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

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 ge...

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Autores: Balado Dacosta, Miguel, Souto, Alba, Vences, Ana, Careaga, Valeria P, Valderrama, Katherine, Segade, Yuri, Rodríguez, Jaime, Rodríguez Osorio, Carlos, Jiménez, Carlos, Lemos Ramos, Manuel Luis
Formato: artículo
Fecha de publicación:2015
País:España
Recursos:Universidad de Santiago de Compostela (USC)
Repositorio:Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
Idioma:inglés
OAI Identifier:oai:minerva.usc.gal:10347/46364
Acesso em linha:https://hdl.handle.net/10347/46364
Access Level:acceso abierto
Palavra-chave:Aeromonas
Aeromonas salmonicida
Iron uptake
Siderophores
Acinetobactin
Amonabactin
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spelling Two Catechol Siderophores, Acinetobactin and Amonabactin, Are Simultaneously Produced by Aeromonas salmonicida subsp. salmonicida Sharing Part of the Biosynthetic PathwayBalado Dacosta, MiguelSouto, AlbaVences, AnaCareaga, Valeria PValderrama, KatherineSegade, YuriRodríguez, JaimeRodríguez Osorio, CarlosJiménez, CarlosLemos Ramos, Manuel LuisAeromonasAeromonas salmonicidaIron uptakeSiderophoresAcinetobactinAmonabactinThe 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.American Chemical SocietyUniversidade de Santiago de Compostela. Instituto de Investigación do Medio Acuático para Unha Saúde Global (iARCUS)Universidade de Santiago de Compostela. Departamento de Microbioloxía e Parasitoloxía20152015-10-1320152015-10-13journal articlehttp://purl.org/coar/resource_type/c_6501AMhttp://purl.org/coar/version/c_ab4af688f83e57aainfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/10347/46364reponame:Minerva. Repositorio Institucional de la Universidad de Santiago de Compostelainstname:Universidad de Santiago de Compostela (USC)InglésengMinisterio de Educación y Ciencia Programa Nacional de Medios de Transporte CSD2007-00002 Mejora de la producción en acuicultura mediante herramientas de biotecnología (Aquagenomics)Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 Programa Nacional de Investigación Fundamental AGL2012-39274-C02-01 CARACTERIZACION DE LA SINTESIS DE SIDEROFOROS COMO FACTOR DE VIRULENCIA EN PHOTOBACTERIUM DAMSELAE SUBSP DAMSELAE: ANALISIS COMPARATIVO CON LA SUBSP PISCICIDAMinisterio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 Programa Nacional de Investigación Fundamental AGL2012-39274-C02-02open accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:minerva.usc.gal:10347/463642026-06-15T12:47:27Z
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 Dacosta, Miguel
Aeromonas
Aeromonas salmonicida
Iron uptake
Siderophores
Acinetobactin
Amonabactin
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 Dacosta, Miguel
Souto, Alba
Vences, Ana
Careaga, Valeria P
Valderrama, Katherine
Segade, Yuri
Rodríguez, Jaime
Rodríguez Osorio, Carlos
Jiménez, Carlos
Lemos Ramos, Manuel Luis
author Balado Dacosta, Miguel
author_facet Balado Dacosta, Miguel
Souto, Alba
Vences, Ana
Careaga, Valeria P
Valderrama, Katherine
Segade, Yuri
Rodríguez, Jaime
Rodríguez Osorio, Carlos
Jiménez, Carlos
Lemos Ramos, Manuel Luis
author_role author
author2 Souto, Alba
Vences, Ana
Careaga, Valeria P
Valderrama, Katherine
Segade, Yuri
Rodríguez, Jaime
Rodríguez Osorio, Carlos
Jiménez, Carlos
Lemos Ramos, Manuel Luis
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade de Santiago de Compostela. Instituto de Investigación do Medio Acuático para Unha Saúde Global (iARCUS)
Universidade de Santiago de Compostela. Departamento de Microbioloxía e Parasitoloxía
dc.subject.none.fl_str_mv Aeromonas
Aeromonas salmonicida
Iron uptake
Siderophores
Acinetobactin
Amonabactin
topic Aeromonas
Aeromonas salmonicida
Iron uptake
Siderophores
Acinetobactin
Amonabactin
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
2015-10-13
2015
2015-10-13
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
AM
http://purl.org/coar/version/c_ab4af688f83e57aa
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/10347/46364
url https://hdl.handle.net/10347/46364
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Ministerio de Educación y Ciencia Programa Nacional de Medios de Transporte CSD2007-00002 Mejora de la producción en acuicultura mediante herramientas de biotecnología (Aquagenomics)
Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 Programa Nacional de Investigación Fundamental AGL2012-39274-C02-01 CARACTERIZACION DE LA SINTESIS DE SIDEROFOROS COMO FACTOR DE VIRULENCIA EN PHOTOBACTERIUM DAMSELAE SUBSP DAMSELAE: ANALISIS COMPARATIVO CON LA SUBSP PISCICIDA
Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 Programa Nacional de Investigación Fundamental AGL2012-39274-C02-02
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 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:Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
instname:Universidad de Santiago de Compostela (USC)
instname_str Universidad de Santiago de Compostela (USC)
reponame_str Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
collection Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,81155

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