Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome

iScience · 15 authors, 13 centres

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TL;DR

The study investigates the chemical mechanisms underpinning symbiosis between tree frogs (Boana prasina) and their skin microbiome, specifically Pseudomonas bacteria.

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The study investigates the chemical mechanisms underpinning symbiosis between tree frogs (Boana prasina) and their skin microbiome, specifically Pseudomonas bacteria. MPFS as a carbon and energy source. Transcriptome analysis of frog skin revealed expression of enzymes (e.g., CPT1, CYP4B1) involved in acylcarnitine metabolism.

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other

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preclinical research

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ORIGINAL PAPER

PMC10587524

Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome

iScience

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ABSTRACT

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. Subject areas: Biological sciences, Microbiology, Microbial metabolism, Omics, Metabolomics

CITATION EXPORT

Andrés E Brunetti, Mariana L Lyra, Anelize Bauermeister et al.. Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome. iScience. (2023). https://doi.org/10.1016/j.isci.2023.108109

AUTHORS

15 · 13 CENTRES

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 GP Melo, Mônica T Pupo, Célio FB Haddad, Gabriela M Cabrera, Jörg Overmann, Norberto P Lopes

1Instituto de Biología Subtropical (IBS, UNaM-CONICET), Posadas, Misiones N3300LQH, Argentina
2NPPNS, Department of Biomolecular Sciences, Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo 14040-903, Brazil
3Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Hans-Knoell-Straße 8, 07745 Jena, Germany
4New York University Abu Dhabi, Saadiyat Island, Abu Dhabi 129188, United Arab Emirates
5Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, São Paulo 05508-000, Brazil
6Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, 38124 Braunschweig, Niedersachsen, Germany
7Central Facility for Microscopy, Helmholtz Centre for Infection Research (HZI), 38124 Braunschweig, Niedersachsen, Germany
8Northwest Metabolomics Research Center, Department of Anesthesiology and Pain Medicine, University of Washington, 850 Republican Street, Seattle, WA 98109, USA
9Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USA
10Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo 14040-903, Brazil
11Departamento de Biodiversidade e Centro de Aquicultura da UNESP (CAUNESP), Instituto de Biociências, UNESP-Universidade Estadual Paulista, Rio Claro, São Paulo 13506-900, Brazil
12Facultad de Ciencias Exactas y Naturales, Departamento de Química Orgánica, Universidad de Buenos Aires, Buenos Aires C1428EGA, Argentina
13Unidad de Microanálisis y Métodos Físicos aplicados a la Química Orgánica (UMYMFOR), Buenos Aires C1428EGA, Argentina

Andrés E Brunetti, Mariana L Lyra, Anelize Bauermeister et al.. Host macrocyclic acylcarnitines mediate symbiotic interactions between frogs and their skin microbiome. iScience. (2023). https://doi.org/10.1016/j.isci.2023.108109