Abstract
The members of Streptomyces have been identified as a major source of antimicrobial agents with broad spectrum. This study is mainly focused on bioactivity-guided isolation and characterization of bioactive molecule from strain Streptomyces sp. T1317-0309 and its whole-genome sequence analysis for possible isolation of novel natural products. Strain Streptomyces sp. T1317-0309 showed 100% sequence similarity with strain Streptomyces lannensis TA4-8T consisting 10, 453,255 bp of genome with 5 scaffolds and 69.9 mol% G + C content. The genome analyses revealed a total of 17 putative biosynthetic gene clusters (BGCs) responsible for various secondary metabolites including actinomycin, bacteriocin, ectoine, melanin, terpene, siderophore, betalactone, NRPS, T2PKS, and T3PKS. The BGC and bioactivity-guided purification of ethyl acetate extract of strain T1317-0309 showed the great potency of antimicrobial activities against various gram-positive multi-drug resistant human pathogens including MRSA. The BGC-predicted bioactive secondary metabolite was identified by various NMR analyses and confirmed as actinomycin D. In addition, this study reveals the first genome study of Streptomyces lannensis as a novel source for actinomycin D.
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References
Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health. 2015;109:309–18.
Dahal RH, Chaudhary DK. Microbial infections and antimicrobial resistance in Nepal: current trends and recommendations. Open Microbiol J. 2018;12:230–42.
Terra L, et al. A novel alkaliphilic Streptomyces inhibits ESKAPE pathogens. Front Microbiol. 2018;9:2458.
Lewis K. Platforms for antibiotic discovery. Nat Rev Drug Disco. 2013;12:371–87.
Dryden MS, et al. Predictors of mortality in Staphylococcus aureus Bacteremia. Clin Microbiol Rev. 2011;25:362–86.
Dahal RH, Shim DS, Kim J. Development of actinobacterial resources for functional cosmetics. J Cosmet Dermatol. 2017;16:243–52.
Schneider O, et al. Genome mining of Streptomyces sp. YIM 130001 isolated from lichen affords new thiopeptide antibiotic. Front Microbiol. 2018;9:3139.
Lackner H, Bahner I, Shigematsu N, Pannell LK, Mauger AB. Structures of five components of the actinomycin Z complex from Streptomyces fradiae, two of which contain 4-chlorothreonine. J Nat Prod. 2000;63:352–6.
Jones GH. Actinomycin production persists in a strain of Streptomyces antibioticus lacking phenoxazinone synthase. Antimicrob Agents Chemother. 2000;44:1322–7.
Sharma M, Manhas RK. Purification and characterization of actinomycins from Streptomyces strain M7 active against methicillin resistant Staphylococcus aureus and vancomycin resistant Enterococcus. BMC Microbiol. 2019;19:44.
Zhang X, Ye X, Chai W, Lian X-Y, Zhang Z. New metabolites and bioactive actinomycins from marine-derived Streptomyces sp. ZZ338. Mar Drugs. 2016;14:181.
Hollstein U, Breitmaier E, Jung G. Carbon-13 nuclear magnetic resonance study of actinomycin D. J Am Chem Soc. 1974;96:8036–40.
Singh SB, Genilloud O, Peláez F. Terrestrial microorganisms – filamentous bacteria. In: Mander L, Lui H-W, editors. Comprehensive natural products II. Oxford: Elsevier; 2010. p. 109–40.
Hu D, et al. Genome guided investigation of antibiotics producing actinomycetales strain isolated from a Macau mangrove ecosystem. Sci Rep. 2018;8:1–12.
Nguyen HT, et al. Streptomyces sp. VN1, a producer of diverse metabolites including non-natural furan-type anticancer compound. Sci Rep. 2020;10:1–14.
Nguyen TM, Seo C, Ji M, Paik MJ, Myung SW, Kim J. Effective soil extraction method for cultivating previously uncultured soil bacteria. Appl Environ Microbiol. 2018;84:e01145–18.
Frank JA, et al. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol. 2008;74:2461–70.
Tatusova T, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614–24.
Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics. 2018;34:1037–9.
Aziz RK, et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75.
Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005;33:W686–9.
Lagesen K, Hallin P, Rødland EA, Stærfeldt H-H, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35:3100–8.
Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.
Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 2019;47:W81–7.
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67:1613–7.
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.
Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.
Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek. 2017;110:1281–6.
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 2013;14:60.
CLSI. M07-A10 Methods for dilution antimicrobial susceptibility sests for bacteria that grow aerobically. Approved standard-tenth ed. Wayne, PA: Clinical & Laboratory Standards Institute; 2015. www.clsi.org.
Arhin FF, et al. Effect of polysorbate 80 on oritavancin binding to plastic surfaces: implications for susceptibility testing. Antimicrob Agents Chemother. 2008;52:1597–603.
Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci. 2009;106:19126–31.
Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res. 2008;36:W181–4.
Mauger AB, Thomas WA. NMR studies of actinomycins varying at the proline sites. Org Magn Reson. 1981;17:186–90.
Chen C, Song F, Wang Q, Abdel-Mageed WM, Guo H, Fu C, et al. A marine-derived Streptomyces sp. MS449 produces high yield of actinomycin X2 and actinomycin D with potent anti-tuberculosis activity. Appl Microbiol Biotechnol. 2012;95:919–27.
Praveen V, Tripathi CKM, Bihari V, Srivastava SC. Production of actinomycin-D by a new isolate, Streptomyces sindenensis. Ann Microbiol. 2008;58:109–14.
Praveen V, Tripathi CKM. Studies on the production of actinomycin-D by Streptomyces griseoruber- a novel source. Lett Appl Microbiol. 2009;49:450–5.
Praveen V, Tripathi CKM, Bihari V. Studies on optimum fermentation conditions for actinomycin-D production by two new strains of Streptomyces spp. Med Chem Res. 2008;17:114–22.
Wei Z, Xu C, Wang J, Lu F, Bie X, Lu Z. Identification and characterization of Streptomyces flavogriseus NJ-4 as a novel producer of actinomycin D and holomycin. PeerJ. 2017;2017:1–19.
Wang D, et al. Identification, bioactivity, and productivity of actinomycins from the marine-derived Streptomyces heliomycini. Front Microbiol. 2017;8:1147.
Funding
This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1F1A1058501).
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Dahal, R.H., Nguyen, T.M., Pandey, R.P. et al. The genome insights of Streptomyces lannensis T1317-0309 reveals actinomycin D production. J Antibiot 73, 837–844 (2020). https://doi.org/10.1038/s41429-020-0343-0
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DOI: https://doi.org/10.1038/s41429-020-0343-0