Characteristics of marine strain Streptomyces sp. with antimicrobial and cytotoxic activity
Keywords:
marine actinobacteria; Streptomyces; genome; exometabolite; cytotoxic activity; antimicrobial activity.
Abstract
The Black Sea is a unique water basin consisting of a thin superficial oxygenic layer with moderate salinity, and a deep anoxic water mass. The microbiota of the Black Sea remains relatively understudied, which makes it interesting first of all from the most practical point of view of the search for producers of new biologically active compounds. A strain of actinobacteria Streptomyces sp. ONU 561 was isolated from the surface of mussel shells collected in the coastal zone of Odesa. It demonstrated a wide range of antagonistic activity, inhibiting the growth of a set of opportunistic pathogens, including representatives of Staphylococcus aureus, Escherichia coli, Proteus vulgaris, and Klebsiella pneumoniae. In addition, bacteria of this strain were able to inhibit the growth of all tested strains of mycelial fungi, including representatives of Aspergillus niger, A. flavus and Fusarium oxysporum species, and Candida albicans yeast. A significant cytotoxic effect was revealed in the cell cultures of human malignant cells – human rhabdomyosarcoma (RD) and human laryngeal adenocarcinoma (Hep-2). Analysis of the exometabolome of the strain did not explain these effects.The strain was comprehensively characterized, including physiological, biochemical, and morphological traits. The complete genome of the strain was sequenced using Illumina HiSeq 4000 (2x150) and ONT and annotated using NCBI PGAP. Its genome has a size of 8 359 197 bp. GC content – 71.59%. Using antiSMASH 7.0, 35 biosynthetic clusters were revealed. The indices of digital DNA-DNA hybridization and orthoANI for all of the type strains with Streptomyces sp. ONU 561 are much lower than threshold values for the species separation. The obtained results, including a comparative analysis of the genome, indicate the possible affiliation of the strain Streptomyces sp. ONU 561 to a new species and the potential ability of these actinobacteria to synthesize previously unknown antibiotic compounds.References
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Amelia-Yap, Z. H., Azman, A. S., AbuBakar, S., & Low, V. L. (2022). Streptomyces derivatives as an insecticide: Current perspectives, challenges and future research needs for mosquito control. Acta Tropica, 229, 106381.
Arumugam, M., Mitra, A., Jaisankar, P., Dasgupta, S., Sen, T., Gachhui, R., Mukhopadhyay, U. K., & Mukherjee, J. (2010). Isolation of an unusual metabolite 2-allyloxyphenol from a marine actinobacterium, its biological activities and applications. Applied Microbiology аnd Biotechnology, 86, 109–117.
Blin, K., Simon, S., Augustijn, H. E., Reitz, Z. L., Biermann, F., Alanjary, M., Fetter, A., Terlouw, B. R., Metcalf, W. W., Helfrich, E. J. N., van Wezel, G. P., Medema, M. H., & Weber, T. (2023). antiSMASH 7.0: New and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Research, 51(1), 46–50.
Bojarska, J., & Wolf, W. M. (2020). Ultra-short cyclo-peptides as bio-inspired therapeutics: Proline-based 2, 5-diketopiperazines (DKP). Proceedings, 79(1), 10.
Buckingham, J. (Ed.). (2023). Dictionary of natural products. Routledge, New York.
Canu, N., Moutiez, M., Belin, P., & Gondry, M. (2020). Cyclodipeptide synthases: A promising biotechnological tool for the synthesis of diverse 2, 5-diketopiperazines. Natural Product Reports, 37(3), 312–321.
Chen, W., Ye, K., Zhu, X., Zhang, H., Si, R., Chen, J., Chen, Z., Song, K., Yu, Z., & Han, B. (2021). Actinomycin X2, an antimicrobial depsipeptide from marine-derived Streptomyces cyaneofuscatus applied as a good natural dye for silk fabric. Marine Drugs, 20(1), 16.
