Metabólitos do fungo mutualista das formigas atíneas como mediadores da interação com o parasita Escovopsis
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Data
2020-02-28
Autores
Oliveira, Karina Bueno de
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Universidade Estadual Paulista (Unesp)
Resumo
O jardim de fungo das formigas atíneas abriga uma microbiota diversa, que contempla interações microbianas mediadas por compostos químicos. Embora estudos investigaram os metabólitos produzidos pelos fungos cultivados (Leucoagaricus spp.) por esses insetos, nada se sabe a respeito dos compostos químicos que atuam na interação com Escovopsis sp., um fungo considerado parasita do parceiro fúngico das atíneas. Neste trabalho investigamos os metabólitos produzidos por três fungos mutualistas cultivados por diferentes formigas atíneas, para responder as seguintes perguntas: a) os metabólitos produzidos pelos fungos mutualistas medeiam a interação com Escovopsis sp.?; b) o dia de crescimento e a concentração dos metabólitos dos fungos mutualistas interferem na resposta de Escovopsis sp.?; c) compostos solúveis e voláteis estão envolvidos na interação? Para tanto, foram realizados bioensaios (i) com os filtrados dos três fungos mutualistas nas concentrações 1:1 e 1:10, obtidos em diferentes dias de cultivo; (ii) com a fração orgânica e subfrações desses filtrados frente a Escovopsis sp., (iii) de volatilidade entre os fungos mutualistas e Escovopsis sp.; além (iv) do estudo químico das frações e subfrações orgânicas. Como resultado, demonstramos que a interação Escovopsis-fungo mutualista é mediada por compostos químicos solúveis e voláteis, pois observamos uma maximização do crescimento micelial do parasita na presença tanto dos filtrados de cultivo dos fungos mutualistas, suas frações e subfrações, quanto nos experimentos de volatilidade. Além disso, identificamos duas substâncias da classe das dicetopiperazinas (subfrações Ϭ3 e Ϭ5) e o 5-hidroximetilfurfural. A dicetopiperazina da subfração Ϭ5 e o 5-hidroximetilfurfural atuam como sinalizadores envolvidos na interação Escovopsis-fungo mutualista, pois o parasita maximiza o crescimento na presença dessas substâncias. Tais compostos foram obtidos dos filtrados do 12º dia de crescimento de Leucoagaricus sp. AR04; no entanto, a resposta de crescimento maximizado do parasita independe das fases de crescimento do fungo mutualista, sendo tal fenômeno observado para os filtrados obtidos em todos os dias de cultivo desse micro-organismo. A antiga história evolutiva compartilhada entre esses dois fungos, talvez seja a responsável pela complexa interação química entre esses micro-organismos, especialmente à habilidade de reconhecimento de Escovopsis sp. para os compostos produzidos pelos fungos cultivados pelas formigas.
The fungus garden of attine ants harbors a diverse microbiota, whose members interact by chemical compounds. Although studies unraveled the metabolites produced by fungi cultivated (Leucoagaricus spp.) by these insects, little is known regarding the chemical compounds involved in the interaction with Escovopsis sp., a fungus known as a parasite of the ant fungal cultivars. Here, we investigated the metabolites produced by three mutualistic fungi cultivated by different attine ants to answer the following questions: a) Do the metabolites produced by the mutualistic fungi mediate the interaction with Escovopsis sp.?; b) Do the day of growth and the concentration of the metabolites interfere in the Escovopsis sp. response?; c) Are soluble and volatile compounds involved in this interaction? We addressed these questions by carrying out bioassays: (i) with culture filtrates of the three mutualistic fungi at two concentrations (1:1 and 1:10), obtained on different days of incubation; (ii) with the organic fraction and subfractions of these filtrates towards Escovopsis sp.; (iii) to determine volatile compounds are involved in the interaction; in addition to (iv) the chemical study of the organic fractions and subfractions. We demonstrated that the interaction between Escovopsis sp. and the mutualistic fungi of attine ants is mediated by soluble and volatile compounds, since we observed a maximization of the parasite's growth in the presence of both the mutualistic fungal culture filtrates, their fractions and subfractions, as well as in the volatility experiments. Also, we identified two substances from the class of diketopiperazines and the 5-hydroxymethylfurfural (subfractions Ϭ3 e Ϭ5). The diketopiperazine Ϭ5 and the 5-hydroxymethylfurfural act as signaling agents involved in the interaction Escovopsis sp. and the mutualistic fungus, because the parasite maximizes its growth in the presence of these substances. Such compounds were obtained from culture filtrates of the 12th day of growth of Leucoagaricus sp. AR04. However, the maximized growth response of the parasite did not depend on the growth phases of mutualistic fungi, because this response was observed in culture filtrates obtained on all days of cultivation of the mutualistic fungi. The ancient evolutionary history shared between these two fungi is likely responsible for the complexity of this chemical interaction, especially the ability of Escovopsis sp. to recognize the compounds produced by the ant fungal cultivars.
The fungus garden of attine ants harbors a diverse microbiota, whose members interact by chemical compounds. Although studies unraveled the metabolites produced by fungi cultivated (Leucoagaricus spp.) by these insects, little is known regarding the chemical compounds involved in the interaction with Escovopsis sp., a fungus known as a parasite of the ant fungal cultivars. Here, we investigated the metabolites produced by three mutualistic fungi cultivated by different attine ants to answer the following questions: a) Do the metabolites produced by the mutualistic fungi mediate the interaction with Escovopsis sp.?; b) Do the day of growth and the concentration of the metabolites interfere in the Escovopsis sp. response?; c) Are soluble and volatile compounds involved in this interaction? We addressed these questions by carrying out bioassays: (i) with culture filtrates of the three mutualistic fungi at two concentrations (1:1 and 1:10), obtained on different days of incubation; (ii) with the organic fraction and subfractions of these filtrates towards Escovopsis sp.; (iii) to determine volatile compounds are involved in the interaction; in addition to (iv) the chemical study of the organic fractions and subfractions. We demonstrated that the interaction between Escovopsis sp. and the mutualistic fungi of attine ants is mediated by soluble and volatile compounds, since we observed a maximization of the parasite's growth in the presence of both the mutualistic fungal culture filtrates, their fractions and subfractions, as well as in the volatility experiments. Also, we identified two substances from the class of diketopiperazines and the 5-hydroxymethylfurfural (subfractions Ϭ3 e Ϭ5). The diketopiperazine Ϭ5 and the 5-hydroxymethylfurfural act as signaling agents involved in the interaction Escovopsis sp. and the mutualistic fungus, because the parasite maximizes its growth in the presence of these substances. Such compounds were obtained from culture filtrates of the 12th day of growth of Leucoagaricus sp. AR04. However, the maximized growth response of the parasite did not depend on the growth phases of mutualistic fungi, because this response was observed in culture filtrates obtained on all days of cultivation of the mutualistic fungi. The ancient evolutionary history shared between these two fungi is likely responsible for the complexity of this chemical interaction, especially the ability of Escovopsis sp. to recognize the compounds produced by the ant fungal cultivars.
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Palavras-chave
Microbiologia, Crescimento, Escovopsis, Metabólitos, Crescimento microbiano, Reconhecimento químico, Biossinalização, Interação química, Chemical recognition, Biosignaling, Chemical interaction, Growth