First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris

Abstract Background Poison frogs are known for the outstanding diversity of alkaloid-based chemical defences with promising therapeutic applications. However, current knowledge about chemical defences in Dendrobatoidea superfamily has two sources of bias. First, cryptic, brown-colored species have b...

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Main Authors: Mabel Gonzalez, Pablo Palacios-Rodriguez, Jack Hernandez-Restrepo, Marco González-Santoro, Adolfo Amézquita, Andrés E. Brunetti, Chiara Carazzone
Format: Article
Language:English
Published: BMC 2021-08-01
Series:Frontiers in Zoology
Subjects:
Online Access:https://doi.org/10.1186/s12983-021-00420-1
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spelling doaj-6a28841e1fa74218afbcf69b827360c92021-08-29T11:30:35ZengBMCFrontiers in Zoology1742-99942021-08-0118111510.1186/s12983-021-00420-1First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventrisMabel Gonzalez0Pablo Palacios-Rodriguez1Jack Hernandez-Restrepo2Marco González-Santoro3Adolfo Amézquita4Andrés E. Brunetti5Chiara Carazzone6Department of Chemistry, Universidad de los AndesDepartment of Biological SciencesDepartment of Biological SciencesDepartment of Biological SciencesDepartment of Biological SciencesLaboratorio de Genética Evolutiva, Instituto de Biología Subtropical (CONICET - UNaM), Facultad de Ciencias Exactas, Universidad Nacional de MisionesDepartment of Chemistry, Universidad de los AndesAbstract Background Poison frogs are known for the outstanding diversity of alkaloid-based chemical defences with promising therapeutic applications. However, current knowledge about chemical defences in Dendrobatoidea superfamily has two sources of bias. First, cryptic, brown-colored species have been neglected in comparison to those conspicuously colored, and second, there has been little interest in characterizing metabolites other than alkaloids mediating defensive functions. In an effort to contribute to fill the gap of knowledge about cryptic species and broadening the spectrum of compounds analyzed we have applied head-space solid phase microextraction coupled to gas chromatography and mass spectrometry (HS-SPME/GC-MS) for extracting amphibian alkaloids and volatile organic compounds (VOCs) from Silverstoneia punctiventris. Results Using the skin from 8 specimens in 4 biological replicates we have found 33 different compounds. Twenty of them were classified as VOCs into 15 chemical classes including alkanes, alcohols, carbonyl compounds, methylpyridines, benzothiazoles, N-alkylpyrrolidines, pyrazines, and sesquiterpenoids, some of which were previously reported as repellents, defence compounds or defence pheromones in other organisms, and as sex pheromones in a treefrog. Interestingly, six of the remaining compounds were identified as alkaloids previously reported in other toxic/unpalatable dendrobatid frogs. Conclusions This is the first report of alkaloids and VOCs found in the Silverstoneia genus, which has been assumed for decades as non-chemically defended. This study establishes HS-SPME/GC-MS as a new application for a simultaneous approach to amphibian alkaloids and VOCs in poison frogs while opens up new research questions to assess the co-occurrence of both type of compounds and to investigate the evolutionary significance of a defence gradient that includes olfactory avoidance, unpalatability, and toxicity in dendrobatids. In addition, our results show that amphibian alkaloids could have a dual function (olfactory at distance, taste by contact) never explored before neither in Silverstonaeia nor in any other dendrobatid species.https://doi.org/10.1186/s12983-021-00420-1HS-SPME/GC-MSOdourChemical communicationAnti-predatory signalUnpalatabilityRepellent
collection DOAJ
language English
format Article
sources DOAJ
author Mabel Gonzalez
Pablo Palacios-Rodriguez
Jack Hernandez-Restrepo
Marco González-Santoro
Adolfo Amézquita
Andrés E. Brunetti
Chiara Carazzone
spellingShingle Mabel Gonzalez
Pablo Palacios-Rodriguez
Jack Hernandez-Restrepo
Marco González-Santoro
Adolfo Amézquita
Andrés E. Brunetti
Chiara Carazzone
First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris
Frontiers in Zoology
HS-SPME/GC-MS
Odour
Chemical communication
Anti-predatory signal
Unpalatability
Repellent
author_facet Mabel Gonzalez
Pablo Palacios-Rodriguez
Jack Hernandez-Restrepo
Marco González-Santoro
Adolfo Amézquita
Andrés E. Brunetti
Chiara Carazzone
author_sort Mabel Gonzalez
title First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris
title_short First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris
title_full First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris
title_fullStr First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris
title_full_unstemmed First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris
title_sort first characterization of toxic alkaloids and volatile organic compounds (vocs) in the cryptic dendrobatid silverstoneia punctiventris
publisher BMC
series Frontiers in Zoology
issn 1742-9994
publishDate 2021-08-01
description Abstract Background Poison frogs are known for the outstanding diversity of alkaloid-based chemical defences with promising therapeutic applications. However, current knowledge about chemical defences in Dendrobatoidea superfamily has two sources of bias. First, cryptic, brown-colored species have been neglected in comparison to those conspicuously colored, and second, there has been little interest in characterizing metabolites other than alkaloids mediating defensive functions. In an effort to contribute to fill the gap of knowledge about cryptic species and broadening the spectrum of compounds analyzed we have applied head-space solid phase microextraction coupled to gas chromatography and mass spectrometry (HS-SPME/GC-MS) for extracting amphibian alkaloids and volatile organic compounds (VOCs) from Silverstoneia punctiventris. Results Using the skin from 8 specimens in 4 biological replicates we have found 33 different compounds. Twenty of them were classified as VOCs into 15 chemical classes including alkanes, alcohols, carbonyl compounds, methylpyridines, benzothiazoles, N-alkylpyrrolidines, pyrazines, and sesquiterpenoids, some of which were previously reported as repellents, defence compounds or defence pheromones in other organisms, and as sex pheromones in a treefrog. Interestingly, six of the remaining compounds were identified as alkaloids previously reported in other toxic/unpalatable dendrobatid frogs. Conclusions This is the first report of alkaloids and VOCs found in the Silverstoneia genus, which has been assumed for decades as non-chemically defended. This study establishes HS-SPME/GC-MS as a new application for a simultaneous approach to amphibian alkaloids and VOCs in poison frogs while opens up new research questions to assess the co-occurrence of both type of compounds and to investigate the evolutionary significance of a defence gradient that includes olfactory avoidance, unpalatability, and toxicity in dendrobatids. In addition, our results show that amphibian alkaloids could have a dual function (olfactory at distance, taste by contact) never explored before neither in Silverstonaeia nor in any other dendrobatid species.
topic HS-SPME/GC-MS
Odour
Chemical communication
Anti-predatory signal
Unpalatability
Repellent
url https://doi.org/10.1186/s12983-021-00420-1
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