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Accessing the specialized metabolome of actinobacteria from the bulk soil of Paullinia cupana Mart. on the Brazilian Amazon: a promising source of bioactive compounds against soybean phytopathogens

  • Soil and Agricultural Microbiology - Research Paper
  • Published:
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Abstract

The Amazon rainforest, an incredibly biodiverse ecosystem, has been increasingly vulnerable to deforestation. Despite its undeniable importance and potential, the Amazonian microbiome has historically received limited study, particularly in relation to its unique arsenal of specialized metabolites. Therefore, in this study our aim was to assess the metabolic diversity and the antifungal activity of actinobacterial strains isolated from the bulk soil of Paullinia cupana, a native crop, in the Brazilian Amazon Rainforest. Extracts from 24 strains were subjected to UPLC-MS/MS analysis using an integrative approach that relied on the Chemical Structural and Compositional Similarity (CSCS) metric, GNPS molecular networking, and in silico dereplication tools. This procedure allowed the comprehensive understanding of the chemical space encompassed by these actinobacteria, which consists of features belonging to known bioactive metabolite classes and several unannotated molecular families. Among the evaluated strains, five isolates exhibited bioactivity against a panel of soybean fungal phytopathogens (Rhizoctonia solani, Macrophomina phaseolina, and Sclerotinia sclerotiorum). A focused inspection led to the annotation of pepstatins, oligomycins, hydroxamate siderophores and dorrigocins as metabolites produced by these bioactive strains, with potentially unknown compounds also comprising their metabolomes. This study introduces a pragmatic protocol grounded in established and readily available tools for the annotation of metabolites and the prioritization of strains to optimize further isolation of specialized metabolites. Conclusively, we demonstrate the relevance of the Amazonian actinobacteria as sources for bioactive metabolites useful for agriculture. We also emphasize the importance of preserving this biome and conducting more in-depth studies on its microbiota.

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Data availability

The datasets generated and analysed during the current study are available in the MASSIVE repository under accession code: MSV000093749, https://massive.ucsd.edu/ProteoSAFe/static/massive.jsp.

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Acknowledgements

The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for financial support (scholarship grant 2022/01529-4 to N.M.M., and grant 2019/17721-9 to Roberto Gomes de Souza Berlinck). A scholarship to N.M.M. and G.A.A-C was also provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Finance Code 001). We cordially acknowledge Roberto Gomes de Souza Berlinck and Fabiana Tessari Rodrigues Martinelli who enabled the UPLC-MS/MS data acquisition, EMBRAPA Soybean for providing the fungal phytopathogenic strains for this study, and the staff members from the Federal University of Amazonas (UFAM) who collaborated with the collection of material for the isolation of microorganisms. The registration code of the microorganism’s strains used herein in the National System for the Management of Genetic Heritage and Associated Traditional Knowledge (SisGen) is A1900BF.

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  1. College of Agriculture “Luiz de Queiroz”, Department of Exact Sciences, University of São Paulo, Piracicaba, SP, 13418-900, Brazil

    Naydja Moralles Maimone & Simone Possedente de Lira

  2. College of Agriculture “Luiz de Queiroz”, Department of Genetics, University of São Paulo, Piracicaba, SP, 13418-900, Brazil

    Gladys Angélica Apaza-Castillo & Maria Carolina Quecine

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Maimone, N.M., Apaza-Castillo, G.A., Quecine, M.C. et al. Accessing the specialized metabolome of actinobacteria from the bulk soil of Paullinia cupana Mart. on the Brazilian Amazon: a promising source of bioactive compounds against soybean phytopathogens. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01286-1

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