1887

Abstract

A polyphasic study was designed to establish the taxonomic status of a Streptomyces strain isolated from soil from the QinLing Mountains, Shaanxi Province, China, and found to be the source of known and new specialized metabolites. Strain MBT76 was found to have chemotaxonomic, cultural and morphological properties consistent with its classification in the genus Streptomyces . The strain formed a distinct branch in the Streptomyces16S rRNA gene tree and was closely related to the type strains of Streptomyces hiroshimensis and Streptomyces mobaraerensis. Multi-locus sequence analyses based on five conserved house-keeping gene alleles showed that strain MBT76 is closely related to the type strain of S. hiroshimensis, as was the case in analysis of a family of conserved proteins. The organism was also distinguished from S. hiroshimensis using cultural and phenotypic features. Average nucleotide identity and digital DNA–DNA hybridization values between the genomes of strain MBT76 and S. hiroshimensis DSM 40037 were 88.96 and 28.4±2.3%, respectively, which is in line with their assignment to different species. On the basis of this wealth of data it is proposed that strain MBT76 (=DSM 106196=NCCB 100637), be classified as a new species, Streptomyces roseifaciens sp. nov.

Keyword(s): Streptomyces
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/content/journal/ijsem/10.1099/ijsem.0.003215
2019-01-21
2019-10-23
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References

  1. Zhu H, Swierstra J, Wu C, Girard G, Choi YH et al. Eliciting antibiotics active against the ESKAPE pathogens in a collection of actinomycetes isolated from mountain soils. Microbiology 2014;160:1714–1725 [CrossRef][PubMed]
    [Google Scholar]
  2. Wu C, Zhu H, van Wezel GP, Choi YH. Metabolomics-guided analysis of isocoumarin production by Streptomyces species MBT76 and biotransformation of flavonoids and phenylpropanoids. Metabolomics 2016;12:90 [CrossRef][PubMed]
    [Google Scholar]
  3. Gubbens J, Wu C, Zhu H, Filippov DV, Florea BI et al. Intertwined precursor supply during biosynthesis of the catecholate-hydroxamate siderophores qinichelins in Streptomyces sp. MBT76. ACS Chem Biol 2017;12:2756–2766 [CrossRef][PubMed]
    [Google Scholar]
  4. Wu C, Du C, Ichinose K, Choi YH, van Wezel GP. Discovery of C-Glycosylpyranonaphthoquinones in Streptomyces sp. MBT76 by a Combined NMR-Based Metabolomics and Bioinformatics Workflow. J Nat Prod 2017;80:269–277 [CrossRef][PubMed]
    [Google Scholar]
  5. Wu C, Ichinose K, Choi YH, van Wezel GP. Aromatic polyketide GTRI-02 is a previously unidentified product of the act gene cluster in Streptomyces coelicolor A3(2). Chembiochem 2017;18:1428–1434 [CrossRef][PubMed]
    [Google Scholar]
  6. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ et al. antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 2017;45:W36–W41 [CrossRef][PubMed]
    [Google Scholar]
  7. Kämpfer P. Family 1. Streptomycetaceae Waksman and Henrici 1943, 339AL emend. Rainey, Ward-Rainey and Stackebrandt, 1997, 486 emend. Kim, Lonsdale, Seong and Goodfellow 2003b, 113 emend. Zhi, Li and Stackebrandt 2009, 600. In Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I et al. (editors) Bergey's Manual of Systematic Bacteriology New York: Springer; 2012
    [Google Scholar]
  8. Labeda DP, Dunlap CA, Rong X, Huang Y, Doroghazi JR et al. Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis. Antonie van Leeuwenhoek 2017;110:563–583 [CrossRef][PubMed]
    [Google Scholar]
  9. Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B et al. Phylogenetic study of the species within the family Streptomycetaceae. Antonie van Leeuwenhoek 2012;101:73–104 [CrossRef][PubMed]
    [Google Scholar]
