1887

Abstract

The filamentous actinomycete that produces the antibiotic GE23077 was isolated by the Lepetit Research Group from a soil sample collected in Thailand, and it was classified as a member of the genus on the basis of its morphology and cell-wall composition. Phylogenetic analysis based on 16S rRNA gene sequences indicated that this strain formed a distinct monophyletic line within the genus and it was most closely related to DSM 45347 (99.31 % similarity) and DSM 44485 (98.94 %). The GE23077-producing strain formed an extensively branched, non-fragmented vegetative mycelium; no pseudosporangia were formed and the arthrospores were organized in slightly twisted chains. The cell wall contained -2,6-diaminopimelic acid and the diagnostic sugar was madurose. The predominant menaquinone was MK-9(H), with minor amounts of MK-9(H) and MK-9(H). The diagnostic phospholipids were phosphatidylinositol and diphosphatidylglycerol. The major cellular fatty acids were C and tuberculostearic acid (10-methyloctadecanoic acid), followed by minor amounts of Cω9, Cω7 and 10-methylheptadecanoic acid. The genomic DNA G+C content was 71.77 mol%. Significant differences in the morphological, chemotaxonomic and biochemical data, and the low DNA–DNA relatedness between the GE23077-producing strain and closely related type strains clearly demonstrate that it represents a novel species of the genus , for which the name sp. nov. is proposed. The type strain is NRRL B-65521(=LMG 31258=DSM 109019).

Funding
This study was supported by the:
  • Università degli Studi dell'Insubria (Award FFABR)
    • Principle Award Recipient: Giorgia Letizia Marcone
  • Università degli Studi dell'Insubria (Award FAR 2018-2019)
    • Principle Award Recipient: Flavia Marinelli
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2020-07-23
2024-04-26
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References

  1. Goodfellow M, Order XV et al. Streptosporangiales ord. nov.. In Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K et al. (editors) Bergey’s Manual of Systematic Bacteriology, Vol. 5, The Actinobacteria New York, NY: Springer; 2012 p 1805
    [Google Scholar]
  2. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the Phylum Actinobacteria . Front Microbiol 2018; 9:2007–2126 [View Article][PubMed]
    [Google Scholar]
  3. Stackebrandt E, Rainey FA, Ward-Rainey NL. Proposal for a new hierarchic classification system, Actinobacteriaactinobacteria classis nov. Int J Syst Bacteriol 1997; 47:479–491 [View Article]
    [Google Scholar]
  4. Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 1970; 20:435–443 [View Article]
    [Google Scholar]
  5. Kroppenstedt RM, Goodfellow M. The family Thermomonosporaceae . In Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH. (editors) The Prokaryotes New York: Springer Verlag; 1991 pp 1085–1114
    [Google Scholar]
  6. Kroppenstedt RM, Goodfellow M. The family Thermomonosporaceae: Actinocorallia, Actinomadura, Spirillospora and Thermomonospora . In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. (editors) The Prokaryotes A Handbook on the Biology of Bacteria New York: Springer; 2006 pp 682–724
    [Google Scholar]
  7. Lechevalier MP, De Bievre C, Lechevalier H. Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 1977; 5:249–260 [View Article]
    [Google Scholar]
  8. Kroppenstedt RM, Stackebrandt E, Goodfellow M. Taxonomic revision of the actinomycete genera Actinomadura and Microtetraspora . Syst Appl Microbiol 1990; 13:148–160 [View Article]
    [Google Scholar]
  9. Hu J, Han C, Yu B, Zhao J, Guo X et al. Actinomadura harenae sp. nov., a novel actinomycete isolated from sea sand in Sanya. Int J Syst Evol Microbiol 2020; 70:766–772 [View Article]
    [Google Scholar]
  10. Wieme AD, Gosselé F, Snauwaert C, Cleenwerck I, Vandamme P. Actinomadura roseirufa sp. nov., producer of semduramicin, a polyether ionophore. Int J Syst Evol Microbiol 2019; 69:3068–3073 [View Article][PubMed]
    [Google Scholar]
  11. Shi L, Han L, Guo X, Zhao J, Wang J et al. Actinomadura logoneensis sp. nov., a novel actinomycete isolated from the soil. Int J Syst Evol Microbiol 2019; 69:2914–2920 [View Article][PubMed]
    [Google Scholar]
  12. Cao C, Xu T, Liu J, Cai X, Sun Y et al. Actinomadura deserti sp. nov., isolated from desert soil. Int J Syst Evol Microbiol 2018; 68:2930–2935 [View Article][PubMed]
    [Google Scholar]
  13. Malisorn K, Kanchanasin P, Phongsopitanun W, Tanasupawat S. Actinomadura rhizosphaerae sp. nov., isolated from rhizosphere soil of the plant Azadirachta indica . Int J Syst Evol Microbiol 2018; 68:3012–3016 [View Article][PubMed]
    [Google Scholar]
