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Description of Streptomyces siderophoricus sp. nov., a promising nocardamine-producing species isolated from the rhizosphere soil of Mangifera indica

The Journal of Antibiotics (2024)Cite this article

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Abstract

An actinomycete, designated strain CH9-7T, was isolated from the rhizosphere soil of Mangifera indica. The morphological and chemotaxonomic properties, such as the production of spiral spore chains and the presence of LL-diaminopimelic acid in the peptidoglycan, showed that it belongs to the genus Streptomyces. Based on the 16S rRNA gene analysis, it was confirmed that strain CH9-7T was a member of the genus Streptomyces and revealed 99.9% 16S rRNA gene sequence similarity to its closest relative strains, Streptomyces lydicus NBRC 13058 T and Streptomyces chattanoogensis NBRC 12754 T. Although the strain showed high 16S rRNA gene sequence similarity values, however, genome relatedness indexes exhibited that the average nucleotide identity based on the MUMmer (ANIm) algorithm, the average amino acid identity (AAI), and the digital DNA–DNA hybridization values between strain CH9-7T and its closest phylogenomic relatives were below the threshold values for delineation of a novel species, (ANIm ranging from 87.5 to 88.6, AAI ranging from 80.6 to 84.6, and dDDH ranging from 28.4 to 31.7), respectively. A taxonomic position of strain CH9-7T in the phylogenomic tree showed that the closest relative strain was S. lydicus NBRC 13058 T. The comparative phenotypic studies between strain CH9-7T and its closest relatives revealed that strain CH9-7T could be classified as a novel species of the genus Streptomyces. Thus, the name Streptomyces siderophoricus sp. nov. is proposed for the strain. The type strain is CH9-7T ( = TBRC 17833 T = NBRC 116426 T). The chemical investigation led to the isolation of four known compounds (compounds 1-4). Among these compounds, compound 1 was identified to be nocardamine, a promising bioactive substance.

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References

  1. Bérdy J. Bioactive microbial metabolites. J Antibiot. 2005;58:1–26.

    Article  Google Scholar 

  2. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol. 2020;70:5607–12.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kämpfer P. The Actinobacteria. In: Goodfellow M, et al. editors. Bergey’s Manual of Systematic Bacteriology. 2nd ed. New York: Springer; 2012. pp 1455–767.

  4. Wang W, Qiu Z, Tan H, Cao L. Siderophore production by actinobacteria. Biometals. 2014;27:623–31.

    Article  CAS  PubMed  Google Scholar 

  5. Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev. 2007;71:413–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kalinovskaya NI, Romanenko LA, Irisawa T, Ermakova SP, Kalinovsky AI. Marine isolate Citricoccus sp. KMM 3890 as a source of a cyclic siderophore nocardamine with antitumor activity. Microbiol Res. 2011;166:654–61.

    Article  CAS  PubMed  Google Scholar 

  7. Cao L, Qiu Z, You J, Tan H, Zhou S. Isolation and characterization of endophytic streptomycete antagonists of fusarium wilt pathogen from surface-sterilized banana roots. FEMS Microbiol Lett. 2005;247:147–52.

    Article  CAS  PubMed  Google Scholar 

  8. Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, et al. Novel plant microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol. 2002;68:2161–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Duangupama T, Pratuangdejkul J, Chongruchiroj S, Pittayakhajonwut P, Intaraudom C, Tadtong S, et al. New insights into the neuroprotective and beta-secretase1 inhibitor profles of tirandamycin B isolated from a newly found Streptomyces composti sp. nov. Sci Rep. 2023;13:4825.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Thawai C, Rungjindamai N, Klanbut K, Tanasupawat S. Nocardia xestospongiae sp. nov., isolated from a marine sponge in the Andaman Sea. Int J Syst Evol Microbiol. 2017;67:1451–56.

    Article  CAS  PubMed  Google Scholar 

  11. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol. 1966;16:313–40.

    Article  Google Scholar 

  12. Duangupama T, Pansomsuay R, Pittayakhajonwut P, Intaraudom C, Suriyachadkun C, He Y-W, Tanasupawat S, Thawai C. Micromonospora solifontis sp. nov., an actinobacterium isolated from hot spring soil. Int J Syst Evol Microbiol. 2023;73:005819.

    Article  CAS  Google Scholar 

  13. Kelly KL. Inter-Society Color Council – National Bureau of Standard Color Name Charts Illustrated with Centroid Colors. Washington DC: US Government Printing Office; 1964.