Espinoza, L. E., Davelos Baines, A. L., & Lowe, K. L. (2013). Biochemical, nutrient and inhibitory characteristics of Streptomyces cultured from a hypersaline estuary, the Laguna Madre (Texas). OnLine Journal of Biological Sciences, 13(1), 18–27.
Galkin, B. M., Filipova, Т. О., Ivanytsia, V. О., & Gudzenko, Т. V. (2022). Bioaktyvni vtorynni metabolity z morskykh mikroorhanizmiv [Biologically active metabolites from marine microorganisms]. Odesa National University Press, Odesa (in Ukrainian).
García-Davis, S., Reyes, C. P., Lagunes, I., Padrón, J. M., Fraile-Nuez, E., Fernández, J. J., & Díaz-Marrero, A. R. (2021). Bioprospecting antiproliferative marine microbiota from submarine volcano Tagoro. Frontiers in Marine Science, 8, 687701.
Ghashghaei, S., Etemadifar, Z., Tavassoli, M., & Mofid, M. R. (2023). Optimization of degenerate PCR conditions for reducing error rates in detection of PKS and NRPS gene groups in actinomycetes. Avicenna Journal of Medical Biotechnology, 15(1), 28.
Goodfellow, M. (2012). Actinobacteria phyl. nov. Bergey’s Manual of Systematics of Archaea and Bacteria. Springer New York Dordrecht Heidelberg London.
Gulder, T. A., & Moore, B. S. (2010). Salinosporamide natural products: Potent 20 S proteasome inhibitors as promising cancer chemotherapeutics. Angewandte Chemie International Edition, 49(49), 9346–9367.
Jaiani, E., Kusradze, I., Kokashvili, T., Geliashvili, N., Janelidze, N., Kotorashvili, A., Kotaria, N., Guchmanidze, A., Tediashvili, M., & Prangishvili, D. (2020). Microbial diversity and phage–host interactions in the Georgian coastal area of the Black Sea revealed by whole genome metagenomic sequencing. Marine Drugs, 18(11), 558.
Kämpfer, P. (2015). Streptomyces. In: Bergey's Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, Ltd.
Karim, M. R. U., In, Y., Zhou, T., Harunari, E., Oku, N., & Igarashi, Y. (2021). Nyuzenamides A and B: Bicyclic peptides with antifungal and cytotoxic activity from a marine-derived Streptomyces sp. Organic Letters, 23(6), 2109–2113.
Kim, H. J., Bo, A. B., Kim, J. D., Kim, Y. S., Khaitov, B., Ko, Y. K., Cho, K. M., Jang, K. S., Park, K. W., & Choi, J. S. (2020). Herbicidal characteristics and structural identification of the potential active compounds from Streptomyces sp. KRA17-580. Journal of Agricultural and Food Chemistry, 68(52), 15373–15380.
Korotaeva, N. V., Strashnova, I. V., Vasylieva, N. Y., Potapenko, K. S., Metelitsyna, I. P., Filipova, T. O., & Ivanytsia, V. O. (2021). Kharakterystyka aktynobakterii, izolovanykh iz Mytilus galloprovincialis Odeskoi zatoky Chornoho moria [Characteristics of actinobacteria from Mytilus galloprovincialis in Odessa gulf, Black Sea]. Microbiology and Biotechnology, 3, 84–98 (in Ukrainian).
Landwehr, W., Wolf, C., & Wink, J. (2016) Actinobacteria and Myxobacteria – two of the most important bacterial resources for novel antibiotics. In: Current topics in microbiology and immunology. Springer International Publishing Switzerland.
Letunic, I., & Bork, P. (2021). Interactive tree of life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic acids Research, 49(W1), 293–296.
Li, Q., Chen, X., Jiang, Y., & Jiang, C. (2016). Morphological identification of Actinobacteria. In: Actinobacteria – basics and biotechnological applications. IntechOpen. Pp. 59–86.
