Abstract
Streptomyces symbionts in insects have shown to be a valuable source of new antibiotics. Here, we report the genome sequence and the potential for antibiotic production of “Streptomyces sp. M54”, an Actinobacteria associated with the eusocial wasp, Polybia plebeja. The Streptomyces sp. M54 genome is composed of a chromosome (7.96 Mb), and a plasmid (1.91 Kb) and harbors 30 biosynthetic gene clusters for secondary metabolites, of which only one third has been previously characterized. Growth inhibition bioassays show that this bacterium produces antimicrobial compounds that are active against Hirsutella citriformis, a natural fungal enemy of its host, and the human pathogens Staphylococcus aureus and Candida albicans. Analyses through TLC-bioautography, LC–MS/MS and NMR allowed the identification of five macrocyclic ionophore antibiotics, with previously reported antibacterial, antitumor and antiviral properties. Phylogenetic analyses placed Streptomyces sp. M54 in a clade of other host-associated strains taxonomically related to Streptomyces griseus. Pangenomic and ANI analyses confirm the identity of one of its closest relatives as Streptomyces sp. LaPpAH-199, a strain isolated from an ant-plant symbiosis in Africa. In summary, our results suggest an insect-microbe association in distant geographic areas and showcase the potential of Streptomyces sp. M54 and related strains for the discovery of novel antibiotics.
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Acknowledgements
We grateful acknowledge Juan Carlos Cambronero-Heinrichs, Ronald Vargas and Lorena Hernandez for support in lab work, Federico Muñoz for providing guidance in the use of the computer cluster at CICIMA, and Reed Stubbendieck, Diego Dierick, Silver Ceballos and Lindsay McCulloch for comments on the manuscript. We thank La Selva Research Station (OTS), CIEMic, CIBCM, CIPRONA and CICIMA (Universidad de Costa Rica), for facilitating the use of research facilities.
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This work was financially supported by “Sistema de Estudios de Posgrado and Vicerrectoría de Investigación, Universidad de Costa Rica” (Research Projects 801-B0-538, 810-B5-772, and 809-B6-656).
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Conceived and designed the experiments: Adrián A. Pinto-Tomás, Catalina Murillo-Cruz, Max Chavarría, Giselle Tamayo-Castillo, Juan J. Araya and Bernal Matarrita-Carranza; Performed the experiments: María Isabel Ríos, María Luisa Gómez-Calvo, Roberto Avendaño, Catalina Murillo-Cruz and Bernal Matarrita-Carranza; Analyzed the data: Max Chavarría, Giselle Tamayo-Castillo, Adrián A. Pinto-Tomás, Catalina Murillo-Cruz and Bernal Matarrita-Carranza; Contributed reagents/materials/analysis tools: Adrián A. Pinto-Tomás, Catalina Murillo-Cruz, Max Chavarría, Giselle Tamayo-Castillo; Wrote the paper: Bernal Matarrita-Carranza, Catalina Murillo-Cruz, Max Chavarría, Giselle Tamayo-Castillo and Adrián A. Pinto-Tomás.
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Online_Resource_3.xlsx. Enrichment scores, p-values, and q-values for enrichment function analysis of cluster of orthologous groups (COGs) of all known Streptomyces genomes that harbor the macrotetrolide biosynthetic gene cluster. (XLSX 27 kb)
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Online_Resoure_4.xlsx. Biosynthetic gene cluster classification of 17 Streptomyces genomes used in BiG-SCAPE analysis. (XLSX 47 kb)
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Matarrita-Carranza, B., Murillo-Cruz, C., Avendaño, R. et al. Streptomyces sp. M54: an actinobacteria associated with a neotropical social wasp with high potential for antibiotic production. Antonie van Leeuwenhoek 114, 379–398 (2021). https://doi.org/10.1007/s10482-021-01520-y
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DOI: https://doi.org/10.1007/s10482-021-01520-y