  10. Parker CT, Tindall BJ, Garrity GM. International code of nomenclature of prokaryotes. Int J System Evol Microbiol 2015
    [Google Scholar]
  11. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C et al. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 2016;80:1–43 [CrossRef][PubMed]
    [Google Scholar]
  12. Hopwood DA. Streptomyces in Nature and Medicine: The Antibiotic makers New York: Oxford University Press; 2007
    [Google Scholar]
  13. Waksman SA, Henrici AT. The nomenclature and classification of the actinomycetes. J Bacteriol 1943;46:337–341[PubMed]
    [Google Scholar]
  14. Kumar Y, Goodfellow M. Reclassification of Streptomyces hygroscopicus strains as Streptomyces aldersoniae sp. nov., Streptomyces angustmyceticus sp. nov., comb. nov., Streptomyces ascomycinicus sp. nov., Streptomyces decoyicus sp. nov., comb. nov., Streptomyces milbemycinicus sp. nov. and Streptomyces wellingtoniae sp. nov. Int J System Microbiol 2010;60:769–775 [CrossRef]
    [Google Scholar]
  15. Goodfellow M, Busarakam K, Idris H, Labeda DP, Nouioui I et al. Streptomyces asenjonii sp. nov., isolated from hyper-arid Atacama Desert soils and emended description of Streptomyces viridosporus Pridham et al. 1958. Antonie van Leeuwenhoek 2017;110:1133–1148 [CrossRef][PubMed]
    [Google Scholar]
  16. Rong X, Huang Y. Multi-locus sequence analysis: taking prokaryotic systematics to the next level. Methods Microbiol 2014;41:221–251
    [Google Scholar]
  17. Girard G, Traag BA, Sangal V, Mascini N, Hoskisson PA et al. A novel taxonomic marker that discriminates between morphologically complex actinomycetes. Open Biol 2013;3:130073 [CrossRef][PubMed]
    [Google Scholar]
  18. Traag BA, van Wezel GP. The SsgA-like proteins in actinomycetes: small proteins up to a big task. Antonie van Leeuwenhoek 2008;94:85–97 [CrossRef][PubMed]
    [Google Scholar]
  19. Hayakawa M, Nomomura H. A new method for the intensive isolation of actinomycetes from soil. Actinomycetologica 1989;3:95–104
    [Google Scholar]
  20. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA et al. Practical Streptomyces genetics Norwich, UK: John Innes Foundation; 2000
    [Google Scholar]
  21. Shirling E, Gottlieb D. Methods for characterization of Streptomyces species. Int J System Evol Microbiol 1966;16:313–340
    [Google Scholar]
  22. Piette A, Derouaux A, Gerkens P, Noens EE, Mazzucchelli G et al. From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J Proteome Res 2005;4:1699–1708 [CrossRef][PubMed]
    [Google Scholar]
  23. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 1983;29:319–322 [CrossRef]
    [Google Scholar]
  24. Collins MD, Goodfellow M, Minnikin DE, Alderson G. Menaquinone composition of mycolic acid-containing actinomycetes and some sporoactinomycetes. J Appl Bacteriol 1985;58:77–86[PubMed]
    [Google Scholar]
  25. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Inc Technical Notes.vol. 101 1990; pp.1
    [Google Scholar]
  26. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613–1617 [CrossRef][PubMed]
    [Google Scholar]
  27. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673–4680[PubMed]
    [Google Scholar]
  28. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981;17:368–376[PubMed]
    [Google Scholar]
  29. Fitch WM. Toward defining course of evolution - minimum change for a specific tree topology. Syst Zool 1971;20:406–&
    [Google Scholar]
  30. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406–425 [CrossRef][PubMed]
    [Google Scholar]
  31. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol, Research Support, N. I.H., Extramural 2011;28:2731–2739
    [Google Scholar]
  32. Guindon S, A Simple GO. fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. System Biol 2003;52:696–704
    [Google Scholar]
