Symbiotic skin bacteria as a source for sex-specific scents in frogs

Andrés E. Brunetti, Mariana L. Lyra, Weilan G. P. Melo, Laura E. Andrade, Pablo Palacios-Rodríguez, Bárbara M. Prado, Célio F. B. Haddad, Mônica T. Pupo, and Norberto P. Lopes
PNAS February 5, 2019 116 (6) 2124-2129; published ahead of print February 5, 2019 https://doi.org/10.1073/pnas.1806834116

  1. Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved December 19, 2018 (received for review April 22, 2018)

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Significance

Symbiotic microbes play pivotal roles in different aspects of animal biology. In particular, it has been increasingly recognized that they may produce molecules used by their host in social interactions. Herein, we report that symbiotic bacteria in amphibians can account for some odorous compounds found in the host. We found that sex-specific scents in a common South American tree frog can be traced to a class of compounds with strong odor properties produced by a bacterium isolated from the frog’s skin. This insight challenges our appreciation of the role of microorganisms in amphibians and not only reveals exciting perspectives into the analysis of a frog’s skin secretion, but also into the association and coevolution of host–microbe interactions in animals.

Abstract

Amphibians are known to possess a wide variety of compounds stored in their skin glands. While significant progress has been made in understanding the chemical diversity and biological relevance of alkaloids, amines, steroids, and peptides, most aspects of the odorous secretions are completely unknown. In this study, we examined sexual variations in the volatile profile from the skin of the tree frog Boana prasina and combined culture and culture-independent methods to investigate if microorganisms might be a source of these compounds. We found that sesquiterpenes, thioethers, and methoxypyrazines are major contributors to the observed sex differences. We also observed that each sex has a distinct profile of methoxypyrazines, and that the chemical origin of these compounds can be traced to a Pseudomonas sp. strain isolated from the frog’s skin. This symbiotic bacterium was present in almost all individuals examined from different sites and was maintained in captive conditions, supporting its significance as the source of methoxypyrazines in these frogs. Our results highlight the potential relevance of bacteria as a source of chemical signals in amphibians and contribute to increasing our understanding of the role that symbiotic associations have in animals.

Footnotes

  • ↵1To whom correspondence may be addressed. Email: andresbrunetti{at}gmail.com or npelopes{at}fcfrp.usp.br.

Published under the PNAS license.

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Symbiotic skin bacteria as a source for sex-specific scents in frogs
Andrés E. Brunetti, Mariana L. Lyra, Weilan G. P. Melo, Laura E. Andrade, Pablo Palacios-Rodríguez, Bárbara M. Prado, Célio F. B. Haddad, Mônica T. Pupo, Norberto P. Lopes
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 2124-2129; DOI: 10.1073/pnas.1806834116
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