Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice

Bacteria can be motile and planktonic or, alteRNAtively, sessile and participating in the biofilm mode of growth. The transition between these lifestyles can be regulated by a second messenger, cyclic dimeric GMP (c-di-GMP). High intracellular c-di-GMP concentration correlates with biofilm formation...

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Autores: Belhart, Keila, Gutierrez, María de la Paz, Zacca, Federico Hernán, Ambrosis, Nicolás Martín, Gestal, Monica Cartelle, Taylor, Dawn, Dahlstrom, Kurt M., Harvill, Eric T., O Toole, George, Sisti, Federico Bernardo, Fernandez, Julieta
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:Argentina
Institución:Consejo Nacional de Investigaciones Científicas y Técnicas
Repositorio:CONICET Digital (CONICET)
Idioma:inglés
OAI Identifier:oai:ri.conicet.gov.ar:11336/180847
Acceso en línea:http://hdl.handle.net/11336/180847
Access Level:acceso abierto
Palabra clave:BIOFILM
BORDETELLA
C-DI-GMP
MOTILITY
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
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oai_identifier_str oai:ri.conicet.gov.ar:11336/180847
network_acronym_str AR
network_name_str Argentina
repository_id_str
dc.title.none.fl_str_mv Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
title Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
spellingShingle Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
Belhart, Keila
BIOFILM
BORDETELLA
C-DI-GMP
MOTILITY
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
title_short Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
title_full Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
title_fullStr Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
title_full_unstemmed Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
title_sort Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice
dc.creator.none.fl_str_mv Belhart, Keila
Gutierrez, María de la Paz
Zacca, Federico Hernán
Ambrosis, Nicolás Martín
Gestal, Monica Cartelle
Taylor, Dawn
Dahlstrom, Kurt M.
Harvill, Eric T.
O Toole, George
Sisti, Federico Bernardo
Fernandez, Julieta
author Belhart, Keila
author_facet Belhart, Keila
Gutierrez, María de la Paz
Zacca, Federico Hernán
Ambrosis, Nicolás Martín
Gestal, Monica Cartelle
Taylor, Dawn
Dahlstrom, Kurt M.
Harvill, Eric T.
O Toole, George
Sisti, Federico Bernardo
Fernandez, Julieta
author_role author
author2 Gutierrez, María de la Paz
Zacca, Federico Hernán
Ambrosis, Nicolás Martín
Gestal, Monica Cartelle
Taylor, Dawn
Dahlstrom, Kurt M.
Harvill, Eric T.
O Toole, George
Sisti, Federico Bernardo
Fernandez, Julieta
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv BIOFILM
BORDETELLA
C-DI-GMP
MOTILITY
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
topic BIOFILM
BORDETELLA
C-DI-GMP
MOTILITY
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
description Bacteria can be motile and planktonic or, alteRNAtively, sessile and participating in the biofilm mode of growth. The transition between these lifestyles can be regulated by a second messenger, cyclic dimeric GMP (c-di-GMP). High intracellular c-di-GMP concentration correlates with biofilm formation and motility inhibition in most bacteria, including Bordetella bronchiseptica, which causes respiratory tract infections in mammals and forms biofilms in infected mice. We previously described the diguanylate cyclase BdcA as involved in c-di-GMP synthesis and motility regulation in B. bronchiseptica; here, we further describe the mechanism whereby BdcA is able to regulate motility and biofilm formation. Amino acid replacement of GGDEF with GGAAF in BdcA is consistent with the conclusion that diguanylate cyclase activity is necessary for biofilm formation and motility regulation, although we were unable to confirm the stability of the mutant protein. In the absence of the bdcA gene, B. bronchiseptica showed enhanced motility, strengthening the hypothesis that BdcA regulates motility in B. bronchiseptica. We showed that c-di-GMP-mediated motility inhibition involved regulation of flagellin expression, as high c-di-GMP levels achieved by expressing BdcA significantly reduced the level of flagellin protein. We also demonstrated that protein BB2109 is necessary for BdcA activity, motility inhibition, and biofilm formation. Finally, absence of the bdcA gene affected bacterial infection, implicating BdcA-regulated functions as important for bacterium-host interactions. This work supports the role of c-di-GMP in biofilm formation and motility regulation in B. bronchiseptica, as well as its impact on pathogenesis. IMPORTANCE Pathogenesis of Bordetella spp., like that of a number of other pathogens, involves biofilm formation. Biofilms increase tolerance to biotic and abiotic factors and are proposed as reservoirs of microbes for transmission to other organs (trachea, lungs) or other hosts. Bis-(3=-5=)-cyclic dimeric GMP (c-di-GMP) is a second messenger that regulates transition between biofilm and planktonic lifestyles. In Bordetella bronchiseptica, high c-di-GMP levels inhibit motility and favor biofilm formation. In the present work, we characterized a B. bronchiseptica diguanylate cyclase, BdcA, which regulates motility and biofilm formation and affects the ability of B. bronchiseptica to colonize the murine respiratory tract. These results provide us with a better understanding of how B. bronchiseptica can infect a host.