Malve, H. (2016). Exploring the ocean for new drug developments: Marine pharmacology. Journal of Pharmacy & Bioallied Sciences, 8(2), 83.
Meier-Kolthoff, J. P., Auch, A. F., Klenk, H. P., & Göker, M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics, 14, 60.
Meier-Kolthoff, J. P., Carbasse, J. S., Peinado-Olarte, R. L., & Göker, M. (2022). TYGS and LPSN: A database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Research, 50(1), 801–807.
Mu, Y., Jiang, Y., Qu, X., Liu, B., Tan, J., Li, G., Jiang, M., Li, L., Li Han, L., & Huang, X. (2021). Oxazolomycins produced by Streptomyces glaucus and their cytotoxic activity. RSC Advances, 11(55), 35011–35019.
Ngamcharungchit, C., Chaimusik, N., Panbangred, W., Euanorasetr, J., & Intra, B. (2023). Bioactive metabolites from terrestrial and marine actinomycetes. Molecules, 28(15), 5915.
Nodwell, J. R. (2007). Novel links between antibiotic resistance and antibiotic production. Journal of Bacteriology, 189(10), 3683–3685.
Oleksak, P., Gonda, J., Nepovimova, E., Kuca, K., & Musilek, K. (2020). The oxazolomycin family: A review of current knowledge. RSC Advances, 10(67), 40745–40794.
Oren, A., & Garrity, G. M. (2022). Notification that new names of prokaryotes, new combinations, and new taxonomic opinions have appeared in volume 71, 10 of the IJSEM. International Journal of Systematic and Evolutionary Microbiology, 72(1), 10–15.
Otsuka, M., Fujita, M., Matsushima, Y., Eguchi, T., Shindo, K., Kakinuma, K. (2000). Biosynthetic pathway of macrolactam polyketide glycoside antitumor antibiotic vicenistatins. Tetrahedron, 56(42), 8281–8286.
Papon, N., Copp, B. R., & Courdavault, V. (2022). Marine drugs: Biology, pipelines, current and future prospects for production. Biotechnology Advances, 54, 107871.
Paulus, C., Rebets, Y., Tokovenko, B., Nadmid, S., Terekhova, L. P., Myronovskyi, M., Zotchev, S. B., Rückert, C., Braig, S., Zahler, S., Kalinowski, J., & Luzhetskyy, A. (2017). New natural products identified by combined genomics-metabolomics profiling of marine Streptomyces sp. MP131-18. Scientific Reports, 7(1), 42382.
Potapenko, K. S., Korotaeva, N. V., & Ivanitsa, V. O. (2021). Vtorynni metabolity morskykh aktynobakterii z antybiotychnoiu aktyvnistiu [Secondary metabolites of marine actinobacteria with antibiotic activity]. Microbiology and Biotechnology, 3, 28–43 (in Ukrainian).
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), 590–596.
Ravindragouda, P., Jeyasekaran, G., & Shanmugam, S. A. (2016). A novel, cost-effective cover slip holder for in situ microscopy of cover slip cultures of actinomycetes. Life Sciences Leaflets, 79, 60–64.
Ruiz-Torres, V., Encinar, J. A., Herranz-Lopez, M., Pérez-Sánchez, A., Galiano, V., Barrajón-Catalán, E., & Micol, V. (2017). An updated review on marine anticancer compounds: The use of virtual screening for the discovery of small-molecule cancer drugs. Molecules, 22(7), 1037.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425.
Salim, A. A., Samarasekera, K., Khalil, Z. G., & Capon, R. J. (2020). Exploring natural product artifacts: The polyketide enterocin warms to a ballet of isomers. Organic Letters, 22(12), 4828–4832.
Schauner, C., Dary, A., Lebrihi, A., Leblond, P., Decaris, B., & Germain, P. (1999). Modulation of lipid metabolism and spiramycin biosynthesis in Streptomyces ambofaciens unstable mutants. Applied and Environmental Microbiology, 65(6), 2730–2737.
