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Characterisation of Two Polyketides from Streptomyces sp. SKH1-2 Isolated from Roots of Musa (ABB) cv. ‘Kluai Sao Kratuep Ho’

  • Nattakorn Kuncharoen
  • Wataru Fukasawa
  • Masato Iwatsuki
  • Mihoko Mori
  • Kazuro Shiomi
  • Somboon TanasupawatEmail author
Original Article

Abstract

An endophytic actinomycete strain SKH1-2 isolated from Musa (ABB) cv. ‘Kluai Sao Kratuep Ho’ collected in Suphan Buri province (14° 54′ 22.5″ N/100° 04′ 50″ E), Thailand, was identified as Streptomyces pseudovenezuelae based on phenotypic and chemotaxonomic characteristics, and 16S rRNA sequence analyses. A chemical investigation led to the isolation of two polyketide molecules from the n-butanol crude extract of the strain SKH1-2 culture broth. The compounds were purified using various chromatographic techniques and identified using spectroscopic methods compared with earlier published data. Compound 1, chartreusin, is known as an anti-Gram (+) bacterial compound and was active against Bacillus subtilis ATCC 6633, Kocuria rhizophila ATCC 9341 and Staphylococcus aureus ATCC 6538p with MIC values of 3.1, 1.6 and 12.5 μg/mL, respectively. Compound 2, lumichrome, did not show activity against all tested microbes. To our knowledge, this is the first report of chartreusin and lumichrome isolated from S. pseudovenezuelae. Taken together, it could be proved that Thai plant species are valuable reservoirs of interesting endophytic actinomycetes producing several interesting biologically active compounds.

Keywords

Antimicrobial activity Endophytic actinomycetes Streptomyces Polyketides 

Notes

Acknowledgements

We faithfully thank Dr. A. Matsumoto, Dr. K. Nonaka, Dr. Y. Asami and Mr. M. Watanabe, Department of Drug Discovery, Kitasato University, for helpful the antimicrobial activity assay.

