Acetylcholine chemotaxis in global bacterial plant pathogens

Interactions within the plant holobiont involve a wide diversity of plant- and microbial-derived signals. Bacterial perception of these signals allows directed movement along chemical gradients through chemotaxis, a process that is an important determinant for plant colonization and infection. The q...

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Autores: Gavira Gallardo, J. A., Gilabert, Manuel J., Santamaría-Hernando, Saray, Molina-Ollero, Ana, Rico-Jiménez, Miriam, Cabrera, Juan J., López-Solanilla, Emilia, Matilla, Miguel A.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/397822
Acceso en línea:http://hdl.handle.net/10261/397822
Access Level:acceso abierto
Palabra clave:Acetylcholine
Bacterial signaling
Chemoreceptor
Chemotaxis
Osmoprotection
Phytopathogens
Structural biology
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Acetylcholine chemotaxis in global bacterial plant pathogens
title Acetylcholine chemotaxis in global bacterial plant pathogens
spellingShingle Acetylcholine chemotaxis in global bacterial plant pathogens
Gavira Gallardo, J. A.
Acetylcholine
Bacterial signaling
Chemoreceptor
Chemotaxis
Osmoprotection
Phytopathogens
Structural biology
title_short Acetylcholine chemotaxis in global bacterial plant pathogens
title_full Acetylcholine chemotaxis in global bacterial plant pathogens
title_fullStr Acetylcholine chemotaxis in global bacterial plant pathogens
title_full_unstemmed Acetylcholine chemotaxis in global bacterial plant pathogens
title_sort Acetylcholine chemotaxis in global bacterial plant pathogens
dc.creator.none.fl_str_mv Gavira Gallardo, J. A.
Gilabert, Manuel J.
Santamaría-Hernando, Saray
Molina-Ollero, Ana
Rico-Jiménez, Miriam
Cabrera, Juan J.
López-Solanilla, Emilia
Matilla, Miguel A.
author Gavira Gallardo, J. A.
author_facet Gavira Gallardo, J. A.
Gilabert, Manuel J.
Santamaría-Hernando, Saray
Molina-Ollero, Ana
Rico-Jiménez, Miriam
Cabrera, Juan J.
López-Solanilla, Emilia
Matilla, Miguel A.
author_role author
author2 Gilabert, Manuel J.
Santamaría-Hernando, Saray
Molina-Ollero, Ana
Rico-Jiménez, Miriam
Cabrera, Juan J.
López-Solanilla, Emilia
Matilla, Miguel A.
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Consejo Superior de Investigaciones Científicas (España)
Gavira Gallardo, J. A. [0000-0002-7386-6484]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Acetylcholine
Bacterial signaling
Chemoreceptor
Chemotaxis
Osmoprotection
Phytopathogens
Structural biology
topic Acetylcholine
Bacterial signaling
Chemoreceptor
Chemotaxis
Osmoprotection
Phytopathogens
Structural biology
description Interactions within the plant holobiont involve a wide diversity of plant- and microbial-derived signals. Bacterial perception of these signals allows directed movement along chemical gradients through chemotaxis, a process that is an important determinant for plant colonization and infection. The quaternary amine acetylcholine is primarily known for its function as a neurotransmitter in mammalian nervous systems, but is emerging as a signal molecule that regulates plant growth, development, and stress resistance. Here, we report that plant pathogenic bacteria of the genera Agrobacterium and Dickeya exhibit strong chemotaxis to acetylcholine. These responses are mediated in Agrobacterium fabrum, Dickeya solani, and Dickeya dadantii by the dCache_1-type ligand binding domain (LBD) containing chemoreceptors AtuA, MkcA, and DdaA, respectively, which recognize acetylcholine with affinities between 19 and 91 µM. These chemoreceptors also recognize additional quaternary amines such as choline, L-carnitine, and betaine. The high-resolution structure of MkcA-LBD of D. solani was solved in complex with choline, which allowed the identification of the molecular determinants of choline and acetylcholine recognition in this chemoreceptor. Functionally, DdaA was found to contribute to competitive colonization fitness in planta. Acetylcholine serves as a nutritional source for A. fabrum, but not for D. solani and D. dadantii, and provides osmoprotective effects in all three phytopathogenic species. Plant-associated bacteria exhibit chemotaxis toward a diversity of key plant signals, and their ability to sense acetylcholine may represent an adaptive strategy to ensure efficient plant infection and manage osmotic stress. Our findings suggest potential co-evolutionary interactions between plants and their associated microbiomes.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