Shirling, E. B., & Gottlieb, D. (1968). Cooperative description of type cultures of Streptomyces III. Additional species descriptions from first and second studies. International Journal of Systematic and Evolutionary Microbiology, 18(4), 279–392.
Stackebrandt, E., Witt, D., Kemmerling, C., Kroppenstedt, R., & Liesack, W. (1991). Designation of streptomycete 16S and 23S rRNA-based target regions for oligonucleotide probes. Applied and Environmental Microbiology, 57(5), 1468–1477.
Suzuki, M., Komaki, H., Kaweewan, I., Dohra, H., Hemmi, H., Nakagawa, H., Yamamura, H., Hayakawa, M., & Kodani, S. (2021). Isolation and structure determination of new linear azole-containing peptides spongiicolazolicins A and B from Streptomyces sp. CWH03. Applied Microbiology and Biotechnology, 105, 93–104.
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027.
Tian, Z., Lu, X. T., Jiang, X., & Tian, J. (2023). Bryostatin-1: A promising compound for neurological disorders. Frontiers in Pharmacology, 14, 1187411.
Vasyleva, N. Y., Krylova, K. D., Kristoffersen, J. B., Dubrovina, O. А., Ivanytsia, V. O. (2018). Mikrobna riznomanitnist’ pryberezhnykh vod Odeskoi zatoky Chornoho moria [Microbial diversity of coastal waters of Odesa Bay of the Black Sea]. Microbiology and Biotechnology, 4, 63–75 (in Ukrainian).
Xu, D. B., Ma, M., Deng, Z. X., & Hong, K. (2015). Genotype-driven isolation of enterocin with novel bioactivities from mangrove-derived Streptomyces qinglanensis 172205. Applied Microbiology and Biotechnology, 99, 5825–5832.
Yamada, Y., Kuzuyama, T., Komatsu, M., Shin-Ya, K., Omura, S., Cane, D. E., & Ikeda, H. (2015). Terpene synthases are widely distributed in bacteria. Proceedings of the National Academy of Sciences, 112(3), 857–862.
Yoon, S. H., Ha, S. M., Kwon, S., Lim, J., Kim, Y., Seo, H., & Chun, J. (2017). Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67(5), 1613.
Zhang, J. C., Yang, Y. B., Zhou, H., Peng, T. F., Yang, F. F., Xu, L. H., & Ding, Z. T. (2014). Medelamine C, A new ω-hydroxy alkylamine derivative from endophytic Streptomyces sp. YIM 66142. Natural Product Communications, 9(1), 99–100.
Zhang, S., Chen, Y., Zhu, J., Lu, Q., Cryle, M. J., Zhang, Y., & Yan, F. (2023). Structural diversity, biosynthesis, and biological functions of lipopeptides from Streptomyces. Natural Product Reports, 40(3), 557–594.
Amelia-Yap, Z. H., Azman, A. S., AbuBakar, S., & Low, V. L. (2022). Streptomyces derivatives as an insecticide: Current perspectives, challenges and future research needs for mosquito control. Acta Tropica, 229, 106381.
Arumugam, M., Mitra, A., Jaisankar, P., Dasgupta, S., Sen, T., Gachhui, R., Mukhopadhyay, U. K., & Mukherjee, J. (2010). Isolation of an unusual metabolite 2-allyloxyphenol from a marine actinobacterium, its biological activities and applications. Applied Microbiology аnd Biotechnology, 86, 109–117.
Blin, K., Simon, S., Augustijn, H. E., Reitz, Z. L., Biermann, F., Alanjary, M., Fetter, A., Terlouw, B. R., Metcalf, W. W., Helfrich, E. J. N., van Wezel, G. P., Medema, M. H., & Weber, T. (2023). antiSMASH 7.0: New and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Research, 51(1), 46–50.