Funding Information

We thank the 2015 Royal Golden Jubilee Ph. D. Programme as a scholarship to N. K. for financial support under the Thailand Research Fund.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Aoyama Y, Katayama T, Yamamoto M, Tanaka H, Kon K (1992) A new antitumor antibiotic product, demethylchartreusin. Isolation and biological activities. J Antibiot 45:875–878CrossRefGoogle Scholar
  2. Arai T (1975) Culture media for actinomycetes. The Society for Actinomycetes, JapanGoogle Scholar
  3. Berrocal MM, Rodríguez J, Ball AS, Pérez-Leblic MI, Arias ME (1997) Solubilisation and mineralisation of [14C] lignocellulose from wheat straw by Streptomyces cyaneus CECT 3335 during growth in solid-state fermentation. Appl Microbiol Biotechnol 48:379–384CrossRefGoogle Scholar
  4. Clinical and Laboratory Standards Institute (CLSI) (2012) Method for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard. M07-A9, Volume 32, No. 3, Replaces M07-A8, Volume 29, No .2Google Scholar
  5. Ding L, Maier A, Fiebig HH, Lin WH, Peschel G, Hertweck C (2012) Kandenols A-E, eudesmenes from an endophytic Streptomyces sp of the mangrove tree Kandelia candel. J Nat Prod 75:2223–2227CrossRefGoogle Scholar
  6. Ding L, Goerls H, Dornblut K, Lin WH, Maier A, Fiebig HH, Hertweck C (2015) Bacaryolanes A-C, rare bacterial caryolanes from a mangrove endophyte. J Nat Prod 78:2963–2967CrossRefGoogle Scholar
  7. El-Shatoury SA, El-Kraly OA, Trujillo ME, El-Kazzaz WM, El-Din ESG, Dewedar A (2013) Generic and functional diversity in endophytic actinomycetes from wild Compositae plant species at South Sinai - Egypt. Res Microbiol 164:761–769CrossRefGoogle Scholar
  8. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  9. Gordon RE, Barnett DA, Handerhan JE, Hor-Nay Pang C (1974) Nocardia coeliaca, Nocardia autotrophica, and nocardin strain. Int J Syst Bacteriol 24:54–63CrossRefGoogle Scholar
  10. Inahashi Y et al (2011) Spoxazomicins A-C, novel antitrypanosomal alkaloids produced by an endophytic actinomycete, Streptosporangium oxazolinicum K07-0460T. J Antibiot 64:303–307CrossRefGoogle Scholar
  11. Inahashi Y et al (2015) Actinoallolides A-E, new anti-trypanosomal macrolides, produced by an endophytic actinomycete, Actinoallomurus fulvus MK10-036. Org Lett 17:864–867CrossRefGoogle Scholar
  12. Kelly KL (1964) Inter-Society Colour Council - National Bureau of Standards Color Name Charts Illustrated with Centroid Colors. US Government Printing Office, Washington DCGoogle Scholar
  13. Kimura MA (1980) Simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  14. Kudo T, Matsushima K, Itoh T, Sasaki J, Suzuki K (1998) Description of four new species of the genus Kineosporia: Kineosporia succinea sp. nov., Kineosporia rhizophila sp. nov., Kineosporia mikuniensis sp. nov. and Kineosporia rhamnosa sp. nov., isolated from plant samples, and amended description of the genus Kineosporia. Int J Syst Bacteriol 48 Pt 4:1245–1255CrossRefGoogle Scholar
  15. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  16. Kuncharoen N, Pittayakhajonwut P, Tanasupawat S (2018) Micromonospora globbae sp nov., an endophytic actinomycete isolated from roots of Globba winitii C. H. Wright. Int J Syst Evol Microbiol 68:1073–1077CrossRefGoogle Scholar
  17. Küster E, Williams ST (1964) Selection of media for isolation of streptomycetes. Nature 202:928–929CrossRefGoogle Scholar
  18. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. Wiley, ChichesterGoogle Scholar
  19. Leach BE, Calhoun KM, Johnson LE, Teeters TM, Jackson WG (1953) Chartreusin, a new antibiotic produced by Streptomyces chartreusis, a new species. J Am Chem Soc 75:4011–4012CrossRefGoogle Scholar
  20. Lechevalier HA, Lechevalier MP, Gerber NN (1971) Chemical composition as a criterion in the classification of actinomycetes. Adv Appl Microbiol 14:47–72CrossRefGoogle Scholar
  21. Liu C, Cao Z, Zhang W, Tickner J, Qiu H, Wang C, Chen K, Wang Z, Tan R, Dong S, Xu J (2018) Lumichrome inhibits osteoclastogenesis and bone resorption through suppressing RANKL-induced NFAT activation and calcium signaling. J Cell Physiol 233:8971–8983CrossRefGoogle Scholar
  22. Makoto H, Hidetoshi E, Masami T, Takeshi H, Hiroshi N, Tsuyoshi T, Hamao U (1982) An inhibitor of sodium-potassium ATPase produced by Streptomyces pseudovenezuelae MF722-02; purification and properties. J Antibiot 35:1448–1453CrossRefGoogle Scholar
  23. Mearns-Spragg A, Bregu M, Boyd KG, Burgess JG (1998) Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates, after exposure to terrestrial bacteria. Lett Appl Microbiol 27:142–146CrossRefGoogle Scholar
  24. Omura S, Tanaka H, Iwai Y, Nishigaki K, Awaya J, Takahashi Y, Masuma R (1978) A new antibiotic, setomimycin, produced by a strain of Streptomyces. J Antibiot 31:1091–1098CrossRefGoogle Scholar
  25. Petinate SD, Branquinha MH, Coelho RR, Vermelho AB, Giovanni-De-Simone S (1999) Purification and partial characterization of an extracellular serine-proteinase of Streptomyces cyaneus isolated from Brazilian cerrado soil. J Appl Microbiol 87:557–563CrossRefGoogle Scholar
  26. Pholo M, Coetzee B, Maree HJ, Young PR, Lloyd JR, Kossmann J, Hills PN (2018) Cell division and turgor mediate enhanced plant growth in Arabidopsis plants treated with the bacterial signalling molecule lumichrome. Planta 248:477–488CrossRefGoogle Scholar
  27. Pridham TG (1970) New names and new combinations in the order Actinomycetales Buchanan 1917. US Dept Agric Tech Bull 1424:1–55Google Scholar
  28. Qin S, Li J, Chen HH, Zhao GZ, Zhu WY, Jiang CL, Xu LH, Li WJ (2009) Isolation, diversity, and antimicrobial activity of rare actinobacteria from medicinal plants of tropical rain forests in Xishuangbanna, China. Appl Environ Microbiol 75:6176–6186CrossRefGoogle Scholar
  29. Rivlin RS (1973) Riboflavin and cancer: a review. Cancer Res 33:1977–1986Google Scholar
  30. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  31. Shi YS, Zhang Y, Chen XZ, Zhang N, Liu YB (2015) Metabolites produced by the endophytic fungus Aspergillus fumigatus from the stem of Erythrophloeum fordii Oliv. Molecules 20:10793–10799CrossRefGoogle Scholar
  32. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340CrossRefGoogle Scholar
  33. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 33:152–155Google Scholar
  34. Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231Google Scholar
  35. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268CrossRefGoogle Scholar
  36. Supong K et al (2016) Antimicrobial compounds from endophytic Streptomyces sp BCC72023 isolated from rice (Oryza sativa L.). Res Microbiol 167:290–298CrossRefGoogle Scholar
  37. Suriyachadkun C, Chunhametha S, Thawai C, Tamura T, Potacharoen W, Kirtikara K, Sanglier JJ (2009) Planotetraspora thailandica sp. nov., isolated from soil in Thailand. Int J Syst Evol Microbiol 59:992–997CrossRefGoogle Scholar
  38. Tsukamoto S, Kato H, Hirota H, Fusetani N (1999) Lumichrome - a larval metamorphosis-inducing substance in the ascidian Halocynthia roretzi. Eur J Biochem 264:785–789CrossRefGoogle Scholar
  39. Yamamoto K, Asano Y (2015) Efficient production of lumichrome by Microbacterium sp. strain TPU 3598. Appl Environ Microbiol 81:7360–7367CrossRefGoogle Scholar
  40. Yoon SH, Ha SM, 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. Int J Syst Evol Microbiol 67:1613–1617CrossRefGoogle Scholar
  41. Yu Z et al (2011) Bafilomycins produced by an endophytic actinomycete Streptomyces sp. YIM56209. J Antibiot 64:159–162CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biochemistry and Microbiology, Faculty of Pharmaceutical SciencesChulalongkorn UniversityBangkokThailand
  2. 2.Graduate School of Infection Control SciencesKitasato UniversityTokyoJapan
  3. 3.Kitasato Institute for Life SciencesKitasato UniversityTokyoJapan

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