Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i>
Piscibactin is a widespread siderophore system present in many different bacteria, especially within the <i>Vibrionaceae</i> family. Previous works showed that most functions required for biosynthesis and transport of this siderophore are encoded by the high-pathogenicity island <i>...
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MDPI AG
2022-08-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/16/8865 |
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| author | Marta A. Lages Lucía Ageitos Jaime Rodríguez Carlos Jiménez Manuel L. Lemos Miguel Balado |
| author_facet | Marta A. Lages Lucía Ageitos Jaime Rodríguez Carlos Jiménez Manuel L. Lemos Miguel Balado |
| author_sort | Marta A. Lages |
| collection | DOAJ |
| description | Piscibactin is a widespread siderophore system present in many different bacteria, especially within the <i>Vibrionaceae</i> family. Previous works showed that most functions required for biosynthesis and transport of this siderophore are encoded by the high-pathogenicity island <i>irp</i>-HPI. In the present work, using <i>Vibrio anguillarum</i> as a model, we could identify additional key functions encoded by <i>irp</i>-HPI that are necessary for piscibactin production and transport and that have remained unknown. Allelic exchange mutagenesis, combined with cross-feeding bioassays and LC-MS analysis, were used to demonstrate that Irp4 protein is an essential component for piscibactin synthesis since it is the thioesterase required for nascent piscibactin be released from the NRPS Irp1. We also show that Irp8 is a MFS-type protein essential for piscibactin secretion. In addition, after passage through the outer membrane transporter FrpA, the completion of ferri-piscibactin internalization through the inner membrane would be achieved by the ABC-type transporter FrpBC. The expression of this transporter is coordinated with the expression of FrpA and with the genes encoding biosynthetic functions. Since piscibactin is a major virulence factor of some pathogenic vibrios, the elements of biosynthesis and transport described here could be additional interesting targets for the design of novel antimicrobials against these bacterial pathogens. |
| first_indexed | 2024-03-09T09:56:31Z |
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| id | doaj.art-97bd576a052745b4a54a9e59fb9889de |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T09:56:31Z |
| publishDate | 2022-08-01 |
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| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-97bd576a052745b4a54a9e59fb9889de2023-12-01T23:46:41ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-08-012316886510.3390/ijms23168865Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i>Marta A. Lages0Lucía Ageitos1Jaime Rodríguez2Carlos Jiménez3Manuel L. Lemos4Miguel Balado5Departmento de Microbiología y Parasitología, Instituto de Acuicultura, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, SpainCentro de Investigacións Científicas Avanzadas (CICA), Departamento de Química, Facultade de Ciencias, Universidade da Coruña, 15071 A Coruña, SpainCentro de Investigacións Científicas Avanzadas (CICA), Departamento de Química, Facultade de Ciencias, Universidade da Coruña, 15071 A Coruña, SpainCentro de Investigacións Científicas Avanzadas (CICA), Departamento de Química, Facultade de Ciencias, Universidade da Coruña, 15071 A Coruña, SpainDepartmento de Microbiología y Parasitología, Instituto de Acuicultura, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, SpainDepartmento de Microbiología y Parasitología, Instituto de Acuicultura, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, SpainPiscibactin is a widespread siderophore system present in many different bacteria, especially within the <i>Vibrionaceae</i> family. Previous works showed that most functions required for biosynthesis and transport of this siderophore are encoded by the high-pathogenicity island <i>irp</i>-HPI. In the present work, using <i>Vibrio anguillarum</i> as a model, we could identify additional key functions encoded by <i>irp</i>-HPI that are necessary for piscibactin production and transport and that have remained unknown. Allelic exchange mutagenesis, combined with cross-feeding bioassays and LC-MS analysis, were used to demonstrate that Irp4 protein is an essential component for piscibactin synthesis since it is the thioesterase required for nascent piscibactin be released from the NRPS Irp1. We also show that Irp8 is a MFS-type protein essential for piscibactin secretion. In addition, after passage through the outer membrane transporter FrpA, the completion of ferri-piscibactin internalization through the inner membrane would be achieved by the ABC-type transporter FrpBC. The expression of this transporter is coordinated with the expression of FrpA and with the genes encoding biosynthetic functions. Since piscibactin is a major virulence factor of some pathogenic vibrios, the elements of biosynthesis and transport described here could be additional interesting targets for the design of novel antimicrobials against these bacterial pathogens.https://www.mdpi.com/1422-0067/23/16/8865siderophorespiscibactin<i>Vibrio anguillarum</i><i>Vibrionaceae</i>bacterial fish diseases |
| spellingShingle | Marta A. Lages Lucía Ageitos Jaime Rodríguez Carlos Jiménez Manuel L. Lemos Miguel Balado Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i> International Journal of Molecular Sciences siderophores piscibactin <i>Vibrio anguillarum</i> <i>Vibrionaceae</i> bacterial fish diseases |
| title | Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i> |
| title_full | Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i> |
| title_fullStr | Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i> |
| title_full_unstemmed | Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i> |
| title_short | Identification of Key Functions Required for Production and Utilization of the Siderophore Piscibactin Encoded by the High-Pathogenicity Island <i>irp</i>-HPI in <i>Vibrionaceae</i> |
| title_sort | identification of key functions required for production and utilization of the siderophore piscibactin encoded by the high pathogenicity island i irp i hpi in i vibrionaceae i |
| topic | siderophores piscibactin <i>Vibrio anguillarum</i> <i>Vibrionaceae</i> bacterial fish diseases |
| url | https://www.mdpi.com/1422-0067/23/16/8865 |
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