Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway

Autores
Balado, Miguel; Souto, Alba; Vences, Ana; Careaga Quiroga, Valeria Pilar; Valderrama, Katherine; Segade, Yuri; Rodríguez, Jaime; Osorio, Carlos R.; Jiménez, Carlos; Lemos, Manuel L.
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The iron uptake mechanisms based on siderophore synthesis used by the fish pathogen Aeromonas salmonicida subsp. salmonicida are still not completely understood, and the precise structure of the siderophore(s) is unknown. The analysis of genome sequences revealed that this bacterium possesses two gene clusters putatively involved in the synthesis of siderophores. One cluster is a candidate to encode the synthesis of acinetobactin, the siderophore of the human pathogen Acinetobacter baumannii, while the second cluster shows high similarity to the genes encoding amonabactin synthesis in Aeromonas hydrophila. Using a combination of genomic analysis, mutagenesis, biological assays, chemical purification, and structural determination procedures, here we demonstrate that most A. salmonicida subsp. salmonicida strains produce simultaneously the two siderophores, acinetobactin and amonabactin. Interestingly, the synthesis of both siderophores relies on a single copy of the genes encoding the synthesis of the catechol moiety (2,3-dihydroxybenzoic acid) and on one encoding a phosphopantetheinyl transferase. These genes are present only in the amonabactin cluster, and a single mutation in any of them abolishes production of both siderophores. We could also demonstrate that some strains, isolated from fish raised in seawater, produce only acinetobactin since they present a deletion in the amonabactin biosynthesis gene amoG. Our study represents the first evidence of simultaneous production of acinetobactin and amonabactin by a bacterial pathogen and reveals the plasticity of bacterial genomes and biosynthetic pathways. The fact that the same siderophore is produced by unrelated pathogens highlights the importance of these systems and their interchangeability between different bacteria.
Fil: Balado, Miguel. Universidad de Santiago de Compostela; España
Fil: Souto, Alba. Universidad da Coruña; España
Fil: Vences, Ana. Universidad de Santiago de Compostela; España
Fil: Careaga Quiroga, Valeria Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad da Coruña; España
Fil: Valderrama, Katherine. Universidad da Coruña; España
Fil: Segade, Yuri. Universidad da Coruña; España
Fil: Rodríguez, Jaime. Universidad da Coruña; España
Fil: Osorio, Carlos R.. Universidad de Santiago de Compostela; España
Fil: Jiménez, Carlos. Universidad da Coruña; España
Fil: Lemos, Manuel L.. Universidad de Santiago de Compostela; España
Materia
Aeromonas
Siderophores
Iron Uptake
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:11336/60237
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/60237
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic PathwayBalado, MiguelSouto, AlbaVences, AnaCareaga Quiroga, Valeria PilarValderrama, KatherineSegade, YuriRodríguez, JaimeOsorio, Carlos R.Jiménez, CarlosLemos, Manuel L.AeromonasSiderophoresIron Uptakehttps://purl.org/becyt/ford/1.4https://purl.org/becyt/ford/1The iron uptake mechanisms based on siderophore synthesis used by the fish pathogen Aeromonas salmonicida subsp. salmonicida are still not completely understood, and the precise structure of the siderophore(s) is unknown. The analysis of genome sequences revealed that this bacterium possesses two gene clusters putatively involved in the synthesis of siderophores. One cluster is a candidate to encode the synthesis of acinetobactin, the siderophore of the human pathogen Acinetobacter baumannii, while the second cluster shows high similarity to the genes encoding amonabactin synthesis in Aeromonas hydrophila. Using a combination of genomic analysis, mutagenesis, biological assays, chemical purification, and structural determination procedures, here we demonstrate that most A. salmonicida subsp. salmonicida strains produce simultaneously the two siderophores, acinetobactin and amonabactin. Interestingly, the synthesis of both siderophores relies on a single copy of the genes encoding the synthesis of the catechol moiety (2,3-dihydroxybenzoic acid) and on one encoding a phosphopantetheinyl transferase. These genes are present only in the amonabactin cluster, and a single mutation in any of them abolishes production of both siderophores. We could also demonstrate that some strains, isolated from fish raised in seawater, produce only acinetobactin since they present a deletion in the amonabactin biosynthesis gene amoG. Our study represents the first evidence of simultaneous production of acinetobactin and amonabactin by a bacterial