary
Conover, Matt S.
Hollis, Thomas
Deora, Rajendar
author Guragain, Manita
author_facet Guragain, Manita
Jennings-Gee, Jamie
Cattelan, Natalia
Finger, Mary
Conover, Matt S.
Hollis, Thomas
Deora, Rajendar
author_role author
author2 Jennings-Gee, Jamie
Cattelan, Natalia
Finger, Mary
Conover, Matt S.
Hollis, Thomas
Deora, Rajendar
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Ciencias Exactas
Bordetella
metabolism
transcriptional regulation
topic Ciencias Exactas
Bordetella
metabolism
transcriptional regulation
dc.description.none.fl_txt_mv Many of the pathogenic species of the genus Bordetella have an absolute requirement for nicotinic acid (NA) for laboratory growth. These Gram-negative bacteria also harbor a gene cluster homologous to the nic cluster of Pseudomonas putida which is involved in the aerobic degradation of NA and its transcriptional control. We report here that BpsR, a negative regulator of biofilm formation and Bps polysaccharide production, controls the growth of Bordetella bronchiseptica by repressing the expression of nic genes. The severe growth defect of the ΔbpsR strain in Stainer-Scholte medium was restored by supplementation with NA, which also functioned as an inducer of nic genes at low micromolar concentrations that are usually present in animals and humans. Purified BpsR protein bound to the nic promoter region, and its DNA binding activity was inhibited by 6-hydroxynicotinic acid (6-HNA), the first metabolite of the NA degradative pathway. Reporter assays with the isogenic mutant derivative of the wild-type (WT) strain harboring deletion in nicA, which encodes a putative nicotinic acid hydroxylase responsible for conversion of NA to 6-HNA, showed that 6-HNA is the actual inducer of the nic genes in the bacterial cell. Gene expression profiling further showed that BpsR dually activated and repressed the expression of genes associated with pathogenesis, transcriptional regulation, metabolism, and other cellular processes. We discuss the implications of these findings with respect to the selection of pyridines such as NA and quinolinic acid for optimum bacterial growth depending on the ecological niche.
Centro de Investigación y Desarrollo en Fermentaciones Industriales
description Many of the pathogenic species of the genus Bordetella have an absolute requirement for nicotinic acid (NA) for laboratory growth. These Gram-negative bacteria also harbor a gene cluster homologous to the nic cluster of Pseudomonas putida which is involved in the aerobic degradation of NA and its transcriptional control. We report here that BpsR, a negative regulator of biofilm formation and Bps polysaccharide production, controls the growth of Bordetella bronchiseptica by repressing the expression of nic genes. The severe growth defect of the ΔbpsR strain in Stainer-Scholte medium was restored by supplementation with NA, which also functioned as an inducer of nic genes at low micromolar concentrations that are usually present in animals and humans. Purified BpsR protein bound to the nic promoter region, and its DNA binding activity was inhibited by 6-hydroxynicotinic acid (6-HNA), the first metabolite of the NA degradative pathway. Reporter assays with the isogenic mutant derivative of the wild-type (WT) strain harboring deletion in nicA, which encodes a putative nicotinic acid hydroxylase responsible for conversion of NA to 6-HNA, showed that 6-HNA is the actual inducer of the nic genes in the bacterial cell. Gene expression profiling further showed that BpsR dually activated and repressed the expression of genes associated with pathogenesis, transcriptional regulation, metabolism, and other cellular processes. We discuss the implications of these findings with respect to the selection of pyridines such as NA and quinolinic acid for optimum bacterial growth depending on the ecological niche.
publishDate 2018
dc.date.none.fl_str_mv 2018
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
Articulo
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://sedici.unlp.edu.ar/handle/10915/107997
url http://sedici.unlp.edu.ar/handle/10915/107997
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/issn/1098-5530
info:eu-repo/semantics/altIdentifier/pmid/29581411
info:eu-repo/semantics/altIdentifier/doi/10.1128/jb.00712-17
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:SEDICI (UNLP)
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reponame_str SEDICI (UNLP)
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instname_str Universidad Nacional de La Plata
instacron_str UNLP
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repository.name.fl_str_mv SEDICI (UNLP) - Universidad Nacional de La Plata
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