Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation

Bacterial surface motility is a complex microbial trait that contributes to host colonization. However, the knowledge about regulatory mechanisms that control surface translocation in rhizobia and their role in the establishment of symbiosis with legumes is still limited. Recently, 2-tridecanone (2-...

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Authors: Brito Santana, Paula; Duque Pedraza, Julián J.; Bernabéu Roda, Lydia M.; Carvia-Hermoso, Cristina; Cuéllar, Virginia; Fuentes Romero, Francisco; Acosta Jurado, Sebastián; Vinardell González, José María; Soto, María J.
Format: Article
Status:Published version
Publication date:2023
Country:España
Institution:Universidad de Sevilla (US)
Repository:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/148099
Online Access:https://hdl.handle.net/11441/148099
https://doi.org/10.3390/ijms24065848
Access Level:Open access
Keyword:Chaperone
Flagella
Nitrogen fixation
Nodulation
Plant colonization
Rhizobium
Stress tolerance
Surface motility
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author Brito Santana, Paula
author2 Duque Pedraza, Julián J.
Bernabéu Roda, Lydia M.
Carvia-Hermoso, Cristina
Cuéllar, Virginia
Fuentes Romero, Francisco
Acosta Jurado, Sebastián
Vinardell González, José María
Soto, María J.
author2_role author
author
author
author
author
author
author
author
author_browse Acosta Jurado, Sebastián
Bernabéu Roda, Lydia M.
Brito Santana, Paula
Carvia-Hermoso, Cristina
Cuéllar, Virginia
Duque Pedraza, Julián J.
Fuentes Romero, Francisco
Soto, María J.
Vinardell González, José María
author_facet Brito Santana, Paula
Duque Pedraza, Julián J.
Bernabéu Roda, Lydia M.
Carvia-Hermoso, Cristina
Cuéllar, Virginia
Fuentes Romero, Francisco
Acosta Jurado, Sebastián
Vinardell González, José María
Soto, María J.
author_role author
collection idUS. Depósito de Investigación de la Universidad de Sevilla
description Bacterial surface motility is a complex microbial trait that contributes to host colonization. However, the knowledge about regulatory mechanisms that control surface translocation in rhizobia and their role in the establishment of symbiosis with legumes is still limited. Recently, 2-tridecanone (2-TDC) was identified as an infochemical in bacteria that hampers microbial colonization of plants. In the alfalfa symbiont Sinorhizobium meliloti, 2-TDC promotes a mode of surface motility that is mostly independent of flagella. To understand the mechanism of action of 2-TDC in S. meliloti and unveil genes putatively involved in plant colonization, Tn5 transposants derived from a flagellaless strain that were impaired in 2-TDC-induced surface spreading were isolated and genetically characterized. In one of the mutants, the gene coding for the chaperone DnaJ was inactivated. Characterization of this transposant and newly obtained flagella-minus and flagella-plus dnaJ deletion mutants revealed that DnaJ is essential for surface translocation, while it plays a minor role in swimming motility. DnaJ loss-of-function reduces salt and oxidative stress tolerance in S. meliloti and hinders the establishment of efficient symbiosis by affecting nodule formation efficiency, cellular infection, and nitrogen fixation. Intriguingly, the lack of DnaJ causes more severe defects in a flagellaless background. This work highlights the role of DnaJ in the free-living and symbiotic lifestyles of S. meliloti.
eu_rights_str_mv openAccess
format article
id ES_86d2ddfd4ab3de9c88b9456c3daca3d9
institution Universidad de Sevilla (US)
instname_str Universidad de Sevilla (US)
network_acronym_str ES
network_name_str España
oai_identifier_str oai:idus.us.es:11441/148099
publishDate 2023
publishDateSort 2023
publisher Multidisciplinary Digital Publishing Institute (MDPI)
publisherStr Multidisciplinary Digital Publishing Institute (MDPI)
reponame_str idUS. Depósito de Investigación de la Universidad de Sevilla
spelling Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation Brito Santana, Paula Duque Pedraza, Julián J. Bernabéu Roda, Lydia M. Carvia-Hermoso, Cristina Cuéllar, Virginia Fuentes Romero, Francisco Acosta Jurado, Sebastián Vinardell González, José María Soto, María J. Chaperone Flagella Nitrogen fixation Nodulation Plant colonization Rhizobium Stress tolerance Surface motility Bacterial surface motility is a complex microbial trait that contributes to host colonization. However, the knowledge about regulatory mechanisms that control surface translocation in rhizobia and their role in the establishment of symbiosis with legumes is still limited. Recently, 2-tridecanone (2-TDC) was identified as an infochemical in bacteria that hampers microbial colonization of plants. In the alfalfa symbiont Sinorhizobium meliloti, 2-TDC promotes a mode of surface motility that is mostly independent of flagella. To understand the mechanism of action of 2-TDC in S. meliloti and unveil genes putatively involved in plant colonization, Tn5 transposants derived from a flagellaless strain that were impaired in 2-TDC-induced surface spreading were isolated and genetically characterized. In one of the mutants, the gene coding for the chaperone DnaJ was inactivated. Characterization of this transposant and newly obtained flagella-minus and flagella-plus dnaJ deletion mutants revealed that DnaJ is essential for surface translocation, while it plays a minor role in swimming motility. DnaJ loss-of-function reduces salt and oxidative stress tolerance in S. meliloti and hinders the establishment of efficient symbiosis by affecting nodule formation efficiency, cellular infection, and nitrogen fixation. Intriguingly, the lack of DnaJ causes more severe defects in a flagellaless background. This work highlights the role of DnaJ in the free-living and symbiotic lifestyles of S. meliloti. Ministerio de Ciencia e Innovación PGC2018-096477-B-I00, PID2019-107634R, PID2021-123540NB-I00 Multidisciplinary Digital Publishing Institute (MDPI) https://hdl.handle.net/11441/148099 https://doi.org/10.3390/ijms24065848
spellingShingle Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
Brito Santana, Paula
Chaperone
Flagella
Nitrogen fixation
Nodulation
Plant colonization
Rhizobium
Stress tolerance
Surface motility
status_str publishedVersion
title Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
title_full Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
title_fullStr Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
title_full_unstemmed Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
title_short Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
title_sort Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
topic Chaperone
Flagella
Nitrogen fixation
Nodulation
Plant colonization
Rhizobium
Stress tolerance
Surface motility
topic_facet Chaperone
Flagella
Nitrogen fixation
Nodulation
Plant colonization
Rhizobium
Stress tolerance
Surface motility
url https://hdl.handle.net/11441/148099
https://doi.org/10.3390/ijms24065848