  14. Himaman W, Thamchaipenet A, Pathom-Aree W, Duangmal K. Actinomycetes from Eucalyptus and their biological activities for controlling Eucalyptus leaf and shoot blight. Microbiol Res 2016; 188-189:42–52 [View Article][PubMed]
    [Google Scholar]
  15. Lee SD, Kim SB. Actinomadura darangshiensis sp. nov., isolated from a volcanic cone. Int J Syst Evol Microbiol 2015; 65:1431–1436 [View Article][PubMed]
    [Google Scholar]
  16. Liu L, Salam N, Jiao J-Y, Jiang H-C, Zhou E-M et al. Diversity of culturable thermophilic Actinobacteria in hot springs in Tengchong, China and studies of their biosynthetic gene profiles. Microb Ecol 2016; 72:150–162 [View Article][PubMed]
    [Google Scholar]
  17. Promnuan Y, Kudo T, Ohkuma M, Chantawannakul P. Actinomadura apis sp. nov., isolated from a honey bee (Apis mellifera) hive, and the reclassification of Actinomadura cremea subsp. rifamycini Gauze et al. 1987 as Actinomadura rifamycini (Gauze et al. 1987) sp. nov., comb. nov. Int J Syst Evol Microbiol 2011; 61:2271–2277 [View Article][PubMed]
    [Google Scholar]
  18. Lee DW, Lee SD. Actinomadura scrupuli sp. nov., isolated from rock. Int J Syst Evol Microbiol 2010; 60:2647–2651 [View Article][PubMed]
    [Google Scholar]
  19. Kumar V, Bharti A, Gupta VK, Gusain O, Bisht GS. Actinomycetes from solitary wasp mud nest and swallow bird mud nest: isolation and screening for their antibacterial activity. World J Microbiol Biotechnol 2012; 28:871–880 [View Article][PubMed]
    [Google Scholar]
  20. Puhl AA, Selinger LB, McAllister TA, Inglis GD. Actinomadura keratinilytica sp. nov., a keratin-degrading actinobacterium isolated from bovine manure compost. Int J Syst Evol Microbiol 2009; 59:828–834 [View Article][PubMed]
    [Google Scholar]
  21. Lu Z, Wang L, Zhang Y, Shi Y, Liu Z et al. Actinomadura catellatispora sp. nov. and Actinomadura glauciflava sp. nov., from a sewage ditch and soil in southern China. Int J Syst Evol Microbiol 2003; 53:137–142 [View Article][PubMed]
    [Google Scholar]
  22. Trujillo ME, Goodfellow M. Numerical phenetic classification of clinically significant aerobic sporoactinomycetes and related organisms. Antonie Van Leeuwenhoek 2003; 84:39–68 [View Article][PubMed]
    [Google Scholar]
  23. Bhattacharjee K, Kumar S, Palepu NR, Patra PK, Rao KM et al. Structure elucidation and in silico docking studies of a novel furopyrimidine antibiotics synthesized by endolithic bacterium Actinomadura sp. AL2. World J Microbiol Biotechnol 2017; 33:178 [View Article][PubMed]
    [Google Scholar]
  24. Kodani S, Komaki H, Ishimura S, Hemmi H, Ohnishi-Kameyama M. Isolation and structure determination of a new lantibiotic cinnamycin B from Actinomadura atramentaria based on genome mining. J Ind Microbiol Biotechnol 2016; 43:1159–1165 [View Article][PubMed]
    [Google Scholar]
  25. Shin B, Kim B-Y, Cho E, Oh K-B, Shin J et al. Actinomadurol, an antibacterial norditerpenoid from a rare actinomycete, Actinomadura sp. KC 191. J Nat Prod 2016; 79:1886–1890 [View Article][PubMed]
    [Google Scholar]
  26. Ciciliato I, Corti E, Sarubbi E, Stefanelli S, Gastaldo L et al. Antibiotics GE23077, novel inhibitors of bacterial RNA polymerase. I. taxonomy, isolation and characterization. J Antibiot 2004; 57:210–217 [View Article][PubMed]
    [Google Scholar]
  27. Wyche TP, Alvarenga RFR, Piotrowski JS, Duster MN, Warrack SR et al. Chemical genomics, structure elucidation, and in vivo studies of the marine-derived anticlostridial Ecteinamycin. ACS Chem Biol 2017; 12:2287–2295 [View Article][PubMed]
    [Google Scholar]
  28. Ciciliato I, Corti E, Sarubbi E, Stefanelli S, Montanini N et al. Antibiotics GE 23077, pharmaceutically acceptable salts and compositions, and use thereof US Patent US6586393; 2003
  29. Selva E. Growing the seeds sown by Piero Sensi. J Antibiot 2014; 67:613–617 [View Article][PubMed]
    [Google Scholar]
  30. Zhang Y, Degen D, Ho MX, Sineva E, Ebright KY et al. GE23077 binds to the RNA polymerase 'i' and 'i+1' sites and prevents the binding of initiating nucleotides. Elife 2014; 3:e02450 [View Article][PubMed]
    [Google Scholar]
  31. Mosaei H, Harbottle J. Mechanisms of antibiotics inhibiting bacterial RNA polymerase. Biochem Soc Trans 2019; 47:339–350 [View Article][PubMed]
    [Google Scholar]
  32. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  33. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces genetics. Norwich, United Kingdom; 2000
  34. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012; 62:716–721 [View Article][PubMed]
    [Google Scholar]
  35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  36. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article][PubMed]
    [Google Scholar]
  37. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
    [Google Scholar]
  38. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article][PubMed]