Bojarska, J., & Wolf, W. M. (2020). Ultra-short cyclo-peptides as bio-inspired therapeutics: Proline-based 2, 5-diketopiperazines (DKP). Proceedings, 79(1), 10.
Buckingham, J. (Ed.). (2023). Dictionary of natural products. Routledge, New York.
Canu, N., Moutiez, M., Belin, P., & Gondry, M. (2020). Cyclodipeptide synthases: A promising biotechnological tool for the synthesis of diverse 2, 5-diketopiperazines. Natural Product Reports, 37(3), 312–321.
Chen, W., Ye, K., Zhu, X., Zhang, H., Si, R., Chen, J., Chen, Z., Song, K., Yu, Z., & Han, B. (2021). Actinomycin X2, an antimicrobial depsipeptide from marine-derived Streptomyces cyaneofuscatus applied as a good natural dye for silk fabric. Marine Drugs, 20(1), 16.
Espinoza, L. E., Davelos Baines, A. L., & Lowe, K. L. (2013). Biochemical, nutrient and inhibitory characteristics of Streptomyces cultured from a hypersaline estuary, the Laguna Madre (Texas). OnLine Journal of Biological Sciences, 13(1), 18–27.
Galkin, B. M., Filipova, Т. О., Ivanytsia, V. О., & Gudzenko, Т. V. (2022). Bioaktyvni vtorynni metabolity z morskykh mikroorhanizmiv [Biologically active metabolites from marine microorganisms]. Odesa National University Press, Odesa (in Ukrainian).
García-Davis, S., Reyes, C. P., Lagunes, I., Padrón, J. M., Fraile-Nuez, E., Fernández, J. J., & Díaz-Marrero, A. R. (2021). Bioprospecting antiproliferative marine microbiota from submarine volcano Tagoro. Frontiers in Marine Science, 8, 687701.
Ghashghaei, S., Etemadifar, Z., Tavassoli, M., & Mofid, M. R. (2023). Optimization of degenerate PCR conditions for reducing error rates in detection of PKS and NRPS gene groups in actinomycetes. Avicenna Journal of Medical Biotechnology, 15(1), 28.
Goodfellow, M. (2012). Actinobacteria phyl. nov. Bergey’s Manual of Systematics of Archaea and Bacteria. Springer New York Dordrecht Heidelberg London.
Gulder, T. A., & Moore, B. S. (2010). Salinosporamide natural products: Potent 20 S proteasome inhibitors as promising cancer chemotherapeutics. Angewandte Chemie International Edition, 49(49), 9346–9367.
Jaiani, E., Kusradze, I., Kokashvili, T., Geliashvili, N., Janelidze, N., Kotorashvili, A., Kotaria, N., Guchmanidze, A., Tediashvili, M., & Prangishvili, D. (2020). Microbial diversity and phage–host interactions in the Georgian coastal area of the Black Sea revealed by whole genome metagenomic sequencing. Marine Drugs, 18(11), 558.
Kämpfer, P. (2015). Streptomyces. In: Bergey's Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, Ltd.
Karim, M. R. U., In, Y., Zhou, T., Harunari, E., Oku, N., & Igarashi, Y. (2021). Nyuzenamides A and B: Bicyclic peptides with antifungal and cytotoxic activity from a marine-derived Streptomyces sp. Organic Letters, 23(6), 2109–2113.
Kim, H. J., Bo, A. B., Kim, J. D., Kim, Y. S., Khaitov, B., Ko, Y. K., Cho, K. M., Jang, K. S., Park, K. W., & Choi, J. S. (2020). Herbicidal characteristics and structural identification of the potential active compounds from Streptomyces sp. KRA17-580. Journal of Agricultural and Food Chemistry, 68(52), 15373–15380.
