A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibiti...

Autores
Pérez Giménez, Julieta; Iturralde, Esteban Tomás; Torres Tejerizo, Gonzalo Arturo; Quelas, Juan Ignacio; Krol, Elizaveta; Borassi, Cecilia; Becker, Anke; Estevez, Jose Manuel; Lodeiro, Anibal
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
When subjected to nutritional stress, bacteria modify their amino acid metabolism and cell division activities by means of the stringent response, which is controlled by the Rsh protein in alphaproteobacteria. An important group of alphaproteobacteria are the rhizobia, which fix atmospheric N2 in symbiosis with legume plants. Although nutritional stress is common for rhizobia while infecting legume roots, the stringent response was scarcely studied in this group of soil bacteria. In this report, we obtained a mutant in the rsh gene of Bradyrhizobium diazoefficiens, the N2-fixing symbiont of soybean. This mutant was defective for type-3-secretion system induction, plant-defense suppression at early root infection, and competition for nodulation. Furthermore, the mutant produced smaller nodules, although with normal morphology, which lead to lower plant biomass production. Soybean genes GmRIC1 and GmRIC2, involved in autoregulation of nodulation, were upregulated in plants inoculated with the mutant in N-free condition. In addition, when plants were inoculated in the presence of 10 mM NH4NO3, the mutant produced nodules containing bacteroids, and GmRIC1 and GmRIC2 were downregulated. The rsh mutant released more auxin to the culture supernatant than the wild type, which might in part explain its symbiotic behavior in the presence of combined-N. These results indicate that B. diazoefficiens stringent response integrates into the plant defense suppression and regulation of nodulation circuits in soybean, perhaps mediated by the type-3-secretion system.IMPORTANCE The symbiotic N2 fixation carried out between prokaryotic rhizobia and legume plants performs a substantial contribution to the N-cycle in the biosphere. This symbiotic association is initiated when rhizobia infect and penetrate the root hairs, which is followed by the growth and development of root nodules within which the infective rhizobia are established and protected. Thus, the nodule environment allows the expression and function of the enzyme complex that catalyzes N2 fixation. However, during early infection the rhizobia find a harsh environment while penetrating the root hairs. To cope with this nuisance, the rhizobia mount a stress response known as stringent response. In turn, the plant regulates nodulation in response to the presence of alternative sources of combined-N in the surrounding medium. Control of these processes is crucial for a successful symbiosis, and here we show how the rhizobial stringent response may modulate plant defense suppression and the networks of regulation of nodulation.
Fil: Pérez Giménez, 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; Argentina
Fil: Iturralde, Esteban Tomás. 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; Argentina
Fil: Torres Tejerizo, Gonzalo Arturo. 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; Argentina
Fil: Quelas, Juan Ignacio. 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; Argentina
Fil: Krol, Elizaveta. Philipps-Universität Marburg; Alemania
Fil: Borassi, Cecilia. 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: Becker, Anke. Philipps-Universität Marburg; Alemania
Fil: Estevez, Jose Manuel. 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. Universidad Andrés Bello; Chile
Fil: Lodeiro, Anibal. 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; Argentina
Materia
BRADYRHIZOBIUM DIAZOEFFICIENS
STRINGENT RESPONSE
PLANT DEFENSE
SYMBIOSIS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/155931

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network_name_str CONICET Digital (CONICET)
spelling A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulationPérez Giménez, JulietaIturralde, Esteban TomásTorres Tejerizo, Gonzalo ArturoQuelas, Juan IgnacioKrol, ElizavetaBorassi, CeciliaBecker, AnkeEstevez, Jose ManuelLodeiro, AnibalBRADYRHIZOBIUM DIAZOEFFICIENSSTRINGENT RESPONSEPLANT DEFENSESYMBIOSIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1When subjected to nutritional stress, bacteria modify their amino acid metabolism and cell division activities by means of the stringent response, which is controlled by the Rsh protein in alphaproteobacteria. An important group of alphaproteobacteria are the rhizobia, which fix atmospheric N2 in symbiosis with legume plants. Although nutritional stress is common for rhizobia while infecting legume roots, the stringent response was scarcely studied in this group of soil bacteria. In this report, we obtained a mutant in the rsh gene of Bradyrhizobium diazoefficiens, the N2-fixing symbiont of soybean. This mutant was defective for type-3-secretion system induction, plant-defense suppression at early root infection, and competition for nodulation. Furthermore, the mutant produced smaller nodules, although with normal morphology, which lead to lower plant biomass production. Soybean genes GmRIC1 and GmRIC2, involved in autoregulation of nodulation, were upregulated in plants inoculated with the mutant in N-free condition. In addition, when plants were inoculated in the presence of 10 mM NH4NO3, the mutant produced nodules containing bacteroids, and GmRIC1 and GmRIC2 were downregulated. The rsh mutant released more auxin to the culture supernatant than the wild type, which might in part explain its symbiotic behavior in the presence of combined-N. These results indicate that B. diazoefficiens stringent response integrates into the plant defense suppression and regulation of nodulation circuits in soybean, perhaps mediated by the type-3-secretion system.IMPORTANCE The symbiotic N2 fixation carried out between prokaryotic rhizobia and legume plants performs a substantial contribution to the N-cycle in the biosphere. This symbiotic association is initiated when rhizobia infect and penetrate the root hairs, which is followed by the growth and development of root nodules within which the infective rhizobia are established and protected. Thus, the nodule environment allows the expression and function of the enzyme complex that catalyzes N2 fixation. However, during early infection the rhizobia find a harsh environment while penetrating the root hairs. To cope with this nuisance, the rhizobia mount a stress response known as stringent response. In turn, the plant regulates nodulation in response to the presence of alternative sources of combined-N in the surrounding medium. Control of these processes is crucial for a successful symbiosis, and here we show how the rhizobial stringent response may modulate plant defense suppression and the networks of regulation of nodulation.Fil: Pérez Giménez, 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; ArgentinaFil: Iturralde, Esteban Tomás. 