pathogen and reveals the plasticity of bacterial genomes and biosynthetic pathways. The fact that the same siderophore is produced by unrelated pathogens highlights the importance of these systems and their interchangeability between different bacteria.Fil: Balado, Miguel. Universidad de Santiago de Compostela; EspañaFil: Souto, Alba. Universidad da Coruña; EspañaFil: Vences, Ana. Universidad de Santiago de Compostela; EspañaFil: Careaga Quiroga, Valeria Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad da Coruña; EspañaFil: Valderrama, Katherine. Universidad da Coruña; EspañaFil: Segade, Yuri. Universidad da Coruña; EspañaFil: Rodríguez, Jaime. Universidad da Coruña; EspañaFil: Osorio, Carlos R.. Universidad de Santiago de Compostela; EspañaFil: Jiménez, Carlos. Universidad da Coruña; EspañaFil: Lemos, Manuel L.. Universidad de Santiago de Compostela; EspañaAmerican Chemical Society2015-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/60237Balado, Miguel; Souto, Alba; Vences, Ana; Careaga Quiroga, Valeria Pilar; Valderrama, Katherine; et al.; Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway; American Chemical Society; ACS Chemical Biology; 10; 12; 12-2015; 2850-28601554-8929CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1021/acschembio.5b00624info:eu-repo/semantics/altIdentifier/url/https://pubs.acs.org/doi/10.1021/acschembio.5b00624info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:36:14Zoai:ri.conicet.gov.ar:11336/60237instacron: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:34982025-09-29 09:36:14.573CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
title Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
spellingShingle Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
Balado, Miguel
Aeromonas
Siderophores
Iron Uptake
title_short Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
title_full Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
title_fullStr Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
title_full_unstemmed Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
title_sort Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway
dc.creator.none.fl_str_mv Balado, Miguel
Souto, Alba
Vences, Ana
Careaga Quiroga, Valeria Pilar
Valderrama, Katherine
Segade, Yuri
Rodríguez, Jaime
Osorio, Carlos R.
Jiménez, Carlos
Lemos, Manuel L.
author Balado, Miguel
author_facet Balado, Miguel
Souto, Alba
Vences, Ana
Careaga Quiroga, Valeria Pilar
Valderrama, Katherine
Segade, Yuri
Rodríguez, Jaime
Osorio, Carlos R.
Jiménez, Carlos
Lemos, Manuel L.
author_role author
author2 Souto, Alba
Vences, Ana
Careaga Quiroga, Valeria Pilar
Valderrama, Katherine
Segade, Yuri
Rodríguez, Jaime
Osorio, Carlos R.
Jiménez, Carlos
Lemos, Manuel L.
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Aeromonas
Siderophores
Iron Uptake
topic Aeromonas
Siderophores
Iron Uptake
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.4
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The iron uptake mechanisms based on siderophore synthesis used by the fish pathogen Aeromonas salmonicida subsp. salmonicida are still not completely understood, and the precise structure of the siderophore(s) is unknown. The analysis of genome sequences revealed that this bacterium possesses two gene clusters putatively involved in the synthesis of siderophores. One cluster is a candidate to encode the synthesis of acinetobactin, the siderophore of the human pathogen Acinetobacter baumannii, while the second cluster shows high similarity to the genes encoding amonabactin synthesis in Aeromonas hydrophila. Using a combination of genomic analysis, mutagenesis, biological assays, chemical purification, and structural determination procedures, here we demonstrate that most A. salmonicida subsp. salmonicida strains produce simultaneously the two siderophores, acinetobactin and amonabactin. Interestingly, the synthesis of both siderophores relies on a single copy of the genes encoding the synthesis of the catechol moiety (2,3-dihydroxybenzoic acid) and on one encoding a phosphopantetheinyl transferase. These genes are present only in the amonabactin cluster, and a single mutation in any of them abolishes production of both siderophores. We could also demonstrate that some strains, isolated from fish raised in seawater, produce only acinetobactin since they present a deletion in the amonabactin biosynthesis gene amoG. Our study represents the first evidence of simultaneous production of acinetobactin and amonabactin by a bacterial pathogen and reveals the plasticity of bacterial genomes and biosynthetic pathways. The fact that the same siderophore is produced by unrelated pathogens highlights the importance of these systems and their interchangeability between different bacteria.