Korotaeva, N. V., Strashnova, I. V., Vasylieva, N. Y., Potapenko, K. S., Metelitsyna, I. P., Filipova, T. O., & Ivanytsia, V. O. (2021). Kharakterystyka aktynobakterii, izolovanykh iz Mytilus galloprovincialis Odeskoi zatoky Chornoho moria [Characteristics of actinobacteria from Mytilus galloprovincialis in Odessa gulf, Black Sea]. Microbiology and Biotechnology, 3, 84–98 (in Ukrainian).
Landwehr, W., Wolf, C., & Wink, J. (2016) Actinobacteria and Myxobacteria – two of the most important bacterial resources for novel antibiotics. In: Current topics in microbiology and immunology. Springer International Publishing Switzerland.
Letunic, I., & Bork, P. (2021). Interactive tree of life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic acids Research, 49(W1), 293–296.
Li, Q., Chen, X., Jiang, Y., & Jiang, C. (2016). Morphological identification of Actinobacteria. In: Actinobacteria – basics and biotechnological applications. IntechOpen. Pp. 59–86.
Malve, H. (2016). Exploring the ocean for new drug developments: Marine pharmacology. Journal of Pharmacy & Bioallied Sciences, 8(2), 83.
Meier-Kolthoff, J. P., Auch, A. F., Klenk, H. P., & Göker, M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics, 14, 60.
Meier-Kolthoff, J. P., Carbasse, J. S., Peinado-Olarte, R. L., & Göker, M. (2022). TYGS and LPSN: A database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Research, 50(1), 801–807.
Mu, Y., Jiang, Y., Qu, X., Liu, B., Tan, J., Li, G., Jiang, M., Li, L., Li Han, L., & Huang, X. (2021). Oxazolomycins produced by Streptomyces glaucus and their cytotoxic activity. RSC Advances, 11(55), 35011–35019.
Ngamcharungchit, C., Chaimusik, N., Panbangred, W., Euanorasetr, J., & Intra, B. (2023). Bioactive metabolites from terrestrial and marine actinomycetes. Molecules, 28(15), 5915.
Nodwell, J. R. (2007). Novel links between antibiotic resistance and antibiotic production. Journal of Bacteriology, 189(10), 3683–3685.
Oleksak, P., Gonda, J., Nepovimova, E., Kuca, K., & Musilek, K. (2020). The oxazolomycin family: A review of current knowledge. RSC Advances, 10(67), 40745–40794.
Oren, A., & Garrity, G. M. (2022). Notification that new names of prokaryotes, new combinations, and new taxonomic opinions have appeared in volume 71, 10 of the IJSEM. International Journal of Systematic and Evolutionary Microbiology, 72(1), 10–15.
Otsuka, M., Fujita, M., Matsushima, Y., Eguchi, T., Shindo, K., Kakinuma, K. (2000). Biosynthetic pathway of macrolactam polyketide glycoside antitumor antibiotic vicenistatins. Tetrahedron, 56(42), 8281–8286.
Papon, N., Copp, B. R., & Courdavault, V. (2022). Marine drugs: Biology, pipelines, current and future prospects for production. Biotechnology Advances, 54, 107871.
Paulus, C., Rebets, Y., Tokovenko, B., Nadmid, S., Terekhova, L. P., Myronovskyi, M., Zotchev, S. B., Rückert, C., Braig, S., Zahler, S., Kalinowski, J., & Luzhetskyy, A. (2017). New natural products identified by combined genomics-metabolomics profiling of marine Streptomyces sp. MP131-18. Scientific Reports, 7(1), 42382.
Potapenko, K. S., Korotaeva, N. V., & Ivanitsa, V. O. (2021). Vtorynni metabolity morskykh aktynobakterii z antybiotychnoiu aktyvnistiu [Secondary metabolites of marine actinobacteria with antibiotic activity]. Microbiology and Biotechnology, 3, 28–43 (in Ukrainian).
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), 590–596.