  33. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  34. Jukes TH, Cantor CR. Evolution of Protein Moleculesvol. 3 London: Academic Press; 1969; pp.21–132
    [Google Scholar]
  35. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985;39:783–791 [CrossRef][PubMed]
    [Google Scholar]
  36. Witt D, Stackebrandt E. Unification of the genera Streptoverticillum and Streptomyces, and amendation of Streptomyces-Waksman and Henrici-1943, 339al. Syst Appl Microbiol 1990;13:361–371
    [Google Scholar]
  37. Shinobu R. On Streptomyces hiroshimensis nov. sp. Seibutsugakkaishi 1955;6:43–46
    [Google Scholar]
  38. Nagatsu J, Suzuki S. Studies on an Antitumor Antibiotic, Cervicarcin. Iii. Taxonomic Studies on the Cervicarcin-Producing Organism, Streptomyces Ogaensis Nov. Sp. J Antibiot 1963;16:203–206
    [Google Scholar]
  39. Benedict RG, Dvonch W, Shotwell OL, Pridham TG, Lindenfelser LA, Cinnamycin LLA. Cinnamycin, an antibiotic from Streptomyces cinnamoneus nov. sp. Antibiot Chemother 1952;2:591–594[PubMed]
    [Google Scholar]
  40. Labeda DP. Multilocus sequence analysis of phytopathogenic species of the genus Streptomyces. Int J Syst Evol Microbiol 2011;61:2525–2531 [CrossRef][PubMed]
    [Google Scholar]
  41. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  42. Nei M, Kumar S. Molecular Evolution and Phylogenetics New York: Oxford University Press; 2000
    [Google Scholar]
  43. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980;16:111–120[PubMed]
    [Google Scholar]
  44. Rong X, Huang Y. Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst Appl Microbiol 2012;35:7–18 [CrossRef][PubMed]
    [Google Scholar]
  45. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al. Report of the Ad-Hoc-Committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 1987;37:463–464
    [Google Scholar]
  46. Baldacci E, Locci R, Genus LR II. Streptoverticillium Baldacci 1958, 15, emed. mur. char. Baldacci, Farina and Locci 1966, 168. In Buchanan RE, Gibbons NE. (editors) Bergey's Manual of Determinative Bacteriology, 8th ed.vol. 1974 Baltimore: Williams & Wilkins; 1958; pp.829–842
    [Google Scholar]
  47. Baldacci E, Farina G, Locci R. Emendation of genus Streptoverticillium Baldacci (1958) and revision of some species. Giorn Microbiol 1966;14:153
    [Google Scholar]
  48. Noens EE, Mersinias V, Traag BA, Smith CP, Koerten HK et al. SsgA-like proteins determine the fate of peptidoglycan during sporulation of Streptomyces coelicolor. Mol Microbiol 2005;58:929–944 [CrossRef][PubMed]
    [Google Scholar]
  49. Willemse J, Borst JW, de Waal E, Bisseling T, van Wezel GP. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev 2011;25:89–99 Research Support, Non-U.S. Gov't [CrossRef][PubMed]
    [Google Scholar]
  50. Williams ST, Goodfellow M, Alderson G, Wellington EM, Sneath PH et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983;129:1743–1813 [CrossRef][PubMed]
    [Google Scholar]
  51. Kelly K. Centroid notations for revised ISCC-NBS colour name blocks. J Res Nat Bur Stand USA 1964;472:
    [Google Scholar]
  52. Murray P, Barron E, Phaller M, Ternover J, Yolkken R. Manual of clinical microbiology. Mycopathologia 1999;146:107–108
    [Google Scholar]
  53. Aziz RK, Bartels D, Best AA, Dejongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008;9:75 [CrossRef][PubMed]
    [Google Scholar]
  54. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 2017;110:1281–1286 [CrossRef][PubMed]
    [Google Scholar]
  55. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013;14:60 [CrossRef][PubMed]
    [Google Scholar]
  56. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009;106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  57. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014;64:316–324 [CrossRef][PubMed]
    [Google Scholar]
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