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info:eu-repo/semantics/publishedVersion
format article
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/397822
url http://hdl.handle.net/10261/397822
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI//PID2019–103972GA-I00
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2023-146281NB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/128294
Gavira, J.A. ; Rico-Jimenez, M. ; Matilla, M.A.; 2025; "Structure of the ligand binding domain of the chemoreceptor MkcA (DSOMK10_RS0100305) of Dickeya solani MK10 in complex with choline [Dataset]; PDB; https://doi.org/10.2210/pdb9heh/pdb
https://doi.org/10.1016/j.micres.2025.128294
Sí
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eu_rights_str_mv openAccess
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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
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spelling Acetylcholine chemotaxis in global bacterial plant pathogensGavira Gallardo, J. A.Gilabert, Manuel J.Santamaría-Hernando, SarayMolina-Ollero, AnaRico-Jiménez, MiriamCabrera, Juan J.López-Solanilla, EmiliaMatilla, Miguel A.AcetylcholineBacterial signalingChemoreceptorChemotaxisOsmoprotectionPhytopathogensStructural biologyInteractions within the plant holobiont involve a wide diversity of plant- and microbial-derived signals. Bacterial perception of these signals allows directed movement along chemical gradients through chemotaxis, a process that is an important determinant for plant colonization and infection. The quaternary amine acetylcholine is primarily known for its function as a neurotransmitter in mammalian nervous systems, but is emerging as a signal molecule that regulates plant growth, development, and stress resistance. Here, we report that plant pathogenic bacteria of the genera Agrobacterium and Dickeya exhibit strong chemotaxis to acetylcholine. These responses are mediated in Agrobacterium fabrum, Dickeya solani, and Dickeya dadantii by the dCache_1-type ligand binding domain (LBD) containing chemoreceptors AtuA, MkcA, and DdaA, respectively, which recognize acetylcholine with affinities between 19 and 91 µM. These chemoreceptors also recognize additional quaternary amines such as choline, L-carnitine, and betaine. The high-resolution structure of MkcA-LBD of D. solani was solved in complex with choline, which allowed the identification of the molecular determinants of choline and acetylcholine recognition in this chemoreceptor. Functionally, DdaA was found to contribute to competitive colonization fitness in planta. Acetylcholine serves as a nutritional source for A. fabrum, but not for D. solani and D. dadantii, and provides osmoprotective effects in all three phytopathogenic species. Plant-associated bacteria exhibit chemotaxis toward a diversity of key plant signals, and their ability to sense acetylcholine may represent an adaptive strategy to ensure efficient plant infection and manage osmotic stress. Our findings suggest potential co-evolutionary interactions between plants and their associated microbiomes.This work was supported by the Spanish Ministry of Science, Innovation and Universities/Agencia Estatal de Investigación 10.13039/501100011033 and FEDER-EU (grants PID2019\u2013103972GA-I00 and PID2023-146281NB-I00 to M.A.M., PID2020\u2013116261GB-I00 to J.A.G, and PID2021\u2013125673OB-I00 to E.L.S) and through a grant from the CSIC (grant 2023AEP002 to M.A.M.).Peer reviewedElsevier BVMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Consejo Superior de Investigaciones Científicas (España)Gavira Gallardo, J. A. [0000-0002-7386-6484]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/397822reponame: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##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-116261GB-I00info:eu-repo/grantAgreement/AEI//PID2019–103972GA-I00info:eu-repo/grantAgreement/AEI//PID2021–125673OB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2023-146281NB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/128294Gavira, J.A. ; Rico-Jimenez, M. ; Matilla, M.A.; 2025; "Structure of the ligand binding domain of the chemoreceptor MkcA (DSOMK10_RS0100305) of Dickeya solani MK10 in complex with choline [Dataset]; PDB; https://doi.org/10.2210/pdb9heh/pdbhttps://doi.org/10.1016/j.micres.2025.128294Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3978222026-05-22T06:33:51Z
score 15.81155

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