    Google Scholar 

  14. Arai T, Tamotsu F, Masa H, Akihiro M, Yuzuru M. Culture media for actinomycetes. Tokyo: The Society for Actinomycetes Japan. 1975; 1–20.

  15. Williams ST. Cross T Actinomycetes. In: Booth C, editor. Methods in Microbiology. Academic Press, London; 1971. pp. 295–334.

  16. Gordon RE, Barnett DA, Handerhan JE, Pang CHN. Nocardia coeliaca, Nocardia autotrophica, and the nocardia strain. Int J Syst Bacteriol. 1974;24:54–63.

    Article  Google Scholar 

  17. Supong K, Suriyachadkun C, Pittayakhajonwut P, Suwanborirux K, Thawai C. Micromonospora spongicola sp. nov., an actinomycete isolated from a marine sponge in the Gulf of Thailand. J Antibiot. 2013;66:505–09.

    Article  CAS  Google Scholar 

  18. Thawai C, Tanasupawat S, Kudo T. Actinaurispora gen. nov., a new member of the family Micromonosporaceae, with description of Actinaurispora siamensis sp. nov. Int J Syst Evol Microbiol. 2010;60:1660–66.

    Article  CAS  PubMed  Google Scholar 

  19. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol. 1983;29:319–22.

    Article  CAS  Google Scholar 

  20. Komagata K, Suzuki KI. Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol. 1987;19:161–207.

    Article  CAS  Google Scholar 

  21. Minnikin DE, Patel PV, Alshamaony L, Goodfellow M. Polar lipid composition in the classification of Nocardia and related bacteria. Int J Syst Evol Microbiol. 1977;27:104–17.

    CAS  Google Scholar 

  22. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note. 101. Newark: Microbial ID Inc; 1990.

    Google Scholar 

  23. Kämpfer P, Kroppenstedt RM. Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol. 1996;42:989–1005.

    Article  Google Scholar 

  24. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol. 1977;100:221–30.

    Article  CAS  PubMed  Google Scholar 

  25. Tamaoka J. Determination of DNA base composition. In: Goodfellow, M, O’Donnell, AG, editors. Chemical methods in prokaryotic systematics. New York: Chichester, John Wiley & Sons. 1994. p. 463–70.

  26. Kittiwongwattana C, Thanaboripat D, Laosinwattana C, Koohakan P, Parinthawong N, Thawai C. Micromonospora oryzae sp. nov., isolated from roots of upland rice. Int J Syst Evol Microbiol. 2015;65:3818–23.

    Article  CAS  PubMed  Google Scholar 

  27. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67:1613–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.

    CAS  PubMed  Google Scholar 

  29. Fitch WM. Toward defining the course of evolution: minimum change for a species tree topology. Sys Zoo. 1971;20:406–16.

    Article  Google Scholar 

  30. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17:368–76.

    Article  CAS  PubMed  Google Scholar 

  31. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91.

    Article  PubMed  Google Scholar 

  33. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T, Bun C, et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res. 2017;45:D535–42.

    Article  CAS  PubMed  Google Scholar 

  34. Richter M, Rosselló-Móra R, Glöckner FO, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinform. 2016;32:929–31.

    Article  CAS  Google Scholar 

  35. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Micro Mag. 2014;9:111–18.

    Google Scholar 

  36. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 2013;14:60–73.

    Article  Google Scholar 

  37. Alanjary M, Steinke K, Ziemert N. AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Res. 2019;47:276–82.

    Article  Google Scholar 

  38. Kämpfer P. Genus Streptomyces. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W et al. editors. Bergey’s manual of systematic bacteriology, 2nd ed. New York: Springer. 2012. p.1455–1767.

  39. Duangupama T, Pittayakhajonwut P, Intaraudom C, Tadtong S, Thawai C. Streptomyces epipremni sp. nov., an endophytic actinomycete isolated from the root of Epipremnum aureum. Int J Syst Evol Microbiol. 2022;72:005179.

    Article  CAS  Google Scholar 

  40. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today. 2006;33:152–5.

    Google Scholar 

  41. Hu S, Li K, Zhang Y, Wang Y, Fu L, Xiao Y, et al. New insights into the threshold values of multi-locus sequence analysis, average nucleotide identity and digital DNA–DNA hybridization in delineating Streptomyces species. Front Microbiol. 2022;13:910277.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Richter M, Rossello-Mora R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA. 2009;106:19126–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.

