The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH or Gap) is a ubiquitous enzyme essential for carbon and energy metabolism in most organisms. Despite its primary role in sugar metabolism, GAPDH is recognized for its involvement in diverse cellular processes, being considered a paradigm among multifun...

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Autores: Casas-Román, Ariana, Lorite, María J., Werner, Mariana, Muñoz, Socorro, Gallegos, María Trinidad, Sanjuán, Juan
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/367145
Acceso en línea:http://hdl.handle.net/10261/367145
Access Level:acceso abierto
Palabra clave:GAPDH
Rhizobia
Moonlighting protein
Cyclic diguanylate
Nitrogen fixation
Symbiosis
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spelling The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.Casas-Román, ArianaLorite, María J.Werner, MarianaMuñoz, SocorroGallegos, María TrinidadSanjuán, JuanGAPDHRhizobiaMoonlighting proteinCyclic diguanylateNitrogen fixationSymbiosisGlyceraldehyde-3-phosphate dehydrogenase (GAPDH or Gap) is a ubiquitous enzyme essential for carbon and energy metabolism in most organisms. Despite its primary role in sugar metabolism, GAPDH is recognized for its involvement in diverse cellular processes, being considered a paradigm among multifunctional/moonlighting proteins. Besides its canonical cytoplasmic location, GAPDH has been detected on cell surfaces or as a secreted protein in prokaryotes, yet little is known about its possible roles in plant symbiotic bacteria. Here we report that Rhizobium etli, a nitrogen-fixing symbiont of common beans, carries a single gap gene responsible for both GAPDH glycolytic and gluconeogenic activities. An active Gap protein is required throughout all stages of the symbiosis between R. etli and its host plant Phaseolus vulgaris. Both glycolytic and gluconeogenic Gap metabolic activities likely contribute to bacterial fitness during early and intermediate stages of the interaction, whereas GAPDH gluconeogenic activity seems critical for nodule invasion and nitrogen fixation. Although the R. etli Gap protein is secreted in a c-di-GMP related manner, no involvement of the R. etli gap gene in c-di-GMP related phenotypes, such as flocculation, biofilm formation or EPS production, was observed. Notably, the R. etli gap gene fully complemented a double gap1/gap2 mutant of Pseudomonas syringae for free life growth, albeit only partially in planta, suggesting potential specific roles for each type of Gap protein. Nevertheless, further research is required to unravel additional functions of the R. etli Gap protein beyond its essential metabolic roles.This work was supported by grants BIO2017‐83533‐P, PID2021‐122418NB‐I00 and PID2022-140168NB-I00 (funded by MCIN/AEI/ 10.13039/501100011033 and by “ERDF A way of making Europe”), grant 2021AEP136 (funded by CSIC) and ProyExcel_00464 (funded by Junta de Andalucía, Spain). ACR was supported by the PRE2018‐083387 predoctoral contract (funded by MCIN/AEI/ 10.13039/501100011033 and by “ESF Investing in your future”).Elsevier BVEuropean CommissionMinisterio de Ciencia e Innovación (España)Junta de AndalucíaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2024202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/367145reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017‐83533‐Pinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021‐122418NB‐I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-140168NB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1016/j.micres.2024.127737http://dx.doi.org/10.1016/j.micres.2024.127737Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3671452026-05-22T06:33:51Z
dc.title.none.fl_str_mv The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
title The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
spellingShingle The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
Casas-Román, Ariana
GAPDH
Rhizobia
Moonlighting protein
Cyclic diguanylate
Nitrogen fixation
Symbiosis
title_short The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
title_full The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
title_fullStr The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
title_full_unstemmed The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
title_sort The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans.
dc.creator.none.fl_str_mv Casas-Román, Ariana
Lorite, María J.
Werner, Mariana
Muñoz, Socorro
Gallegos, María Trinidad
Sanjuán, Juan
author Casas-Román, Ariana
author_facet Casas-Román, Ariana
Lorite, María J.
Werner, Mariana
Muñoz, Socorro
Gallegos, María Trinidad
Sanjuán, Juan
author_role author
author2 Lorite, María J.
Werner, Mariana
Muñoz, Socorro
Gallegos, María Trinidad
Sanjuán, Juan
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministerio de Ciencia e Innovación (España)
Junta de Andalucía
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv GAPDH
Rhizobia
Moonlighting protein
Cyclic diguanylate
Nitrogen fixation
Symbiosis
topic GAPDH
Rhizobia
Moonlighting protein
Cyclic diguanylate
Nitrogen fixation
Symbiosis
description Glyceraldehyde-3-phosphate dehydrogenase (GAPDH or Gap) is a ubiquitous enzyme essential for carbon and energy metabolism in most organisms. Despite its primary role in sugar metabolism, GAPDH is recognized for its involvement in diverse cellular processes, being considered a paradigm among multifunctional/moonlighting proteins. Besides its canonical cytoplasmic location, GAPDH has been detected on cell surfaces or as a secreted protein in prokaryotes, yet little is known about its possible roles in plant symbiotic bacteria. Here we report that Rhizobium etli, a nitrogen-fixing symbiont of common beans, carries a single gap gene responsible for both GAPDH glycolytic and gluconeogenic activities. An active Gap protein is required throughout all stages of the symbiosis between R. etli and its host plant Phaseolus vulgaris. Both glycolytic and gluconeogenic Gap metabolic activities likely contribute to bacterial fitness during early and intermediate stages of the interaction, whereas GAPDH gluconeogenic activity seems critical for nodule invasion and nitrogen fixation. Although the R. etli Gap protein is secreted in a c-di-GMP related manner, no involvement of the R. etli gap gene in c-di-GMP related phenotypes, such as flocculation, biofilm formation or EPS production, was observed. Notably, the R. etli gap gene fully complemented a double gap1/gap2 mutant of Pseudomonas syringae for free life growth, albeit only partially in planta, suggesting potential specific roles for each type of Gap protein. Nevertheless, further research is required to unravel additional functions of the R. etli Gap protein beyond its essential metabolic roles.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
2024
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/10261/367145
url http://hdl.handle.net/10261/367145
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#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017‐83533‐P
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021‐122418NB‐I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-140168NB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1016/j.micres.2024.127737
http://dx.doi.org/10.1016/j.micres.2024.127737
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier BV
publisher.none.fl_str_mv Elsevier BV
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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