Fil: Balado, Miguel. Universidad de Santiago de Compostela; España
Fil: Souto, Alba. Universidad da Coruña; España
Fil: Vences, Ana. Universidad de Santiago de Compostela; España
Fil: Careaga Quiroga, Valeria Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad da Coruña; España
Fil: Valderrama, Katherine. Universidad da Coruña; España
Fil: Segade, Yuri. Universidad da Coruña; España
Fil: Rodríguez, Jaime. Universidad da Coruña; España
Fil: Osorio, Carlos R.. Universidad de Santiago de Compostela; España
Fil: Jiménez, Carlos. Universidad da Coruña; España
Fil: Lemos, Manuel L.. Universidad de Santiago de Compostela; España
description The iron uptake mechanisms based on siderophore synthesis used by the fish pathogen Aeromonas salmonicida subsp. salmonicida are still not completely understood, and the precise structure of the siderophore(s) is unknown. The analysis of genome sequences revealed that this bacterium possesses two gene clusters putatively involved in the synthesis of siderophores. One cluster is a candidate to encode the synthesis of acinetobactin, the siderophore of the human pathogen Acinetobacter baumannii, while the second cluster shows high similarity to the genes encoding amonabactin synthesis in Aeromonas hydrophila. Using a combination of genomic analysis, mutagenesis, biological assays, chemical purification, and structural determination procedures, here we demonstrate that most A. salmonicida subsp. salmonicida strains produce simultaneously the two siderophores, acinetobactin and amonabactin. Interestingly, the synthesis of both siderophores relies on a single copy of the genes encoding the synthesis of the catechol moiety (2,3-dihydroxybenzoic acid) and on one encoding a phosphopantetheinyl transferase. These genes are present only in the amonabactin cluster, and a single mutation in any of them abolishes production of both siderophores. We could also demonstrate that some strains, isolated from fish raised in seawater, produce only acinetobactin since they present a deletion in the amonabactin biosynthesis gene amoG. Our study represents the first evidence of simultaneous production of acinetobactin and amonabactin by a bacterial pathogen and reveals the plasticity of bacterial genomes and biosynthetic pathways. The fact that the same siderophore is produced by unrelated pathogens highlights the importance of these systems and their interchangeability between different bacteria.
publishDate 2015
dc.date.none.fl_str_mv 2015-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/60237
Balado, Miguel; Souto, Alba; Vences, Ana; Careaga Quiroga, Valeria Pilar; Valderrama, Katherine; et al.; Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway; American Chemical Society; ACS Chemical Biology; 10; 12; 12-2015; 2850-2860
1554-8929
CONICET Digital
CONICET
url http://hdl.handle.net/11336/60237
identifier_str_mv Balado, Miguel; Souto, Alba; Vences, Ana; Careaga Quiroga, Valeria Pilar; Valderrama, Katherine; et al.; Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic Pathway; American Chemical Society; ACS Chemical Biology; 10; 12; 12-2015; 2850-2860
1554-8929
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1021/acschembio.5b00624
info:eu-repo/semantics/altIdentifier/url/https://pubs.acs.org/doi/10.1021/acschembio.5b00624
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Chemical Society
publisher.none.fl_str_mv American Chemical Society
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.069144

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