Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome
Summary: The host-microbiome associations occurring on the skin of vertebrates significantly influence hosts’ health. However, the factors mediating their interactions remain largely unknown. Herein, we used integrated technical and ecological frameworks to investigate the skin metabolites sustainin...
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| Format: | Article |
| Language: | English |
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Elsevier
2023-11-01
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| Series: | iScience |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223021867 |
| _version_ | 1797658966186000384 |
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| author | Andrés E. Brunetti Mariana L. Lyra Anelize Bauermeister Boyke Bunk Christian Boedeker Mathias Müsken Fausto Carnevale Neto Jacqueline Nakau Mendonça Andrés Mauricio Caraballo-Rodríguez Weilan G.P. Melo Mônica T. Pupo Célio F.B. Haddad Gabriela M. Cabrera Jörg Overmann Norberto P. Lopes |
| author_facet | Andrés E. Brunetti Mariana L. Lyra Anelize Bauermeister Boyke Bunk Christian Boedeker Mathias Müsken Fausto Carnevale Neto Jacqueline Nakau Mendonça Andrés Mauricio Caraballo-Rodríguez Weilan G.P. Melo Mônica T. Pupo Célio F.B. Haddad Gabriela M. Cabrera Jörg Overmann Norberto P. Lopes |
| author_sort | Andrés E. Brunetti |
| collection | DOAJ |
| description | Summary: The host-microbiome associations occurring on the skin of vertebrates significantly influence hosts’ health. However, the factors mediating their interactions remain largely unknown. Herein, we used integrated technical and ecological frameworks to investigate the skin metabolites sustaining a beneficial symbiosis between tree frogs and bacteria. We characterize macrocyclic acylcarnitines as the major metabolites secreted by the frogs’ skin and trace their origin to an enzymatic unbalance of carnitine palmitoyltransferases. We found that these compounds colocalize with bacteria on the skin surface and are mostly represented by members of the Pseudomonas community. We showed that Pseudomonas sp. MPFS isolated from frogs’ skin can exploit acylcarnitines as its sole carbon and nitrogen source, and this metabolic capability is widespread in Pseudomonas. We summarize frogs’ multiple mechanisms to filter environmental bacteria and highlight that acylcarnitines likely evolved for another function but were co-opted to provide nutritional benefits to the symbionts. |
| first_indexed | 2024-03-11T18:07:05Z |
| format | Article |
| id | doaj.art-52e1e6cd9bf64c0aa306b2c08e112929 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-11T18:07:05Z |
| publishDate | 2023-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-52e1e6cd9bf64c0aa306b2c08e1129292023-10-17T04:07:19ZengElsevieriScience2589-00422023-11-012611108109Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiomeAndrés E. Brunetti0Mariana L. Lyra1Anelize Bauermeister2Boyke Bunk3Christian Boedeker4Mathias Müsken5Fausto Carnevale Neto6Jacqueline Nakau Mendonça7Andrés Mauricio Caraballo-Rodríguez8Weilan G.P. Melo9Mônica T. Pupo10Célio F.B. Haddad11Gabriela M. Cabrera12Jörg Overmann13Norberto P. Lopes14Instituto de Biología Subtropical (IBS, UNaM-CONICET), Posadas, Misiones N3300LQH, Argentina; NPPNS, Department of Biomolecular Sciences, Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo 14040-903, Brazil; Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Hans-Knoell-Straße 8, 07745 Jena, Germany; Corresponding authorNew York University Abu Dhabi, Saadiyat Island, Abu Dhabi 129188, United Arab EmiratesInstituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, São Paulo 05508-000, BrazilLeibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, 38124 Braunschweig, Niedersachsen, GermanyLeibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, 38124 Braunschweig, Niedersachsen, GermanyCentral Facility for Microscopy, Helmholtz Centre for Infection Research (HZI), 38124 Braunschweig, Niedersachsen, GermanyNorthwest Metabolomics Research Center, Department of Anesthesiology and Pain Medicine, University of Washington, 850 Republican Street, Seattle, WA 98109, USANPPNS, Department of Biomolecular Sciences, Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo 14040-903, BrazilCollaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USAFaculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo 14040-903, BrazilFaculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo 14040-903, BrazilDepartamento de Biodiversidade e Centro de Aquicultura da UNESP (CAUNESP), Instituto de Biociências, UNESP-Universidade Estadual Paulista, Rio Claro, São Paulo 13506-900, BrazilFacultad de Ciencias Exactas y Naturales, Departamento de Química Orgánica, Universidad de Buenos Aires, Buenos Aires C1428EGA, Argentina; Unidad de Microanálisis y Métodos Físicos aplicados a la Química Orgánica (UMYMFOR), Buenos Aires C1428EGA, ArgentinaLeibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, 38124 Braunschweig, Niedersachsen, Germany; Corresponding authorNPPNS, Department of Biomolecular Sciences, Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo 14040-903, Brazil; Corresponding authorSummary: The host-microbiome associations occurring on the skin of vertebrates significantly influence hosts’ health. However, the factors mediating their interactions remain largely unknown. Herein, we used integrated technical and ecological frameworks to investigate the skin metabolites sustaining a beneficial symbiosis between tree frogs and bacteria. We characterize macrocyclic acylcarnitines as the major metabolites secreted by the frogs’ skin and trace their origin to an enzymatic unbalance of carnitine palmitoyltransferases. We found that these compounds colocalize with bacteria on the skin surface and are mostly represented by members of the Pseudomonas community. We showed that Pseudomonas sp. MPFS isolated from frogs’ skin can exploit acylcarnitines as its sole carbon and nitrogen source, and this metabolic capability is widespread in Pseudomonas. We summarize frogs’ multiple mechanisms to filter environmental bacteria and highlight that acylcarnitines likely evolved for another function but were co-opted to provide nutritional benefits to the symbionts.http://www.sciencedirect.com/science/article/pii/S2589004223021867Biological sciencesMicrobiologyMicrobial metabolismOmicsMetabolomics |
| spellingShingle | Andrés E. Brunetti Mariana L. Lyra Anelize Bauermeister Boyke Bunk Christian Boedeker Mathias Müsken Fausto Carnevale Neto Jacqueline Nakau Mendonça Andrés Mauricio Caraballo-Rodríguez Weilan G.P. Melo Mônica T. Pupo Célio F.B. Haddad Gabriela M. Cabrera Jörg Overmann Norberto P. Lopes Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome iScience Biological sciences Microbiology Microbial metabolism Omics Metabolomics |
| title | Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome |
| title_full | Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome |
| title_fullStr | Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome |
| title_full_unstemmed | Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome |
| title_short | Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome |
| title_sort | host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome |
| topic | Biological sciences Microbiology Microbial metabolism Omics Metabolomics |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223021867 |
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