publishDate 2019
dc.date.none.fl_str_mv 2019-06
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/11336/180847
Belhart, Keila; Gutierrez, María de la Paz; Zacca, Federico Hernán; Ambrosis, Nicolás Martín; Gestal, Monica Cartelle; et al.; Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice; American Society for Microbiology; Journal of Bacteriology; 201; 17; 6-2019; 1-31
0021-9193
CONICET Digital
CONICET
url http://hdl.handle.net/11336/180847
identifier_str_mv Belhart, Keila; Gutierrez, María de la Paz; Zacca, Federico Hernán; Ambrosis, Nicolás Martín; Gestal, Monica Cartelle; et al.; Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice; American Society for Microbiology; Journal of Bacteriology; 201; 17; 6-2019; 1-31
0021-9193
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://journals.asm.org/doi/10.1128/JB.00011-19
info:eu-repo/semantics/altIdentifier/doi/10.1128/JB.00011-19
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
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:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
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
_version_ 1799195686479069184
spelling Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in miceBelhart, KeilaGutierrez, María de la PazZacca, Federico HernánAmbrosis, Nicolás MartínGestal, Monica CartelleTaylor, DawnDahlstrom, Kurt M.Harvill, Eric T.O Toole, GeorgeSisti, Federico BernardoFernandez, JulietaBIOFILMBORDETELLAC-DI-GMPMOTILITYhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Bacteria can be motile and planktonic or, alteRNAtively, sessile and participating in the biofilm mode of growth. The transition between these lifestyles can be regulated by a second messenger, cyclic dimeric GMP (c-di-GMP). High intracellular c-di-GMP concentration correlates with biofilm formation and motility inhibition in most bacteria, including Bordetella bronchiseptica, which causes respiratory tract infections in mammals and forms biofilms in infected mice. We previously described the diguanylate cyclase BdcA as involved in c-di-GMP synthesis and motility regulation in B. bronchiseptica; here, we further describe the mechanism whereby BdcA is able to regulate motility and biofilm formation. Amino acid replacement of GGDEF with GGAAF in BdcA is consistent with the conclusion that diguanylate cyclase activity is necessary for biofilm formation and motility regulation, although we were unable to confirm the stability of the mutant protein. In the absence of the bdcA gene, B. bronchiseptica showed enhanced motility, strengthening the hypothesis that BdcA regulates motility in B. bronchiseptica. We showed that c-di-GMP-mediated motility inhibition involved regulation of flagellin expression, as high c-di-GMP levels achieved by expressing BdcA significantly reduced the level of flagellin protein. We also demonstrated that protein BB2109 is necessary for BdcA activity, motility inhibition, and biofilm formation. Finally, absence of the bdcA gene affected bacterial infection, implicating BdcA-regulated functions as important for bacterium-host interactions. This work supports the role of c-di-GMP in biofilm formation and motility regulation in B. bronchiseptica, as well as its impact on pathogenesis. IMPORTANCE Pathogenesis of Bordetella spp., like that of a number of other pathogens, involves biofilm formation. Biofilms increase tolerance to biotic and abiotic factors and are proposed as reservoirs of microbes for transmission to other organs (trachea, lungs) or other hosts. Bis-(3=-5=)-cyclic dimeric GMP (c-di-GMP) is a second messenger that regulates transition between biofilm and planktonic lifestyles. In Bordetella bronchiseptica, high c-di-GMP levels inhibit motility and favor biofilm formation. In the present work, we characterized a B. bronchiseptica diguanylate cyclase, BdcA, which regulates motility and biofilm formation and affects the ability of B. bronchiseptica to colonize the murine respiratory tract. These results provide us with a better understanding of how B. bronchiseptica can infect a host.Fil: Belhart, Keila. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaFil: Gutierrez, María de la Paz. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaFil: Zacca, Federico Hernán. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaFil: Ambrosis, Nicolás Martín. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaFil: Gestal, Monica Cartelle. Georgia State University; Estados UnidosFil: Taylor, Dawn. Georgia State University; Estados UnidosFil: Dahlstrom, Kurt M.. Geisel School of Medicine at Dartmouth; Estados UnidosFil: Harvill, Eric T.. Georgia State University; Estados UnidosFil: O Toole, George. Geisel School of Medicine at Dartmouth; Estados UnidosFil: Sisti, Federico Bernardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaFil: Fernandez, Julieta. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaAmerican Society for Microbiology2019-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/180847Belhart, Keila; Gutierrez, María de la Paz; Zacca, Federico Hernán; Ambrosis, Nicolás Martín; Gestal, Monica Cartelle; et al.; Bordetella bronchiseptica diguanylate cyclase bdca regulates motility and is important for the establishment of respiratory infection in mice; American Society for Microbiology; Journal of Bacteriology; 201; 17; 6-2019; 1-310021-9193CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://journals.asm.org/doi/10.1128/JB.00011-19info:eu-repo/semantics/altIdentifier/doi/10.1128/JB.00011-19info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2024-05-08T14:00:21Zoai:ri.conicet.gov.ar:11336/180847instacron: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:34982024-05-08 14:00:21.467CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
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