The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42

Bacterial exopolysaccharides (EPS) have been implicated in a variety of functions that assist in bacterial survival, colonization, and host–microbe interactions. Among them, bacterial linear β-glucans are polysaccharides formed by D-glucose units linked by β-glycosidic bonds, which include curdlan,...

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Autores: Pérez-Mendoza, Daniel, Romero-Jiménez, Lorena, Rodríguez-Carvajal, Miguel A., Lorite, María J., Muñoz, Socorro, Olmedilla, Adela, Sanjuán, Juan
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/286838
Acceso en línea:http://hdl.handle.net/10261/286838
Access Level:acceso abierto
Palabra clave:β-glucan
Rhizobium etli
Cyclic-di-GMP
Cellulose
Mixed-linkage-β-glucan (MLG)
Symbiosis
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spelling The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42Pérez-Mendoza, DanielRomero-Jiménez, LorenaRodríguez-Carvajal, Miguel A.Lorite, María J.Muñoz, SocorroOlmedilla, AdelaSanjuán, Juanβ-glucanRhizobium etliCyclic-di-GMPCelluloseMixed-linkage-β-glucan (MLG)SymbiosisBacterial exopolysaccharides (EPS) have been implicated in a variety of functions that assist in bacterial survival, colonization, and host–microbe interactions. Among them, bacterial linear β-glucans are polysaccharides formed by D-glucose units linked by β-glycosidic bonds, which include curdlan, cellulose, and the new described Mixed Linkage β-Glucan (MLG). Bis-(3′,5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a universal bacterial second messenger that usually promote EPS production. Here, we report Rhizobium etli as the first bacterium capable of producing cellulose and MLG. Significant amounts of these two β-glucans are not produced under free-living laboratory conditions, but their production is triggered upon elevation of intracellular c-di-GMP levels, both contributing to Congo red (CR) and Calcofluor (CF) phenotypes. Cellulose turned out to be more relevant for free-living phenotypes promoting flocculation and biofilm formation under high c-di-GMP conditions. None of these two EPS are essential for attachment to roots of Phaseolus vulgaris, neither for nodulation nor for symbiotic nitrogen fixation. However, both β-glucans separately contribute to the fitness of interaction between R. etli and its host. Overproduction of these β-glucans, particularly cellulose, appears detrimental for symbiosis. This indicates that their activation by c-di-GMP must be strictly regulated in time and space and should be controlled by different, yet unknown, regulatory pathways.This research was supported by CSIC grant 2021AEP136 and grants BIO2014-55075-P and BIO2017-83533-P, funded by MCIN/AEI/ 10.13039/501100011033 and by “ERDF A way of making Europe” by the European Union. DPM was supported by the Andalucía Talent Hub Program launched by the Andalusian Knowledge Agency, co-funded by the European Union’s Seventh Framework Program, Marie Skłodowska-Curie actions (COFUND—Grant Agreement no. 291780) and the Ministry of Economy, Innovation, Science, and Employment of the Junta de Andalucía. LRJ was supported by JAE-Pre fellowship (CSIC).Multidisciplinary Digital Publishing InstituteMinisterio de Ciencia e Innovación (España)European CommissionJunta de AndalucíaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320222023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/286838reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO//BIO2014-55075-Pinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-83533-Phttp://dx.doi.org/10.3390/biology11091364Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2868382026-05-22T06:33:51Z
dc.title.none.fl_str_mv The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
title The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
spellingShingle The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
Pérez-Mendoza, Daniel
β-glucan
Rhizobium etli
Cyclic-di-GMP
Cellulose
Mixed-linkage-β-glucan (MLG)
Symbiosis
title_short The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
title_full The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
title_fullStr The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
title_full_unstemmed The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
title_sort The role of two linear β-Glucans activated by c-di-GMP in Rhizobium etli CFN42
dc.creator.none.fl_str_mv Pérez-Mendoza, Daniel
Romero-Jiménez, Lorena
Rodríguez-Carvajal, Miguel A.
Lorite, María J.
Muñoz, Socorro
Olmedilla, Adela
Sanjuán, Juan
author Pérez-Mendoza, Daniel
author_facet Pérez-Mendoza, Daniel
Romero-Jiménez, Lorena
Rodríguez-Carvajal, Miguel A.
Lorite, María J.
Muñoz, Socorro
Olmedilla, Adela
Sanjuán, Juan
author_role author
author2 Romero-Jiménez, Lorena
Rodríguez-Carvajal, Miguel A.
Lorite, María J.
Muñoz, Socorro
Olmedilla, Adela
Sanjuán, Juan
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
European Commission
Junta de Andalucía
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv β-glucan
Rhizobium etli
Cyclic-di-GMP
Cellulose
Mixed-linkage-β-glucan (MLG)
Symbiosis
topic β-glucan
Rhizobium etli
Cyclic-di-GMP
Cellulose
Mixed-linkage-β-glucan (MLG)
Symbiosis
description Bacterial exopolysaccharides (EPS) have been implicated in a variety of functions that assist in bacterial survival, colonization, and host–microbe interactions. Among them, bacterial linear β-glucans are polysaccharides formed by D-glucose units linked by β-glycosidic bonds, which include curdlan, cellulose, and the new described Mixed Linkage β-Glucan (MLG). Bis-(3′,5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a universal bacterial second messenger that usually promote EPS production. Here, we report Rhizobium etli as the first bacterium capable of producing cellulose and MLG. Significant amounts of these two β-glucans are not produced under free-living laboratory conditions, but their production is triggered upon elevation of intracellular c-di-GMP levels, both contributing to Congo red (CR) and Calcofluor (CF) phenotypes. Cellulose turned out to be more relevant for free-living phenotypes promoting flocculation and biofilm formation under high c-di-GMP conditions. None of these two EPS are essential for attachment to roots of Phaseolus vulgaris, neither for nodulation nor for symbiotic nitrogen fixation. However, both β-glucans separately contribute to the fitness of interaction between R. etli and its host. Overproduction of these β-glucans, particularly cellulose, appears detrimental for symbiosis. This indicates that their activation by c-di-GMP must be strictly regulated in time and space and should be controlled by different, yet unknown, regulatory pathways.
publishDate 2022
dc.date.none.fl_str_mv 2022
2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/286838
url http://hdl.handle.net/10261/286838
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO//BIO2014-55075-P
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-83533-P
http://dx.doi.org/10.3390/biology11091364
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute
publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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