    [Google Scholar]
  39. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  40. 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 [View Article][PubMed]
    [Google Scholar]
  41. Ara I, Matsumoto A, Bakir MA, Kudo T, Omura S et al. Actinomadura bangladeshensis sp. nov. and Actinomadura chokoriensis sp. nov. Int J Syst Evol Microbiol 2008; 58:1653–1659 [View Article][PubMed]
    [Google Scholar]
  42. Quintana ET, Trujillo ME, Goodfellow M. Actinomadura mexicana sp. nov. and Actinomadura meyerii sp. nov., two novel soil sporoactinomycetes. Syst Appl Microbiol 2003; 26:511–517 [View Article][PubMed]
    [Google Scholar]
  43. Nonomura H. Design of a new medium for isolation of soil actinomycetes. The Actinomycetes 1984; 18:206–209
    [Google Scholar]
  44. Waksman SA. Classification, Identification, and Description of Genera and Species. The Actinomycetes Baltimore: Williams & Wilkins; 1961 pp 328–334
    [Google Scholar]
  45. Marcone GL, Binda E, Reguzzoni M, Gastaldo L, Dalmastri C et al. Classification of Actinoplanes sp. ATCC 33076, an actinomycete that produces the glycolipodepsipeptide antibiotic ramoplanin, as Actinoplanes ramoplaninifer sp. nov. Int J Syst Evol Microbiol 2017; 67:4181–4188 [View Article][PubMed]
    [Google Scholar]
  46. Dalmastri C, Gastaldo L, Marcone GL, Binda E, Congiu T et al. Classification of Nonomuraea sp. ATCC 39727, an actinomycete that produces the glycopeptide antibiotic A40926, as Nonomuraea gerenzanensis sp. nov. Int J Syst Evol Microbiol 2016; 66:912–921 [View Article][PubMed]
    [Google Scholar]
  47. Maerz A, Paul MR. A Dictionary of Color, 2nd ed. New York: McGraw-Hill Book Company Inc; 1950
    [Google Scholar]
  48. Tresner HD, Backus EJ. System of color wheels for streptomycete taxonomy. Appl Microbiol 1963; 11:335–338 [View Article][PubMed]
    [Google Scholar]
  49. Goodfellow M, Alderson G, Lacey J. Numerical taxonomy of Actinomadura and related actinomycetes. J Gen Microbiol 1979; 112:95–111 [View Article][PubMed]
    [Google Scholar]
  50. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article][PubMed]
    [Google Scholar]
  51. Saddler GS, Tavecchia P, Lociuro S, Zanol M, Colombo L et al. Analysis of madurose and other actinomycete whole cell sugars by gas chromatography. J Microbiol Meth 1991; 14:185–191 [View Article]
    [Google Scholar]
  52. Minnikin DE, O'Donnel AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure of isoprenoid quinones and polar lipids. J Microbiol Meth 1984; 2:233–241
    [Google Scholar]
  53. Kroppenstedt RM. Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 1982; 5:2359–2367 [View Article]
    [Google Scholar]
  54. Tindall BJ, Sikorski J, Smibert RM, Kreig NR et al. Phenotypic characterization and the principles of comparative systematics. In Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM et al. (editors) Methods for General and Molecular Microbiology Washington, DC USA: ASM Press; 2007 pp 330–393
    [Google Scholar]
  55. Kuykendall LD, Roy MA, O'Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum . Int J Syst Bacteriol 1988; 38:358–361 [View Article]
    [Google Scholar]
  56. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [View Article][PubMed]
    [Google Scholar]
  57. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet j. 2011; 17:10–12 [View Article]
    [Google Scholar]
  58. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  59. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article][PubMed]
    [Google Scholar]
  60. Cashion P, Holder-Franklin MA, McCully J, Franklin M. A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 1977; 81:461–466 [View Article][PubMed]
    [Google Scholar]
  61. De Ley J, Tijtgat R. Evaluation of membrane filter methods for DNA-DNA hybridization. Antonie van Leeuwenhoek 1970; 36:461–474 [View Article][PubMed]
    [Google Scholar]
  62. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR et al. Report of the AD hoc Committee on reconciliation of approaches to bacterial Systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
    [Google Scholar]
  63. Huss VA, Festl H, Schleifer KH. Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 1983; 4:184–192 [View Article][PubMed]
    [Google Scholar]
  64. 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; 110:1281–1286 [View Article][PubMed]
    [Google Scholar]
  65. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60–73 [View Article][PubMed]
    [Google Scholar]
  66. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article][PubMed]
    [Google Scholar]
  67. 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 [View Article][PubMed]
    [Google Scholar]
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