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: Torres Tejerizo, Gonzalo Arturo. 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: Quelas, Juan Ignacio. 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: Krol, Elizaveta. Philipps-Universität Marburg; AlemaniaFil: Borassi, Cecilia. 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: Becker, Anke. Philipps-Universität Marburg; AlemaniaFil: Estevez, Jose Manuel. 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. Universidad Andrés Bello; ChileFil: Lodeiro, Anibal. 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 Microbiology2021-04-13info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/155931Pérez Giménez, Julieta; Iturralde, Esteban Tomás; Torres Tejerizo, Gonzalo Arturo; Quelas, Juan Ignacio; Krol, Elizaveta; et al.; A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation; American Society for Microbiology; Applied and Environmental Microbiology; 87; 9; 13-4-2021; 1-140099-2240CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://aem.asm.org/lookup/doi/10.1128/AEM.02989-20info:eu-repo/semantics/altIdentifier/doi/10.1128/AEM.02989-20info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:00:51Zoai:ri.conicet.gov.ar:11336/155931instacron: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 10:00:51.812CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
title A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
spellingShingle A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
Pérez Giménez, Julieta
BRADYRHIZOBIUM DIAZOEFFICIENS
STRINGENT RESPONSE
PLANT DEFENSE
SYMBIOSIS
title_short A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
title_full A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
title_fullStr A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
title_full_unstemmed A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
title_sort A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation
dc.creator.none.fl_str_mv Pérez Giménez, Julieta
Iturralde, Esteban Tomás
Torres Tejerizo, Gonzalo Arturo
Quelas, Juan Ignacio
Krol, Elizaveta
Borassi, Cecilia
Becker, Anke
Estevez, Jose Manuel
Lodeiro, Anibal
author Pérez Giménez, Julieta
author_facet Pérez Giménez, Julieta
Iturralde, Esteban Tomás
Torres Tejerizo, Gonzalo Arturo
Quelas, Juan Ignacio
Krol, Elizaveta
Borassi, Cecilia
Becker, Anke
Estevez, Jose Manuel
Lodeiro, Anibal
author_role author
author2 Iturralde, Esteban Tomás
Torres Tejerizo, Gonzalo Arturo
Quelas, Juan Ignacio
Krol, Elizaveta
Borassi, Cecilia
Becker, Anke
Estevez, Jose Manuel
Lodeiro, Anibal
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv BRADYRHIZOBIUM DIAZOEFFICIENS
STRINGENT RESPONSE
PLANT DEFENSE
SYMBIOSIS
topic BRADYRHIZOBIUM DIAZOEFFICIENS
STRINGENT RESPONSE
PLANT DEFENSE
SYMBIOSIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv When subjected to nutritional stress, bacteria modify their amino acid metabolism and cell division activities by means of the stringent response, which is controlled by the Rsh protein in alphaproteobacteria. An important group of alphaproteobacteria are the rhizobia, which fix atmospheric N2 in symbiosis with legume plants. Although nutritional stress is common for rhizobia while infecting legume roots, the stringent response was scarcely studied in this group of soil bacteria. In this report, we obtained a mutant in the rsh gene of Bradyrhizobium diazoefficiens, the N2-fixing symbiont of soybean. This mutant was defective for type-3-secretion system induction, plant-defense suppression at early root infection, and competition for nodulation. Furthermore, the mutant produced smaller nodules, although with normal morphology, which lead to lower plant biomass production. Soybean genes GmRIC1 and GmRIC2, involved in autoregulation of nodulation, were upregulated in plants inoculated with the mutant in N-free condition. In addition, when plants were inoculated in the presence of 10 mM NH4NO3, the mutant produced nodules containing bacteroids, and GmRIC1 and GmRIC2 were downregulated. The rsh mutant released more auxin to the culture supernatant than the wild type, which might in part explain its symbiotic behavior in the presence of combined-N. These results indicate that B. diazoefficiens stringent response integrates into the plant defense suppression and regulation of nodulation circuits in soybean, perhaps mediated by the type-3-secretion system.IMPORTANCE The symbiotic N2 fixation carried out between prokaryotic rhizobia and legume plants performs a substantial contribution to the N-cycle in the biosphere. This symbiotic association is initiated when rhizobia infect and penetrate the root hairs, which is followed by the growth and development of root nodules within which the infective rhizobia are established and protected. Thus, the nodule environment allows the expression and function of the enzyme complex that catalyzes N2 fixation. However, during early infection the rhizobia find a harsh environment while penetrating the root hairs. To cope with this nuisance, the rhizobia mount a stress response known as stringent response. In turn, the plant regulates nodulation in response to the presence of alternative sources of combined-N in the surrounding medium. Control of these processes is crucial for a successful symbiosis, and here we show how the rhizobial stringent response may modulate plant defense suppression and the networks of regulation of nodulation.
