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

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Brunetti, Andres E. ; Lyra, Mariana L. ; Bauermeister, Anelize ; Bunk, Boyke ; Boedeker, Christian ; Muesken, Mathias ; Neto, Fausto Carnevale ; Mendonca, Jacqueline Nakau ; Caraballo-Rodriguez, Andres Mauricio ; Melo, Weilan G. P. ; Pupo, Monica T. ; Haddad, Celio F. B. ; Cabrera, Gabriela M. ; Overmann, Joerg ; Lopes, Norberto P.

• Document type: Journal article
• Source: ISCIENCE; v. 26, n. 11, p. 20-pg., 2023-10-16.

Abstract

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. (AU)

• FAPESP's process: 17/26162-8 - Diversity and conservation of Brazilian amphibians
• Grantee: Mariana Lúcio Lyra
• Support Opportunities: Scholarships in Brazil - Technical Training Program - Technical Training
• FAPESP's process: 21/10639-5 - Center for Research on Biodiversity Dynamics and Climate Change
• Grantee: Leonor Patricia Cerdeira Morellato
• Support Opportunities: Research Grants - Research, Innovation and Dissemination Centers - RIDC
• FAPESP's process: 20/02207-5 - Inventorying secondary metabolism applying metabolomic strategies: contribution to the Brazilian biodiversity valuation
• Grantee: Norberto Peporine Lopes
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants
• FAPESP's process: 17/23725-1 - Genomic Analysis of Skin Symbiotic Bacteria in Frogs as Potential Source of Volatile Compounds
• Grantee: Andrés Eduardo Brunetti
• Support Opportunities: Scholarships abroad - Research Internship - Post-doctor
• FAPESP's process: 12/21803-1 - Elicitation of natural products biosynthesis by endophytic microorganisms’ interaction
• Grantee: Andrés Mauricio Caraballo Rodríguez
• Support Opportunities: Scholarships in Brazil - Doctorate
• FAPESP's process: 14/50265-3 - Distribution and metabolism of natural and synthetic xenobiotics: from the comprehension of reactional process to tissue imaging generation
• Grantee: Norberto Peporine Lopes
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants
• FAPESP's process: 14/20915-6 - Chemical ecology in anurans: characterization of volatile compounds and peptide pheromones from the skin secretions of frogs
• Grantee: Andrés Eduardo Brunetti
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 17/17648-4 - Integrative approach on the sustainable prospection of marine natural products: from diversity to anticancer compounds
• Grantee: Anelize Bauermeister
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 14/01651-8 - Elicitation of natural products biosynthesis from endophytic microorganisms' interactions
• Grantee: Andrés Mauricio Caraballo Rodríguez
• Support Opportunities: Scholarships abroad - Research Internship - Doctorate
• FAPESP's process: 15/01001-6 - Discovering bacterial symbionts diversity associated with ants in different Brazilian biomes
• Grantee: Weilan Gomes da Paixão Melo
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 13/50954-0 - Novel therapeutic agents from the bacterial symbionts of Brazilian invertebrates
• Grantee: Mônica Tallarico Pupo
• Support Opportunities: BIOTA-FAPESP Program - Thematic Grants