    Article  CAS  PubMed  Google Scholar 

  44. Maehr H, Benz W, Smallheer J, Williams TH. Mikrobielle Produkte, I NMR-Spektren von Nocardamin und Massenspektrum des Tri-O-methyl-nocardamins / Microbiological Products, I NMR Spectra of Nocardamine and Mass Spectra of Tri-O-methyl-nocardamine. Z Naturforsch B. 1977;32:937–42.

    Article  Google Scholar 

  45. Kim YP, Takamatsu S, Hayashi M, Komiyama K, Omura S. Pyridindolols K1 and K2, new alkaloids from Streptomyces sp. K93-0711. J Antibiot. 1997;50:189–93.

    Article  CAS  Google Scholar 

  46. Dillman RL, Cardellina JH. Aromatic secondary metabolites from the sponge Tedania ignis. J Nat Prod. 1991;54:1056–61.

    Article  CAS  Google Scholar 

  47. Keller-Schierlein W, Müller A, Hagmann L, Schneider U, Zähner H. Stoffwechselprodukte von Mikroorganismen. 232. Mitteilung. (E)-3-(1H-Pyrrol-3-yl)-2-propensäure und (E)-3-(1H-Pyrrol-3-yl)-2-propensäureamid aus Streptomyces parvulus, Stamm Tü 2480. Helv Chim Acta. 1985;68:559–62.

    Article  CAS  Google Scholar 

  48. Stoll A, Brack A, Renz J. Nocardamin, ein neues Antibioticum aus einer Nocardia-Art: (9. Mitteilung über antibakterielle Stoffe). Schweiz Z Pathol Bacteriol. 1951;14:225–33.

    CAS  Google Scholar 

  49. Lee H-S, Shin HJ, Jang KH, Kim TS, Oh K-B, Shin J. Cyclic peptides of the nocardamine class from a marine-derived bacterium of the genus Streptomyces. J Nat Prod. 2005;68:623–25.

    Article  CAS  PubMed  Google Scholar 

  50. Aoyagi T, Kumagai M, Hazato T, Hamada M, Takeuchi T. Pyridindolol, a new beta-galactosidase inhibitor produced by actinomycetes. J Antibiot. 1975;28:555–57.

    Article  CAS  Google Scholar 

  51. Hagmann L, Keller-Schierlein W, Wahl B, Zähner H. Metabolites of microorganisms pyridindolol glucosides from Streptomyces parvulus. J Antibiot. 1988;41:289–95.

    Article  CAS  Google Scholar 

  52. Bernart M, Gerwick WH. 3-(Hydroxyacetyl)indole, a plant growth regulator from the Oregon red alga Prionitis lanceolata. Phytochem. 1990;29:3697–98.

    Article  CAS  Google Scholar 

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Acknowledgements

The research on “Bio-product development from actinomycetes to enhance the biomolecules degradation for organic fertilizer production” by King Mongkut’s Institute of Technology Ladkrabang (KMITL) has received funding support from the NSRF (FRB660065/0258-RE-KRIS/FF66/04). We thank the Actinobacterial Research Unit (ARU), Faculty of Science, King Mongkut’s Institute of Technology Ladkrabang, for laboratory support. The authors gratefully acknowledge Prof. Aharon Oren (The Hebrew University of Jerusalem, Jerusalem, Israel) for his valuable help on nomenclature aspects.

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Authors and Affiliations

  1. Department of Biology, School of Science, King Mongkut’s Institute of Technology Ladkrabang, Bangkok, Thailand

    Thitikorn Duangupama & Chitti Thawai

  2. National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand

    Pattama Pittayakhajonwut & Chakapong Intaraudom

  3. Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand

    Chanwit Suriyachadkun

  4. Department of Pharmacognosy, Faculty of Pharmacy, Srinakharinwirot University, Nakhon nayok, Thailand

    Sarin Tadtong

  5. Department of Plant Pathology, Faculty of Agriculture, Kasetsart University, Bangkok, Thailand

    Nattakorn Kuncharoen

  6. State Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, Shanghai Jiao Tong University, Shanghai, PR China

    Ya-Wen He

  7. Department of Biochemistry and Microbiology, Faculty of Pharmaceutical Sciences, Chulalongkorn University, Bangkok, Thailand

    Somboon Tanasupawat

  8. Actinobacterial Research Unit, School of Science, King Mongkut’s Institute of Technology Ladkrabang, Bangkok, Thailand

    Chitti Thawai

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Duangupama, T., Pittayakhajonwut, P., Intaraudom, C. et al. Description of Streptomyces siderophoricus sp. nov., a promising nocardamine-producing species isolated from the rhizosphere soil of Mangifera indica. J Antibiot (2024). https://doi.org/10.1038/s41429-024-00763-x

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