Ravindragouda, P., Jeyasekaran, G., & Shanmugam, S. A. (2016). A novel, cost-effective cover slip holder for in situ microscopy of cover slip cultures of actinomycetes. Life Sciences Leaflets, 79, 60–64.
Ruiz-Torres, V., Encinar, J. A., Herranz-Lopez, M., Pérez-Sánchez, A., Galiano, V., Barrajón-Catalán, E., & Micol, V. (2017). An updated review on marine anticancer compounds: The use of virtual screening for the discovery of small-molecule cancer drugs. Molecules, 22(7), 1037.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425.
Salim, A. A., Samarasekera, K., Khalil, Z. G., & Capon, R. J. (2020). Exploring natural product artifacts: The polyketide enterocin warms to a ballet of isomers. Organic Letters, 22(12), 4828–4832.
Schauner, C., Dary, A., Lebrihi, A., Leblond, P., Decaris, B., & Germain, P. (1999). Modulation of lipid metabolism and spiramycin biosynthesis in Streptomyces ambofaciens unstable mutants. Applied and Environmental Microbiology, 65(6), 2730–2737.
Shirling, E. B., & Gottlieb, D. (1968). Cooperative description of type cultures of Streptomyces III. Additional species descriptions from first and second studies. International Journal of Systematic and Evolutionary Microbiology, 18(4), 279–392.
Stackebrandt, E., Witt, D., Kemmerling, C., Kroppenstedt, R., & Liesack, W. (1991). Designation of streptomycete 16S and 23S rRNA-based target regions for oligonucleotide probes. Applied and Environmental Microbiology, 57(5), 1468–1477.
Suzuki, M., Komaki, H., Kaweewan, I., Dohra, H., Hemmi, H., Nakagawa, H., Yamamura, H., Hayakawa, M., & Kodani, S. (2021). Isolation and structure determination of new linear azole-containing peptides spongiicolazolicins A and B from Streptomyces sp. CWH03. Applied Microbiology and Biotechnology, 105, 93–104.
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027.
Tian, Z., Lu, X. T., Jiang, X., & Tian, J. (2023). Bryostatin-1: A promising compound for neurological disorders. Frontiers in Pharmacology, 14, 1187411.
Vasyleva, N. Y., Krylova, K. D., Kristoffersen, J. B., Dubrovina, O. А., Ivanytsia, V. O. (2018). Mikrobna riznomanitnist’ pryberezhnykh vod Odeskoi zatoky Chornoho moria [Microbial diversity of coastal waters of Odesa Bay of the Black Sea]. Microbiology and Biotechnology, 4, 63–75 (in Ukrainian).
Xu, D. B., Ma, M., Deng, Z. X., & Hong, K. (2015). Genotype-driven isolation of enterocin with novel bioactivities from mangrove-derived Streptomyces qinglanensis 172205. Applied Microbiology and Biotechnology, 99, 5825–5832.
Yamada, Y., Kuzuyama, T., Komatsu, M., Shin-Ya, K., Omura, S., Cane, D. E., & Ikeda, H. (2015). Terpene synthases are widely distributed in bacteria. Proceedings of the National Academy of Sciences, 112(3), 857–862.
Yoon, S. H., Ha, S. M., Kwon, S., Lim, J., Kim, Y., Seo, H., & Chun, J. (2017). Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67(5), 1613.
Zhang, J. C., Yang, Y. B., Zhou, H., Peng, T. F., Yang, F. F., Xu, L. H., & Ding, Z. T. (2014). Medelamine C, A new ω-hydroxy alkylamine derivative from endophytic Streptomyces sp. YIM 66142. Natural Product Communications, 9(1), 99–100.
Zhang, S., Chen, Y., Zhu, J., Lu, Q., Cryle, M. J., Zhang, Y., & Yan, F. (2023). Structural diversity, biosynthesis, and biological functions of lipopeptides from Streptomyces. Natural Product Reports, 40(3), 557–594.
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2023-11-24
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