Fil: Pérez Giménez, 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; Argentina
Fil: Iturralde, Esteban Tomás. 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; Argentina
Fil: Torres Tejerizo, Gonzalo Arturo. 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; Argentina
Fil: Quelas, Juan Ignacio. 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; Argentina
Fil: Krol, Elizaveta. Philipps-Universität Marburg; Alemania
Fil: Borassi, Cecilia. 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: Becker, Anke. Philipps-Universität Marburg; Alemania
Fil: Estevez, Jose Manuel. 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. Universidad Andrés Bello; Chile
Fil: Lodeiro, Anibal. 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; Argentina
description When subjected to nutritional stress, bacteria modify their amino acid metabolism and cell division activities by means of the stringent response, which is controlled by the Rsh protein in alphaproteobacteria. An important group of alphaproteobacteria are the rhizobia, which fix atmospheric N2 in symbiosis with legume plants. Although nutritional stress is common for rhizobia while infecting legume roots, the stringent response was scarcely studied in this group of soil bacteria. In this report, we obtained a mutant in the rsh gene of Bradyrhizobium diazoefficiens, the N2-fixing symbiont of soybean. This mutant was defective for type-3-secretion system induction, plant-defense suppression at early root infection, and competition for nodulation. Furthermore, the mutant produced smaller nodules, although with normal morphology, which lead to lower plant biomass production. Soybean genes GmRIC1 and GmRIC2, involved in autoregulation of nodulation, were upregulated in plants inoculated with the mutant in N-free condition. In addition, when plants were inoculated in the presence of 10 mM NH4NO3, the mutant produced nodules containing bacteroids, and GmRIC1 and GmRIC2 were downregulated. The rsh mutant released more auxin to the culture supernatant than the wild type, which might in part explain its symbiotic behavior in the presence of combined-N. These results indicate that B. diazoefficiens stringent response integrates into the plant defense suppression and regulation of nodulation circuits in soybean, perhaps mediated by the type-3-secretion system.IMPORTANCE The symbiotic N2 fixation carried out between prokaryotic rhizobia and legume plants performs a substantial contribution to the N-cycle in the biosphere. This symbiotic association is initiated when rhizobia infect and penetrate the root hairs, which is followed by the growth and development of root nodules within which the infective rhizobia are established and protected. Thus, the nodule environment allows the expression and function of the enzyme complex that catalyzes N2 fixation. However, during early infection the rhizobia find a harsh environment while penetrating the root hairs. To cope with this nuisance, the rhizobia mount a stress response known as stringent response. In turn, the plant regulates nodulation in response to the presence of alternative sources of combined-N in the surrounding medium. Control of these processes is crucial for a successful symbiosis, and here we show how the rhizobial stringent response may modulate plant defense suppression and the networks of regulation of nodulation.
publishDate 2021
dc.date.none.fl_str_mv 2021-04-13
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
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dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/155931
Pérez Giménez, Julieta; Iturralde, Esteban Tomás; Torres Tejerizo, Gonzalo Arturo; Quelas, Juan Ignacio; Krol, Elizaveta; et al.; A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation; American Society for Microbiology; Applied and Environmental Microbiology; 87; 9; 13-4-2021; 1-14
0099-2240
CONICET Digital
CONICET
url http://hdl.handle.net/11336/155931
identifier_str_mv Pérez Giménez, Julieta; Iturralde, Esteban Tomás; Torres Tejerizo, Gonzalo Arturo; Quelas, Juan Ignacio; Krol, Elizaveta; et al.; A stringent response-defective Bradyrhizobium diazoefficiens does not activate the type-3-secretion system, elicits early plant defense, and circumvents NH 4 NO 3 -induced inhibition of nodulation; American Society for Microbiology; Applied and Environmental Microbiology; 87; 9; 13-4-2021; 1-14
0099-2240
CONICET Digital
CONICET
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dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
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