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Abstract

In 1973, Eli Lilly and Company described the filamentous actinomycete producing the glycopeptide antibiotic A477 as an species on the basis of its morphological and physiological features and deposited it as NRRL 3884. In this paper, we report that the phylogenetic analysis based on the 16S rRNA gene sequence and the whole genome phylogenomic study indicate that NRRL 3884 forms a distinct monophyletic line within the genus , being most closely related to NBRC 14524 [99.6 % 16S rRNA gene similarity, 89.4 % average nucleotide identity (ANI), 46.0 % digital DNA–DNA hybridization (dDDH)] and NBRC 13996 (98.8 % 16S rRNA gene similarity, 89.0 % ANI, 47.0 % dDDH). NRRL 3884 forms an extensively branched, non-fragmented vegetative mycelium; either sterile aerial hyphae or regular subglobose sporangia are formed depending on cultivation conditions. The cell wall contains -2,6-diaminopimelic acid and 2,6-diamino-3-hydroxypimelic acid and the diagnostic sugars are glucose, mannose and ribose with a minor amount of rhamnose. The predominant menaquinone (MK) is MK-9(H), with minor amounts of MK-9(H), MK-9(H) and MK-9(H). Mycolic acids are absent. The diagnostic phospholipids are diphosphatidylglycerol and phosphatidylethanolamine. The major cellular fatty acids are anteiso-C, iso-C and iso-C, with moderate amounts of anteiso-C and iso-C. The genomic G+C content is 71.5 mol%. Significant differences in the genomic, morphological, chemotaxonomic and biochemical data between NRRL 3884 and the two most closely related type strains clearly demonstrate that NRRL 3884 represents a novel species of the genus , for which the name sp. nov. is proposed. The type strain is NRRL 3884 (=DSM 116196).

Funding
This study was supported by the:
  • Fondo Ateneo per la Ricerca (Award Fondo Ateneo per la Ricerca (FAR) 2020-2021)
    • Principle Award Recipient: FlaviaMarinelli
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2024-01-08
2025-04-19
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References

  1. Couch JN. Actinoplanes, a new genus of the Actinomycetales. J Elisha Mitchell Sci Soc 1950; 66:87–92
    [Google Scholar]
  2. Vobis G, Schäfer J, Kämpfer P. Actinoplanes. In Whitman WB. eds Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons Inc; 2015 pp 1–41 [View Article]
    [Google Scholar]
  3. Schwientek P, Szczepanowski R, Rückert C, Kalinowski J, Klein A et al. The complete genome sequence of the acarbose producer Actinoplanes sp. SE50/110. BMC Genomics 2012; 13:1–18 [View Article] [PubMed]
    [Google Scholar]
  4. Yamamura H, Ohnishi Y, Ishikawa J, Ichikawa N, Ikeda H et al. Complete genome sequence of the motile actinomycete Actinoplanes missouriensis 431T (= NBRC 102363T). Stand Genomic Sci 2012; 7:294–303 [View Article] [PubMed]
    [Google Scholar]
  5. 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; 9:1–119 [View Article] [PubMed]
    [Google Scholar]
  6. Tamura T, Hatano K. Phylogenetic analysis of the genus Actinoplanes and transfer of Actinoplanes minutisporangius Ruan et al. 1986 and “Actinoplanes aurantiacus” to Cryptosporangium minutisporangium comb. nov. and Cryptosporangium aurantiacum sp. nov. Int J Syst Evol Microbiol 2001; 51:2119–2125 [View Article] [PubMed]
    [Google Scholar]
  7. 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]
  8. Habib N, Khan IU, Chu X, Xiao M, Li S et al. Actinoplanes deserti sp. nov., isolated from a desert soil sample. Antonie van Leeuwenhoek 2018; 111:2303–2310 [View Article] [PubMed]
    [Google Scholar]
  9. Luo X, Sun X, Huang Z, He C, Zhao J et al. Actinoplanes flavus sp. nov., a novel cellulase-producing actinobacterium isolated from coconut palm rhizosphere soil. Int J Syst Evol Microbiol 2021; 71:004990 [View Article] [PubMed]
    [Google Scholar]
  10. Ding L-M, Ding P-Z, Liu W-L, Shen H-L, Xia Z-F et al. Three novel Actinoplanes species isolated by using polyaspartic acid as a water-retaining agent for the enrichment in situ. Int J Syst Evol Microbiol 2023; 73:005705 [View Article] [PubMed]
    [Google Scholar]
  11. Lechevalier MP, De Bievre C, Lechevalier H. Chemotaxonomy of aerobic Actinomycetes: phospholipid composition. Biochem Syst Ecol 1977; 5:249–260 [View Article]
    [Google Scholar]
  12. Gao R, Liu C, Zhao J, Jia F, Li C et al. Actinoplanes lutulentus sp. nov., isolated from mucky soil in China. Int J Syst Evol Microbiol 2014; 64:1782–1788 [View Article] [PubMed]
    [Google Scholar]
  13. Tiwari K, Gupta RK. Rare actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 2012; 32:108–132 [View Article] [PubMed]
    [Google Scholar]
  14. Xie Q-Y, Ma Q-Y, Yi K-X, Yang L, Dai H-F et al. Actinoplanes maris sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 2023; 73:005911 [View Article] [PubMed]
    [Google Scholar]
  15. Zhang Y, Zhang J, Fan L, Pang H, Xin Y et al. Actinoplanes atraurantiacus sp. nov., isolated from soil. Int J Syst Evol Microbiol 2012; 62:2533–2537 [View Article] [PubMed]
    [Google Scholar]
  16. Sazak A, Sahin N, Camas M. Actinoplanes abujensis sp. nov., isolated from Nigerian arid soil. Int J Syst Evol Microbiol 2012; 62:960–965 [View Article] [PubMed]
    [Google Scholar]
  17. Qu Z, Bao X-D, Xie Q-Y, Zhao Y-X, Yan B et al. Actinoplanes sediminis sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 2018; 68:71–75 [View Article] [PubMed]
    [Google Scholar]
  18. He H, Xing J, Liu C, Li C, Ma Z et al. Actinoplanes rhizophilus sp. nov., an actinomycete isolated from the rhizosphere of Sansevieria trifasciata Prain. Int J Syst Evol Microbiol 2015; 65:4763–4768 [View Article] [PubMed]
    [Google Scholar]
  19. Saeng-in P, Kanchanasin P, Yuki M, Kudo T, Ohkuma M et al. Actinoplanes lichenicola sp. nov. and Actinoplanes ovalisporus sp. nov., isolated from lichen in Thailand. Int J Syst Evol Microbiol 2021; 71:004921 [View Article]
    [Google Scholar]
  20. Gren T, Ortseifen V, Wibberg D, Schneiker-Bekel S, Bednarz H et al. Genetic engineering in Actinoplanes sp. SE50/110 - development of an intergeneric conjugation system for the introduction of actinophage-based integrative vectors. J Biotechnol 2016; 232:79–88 [View Article] [PubMed]
    [Google Scholar]
  21. Yushchuk O, Ostash B, Truman AW, Marinelli F, Fedorenko V. Teicoplanin biosynthesis: unraveling the interplay of structural, regulatory, and resistance genes. Appl Microbiol Biotechnol 2020; 104:3279–3291 [View Article] [PubMed]
    [Google Scholar]
  22. Kirillov S, Vitali LA, Goldstein BP, Monti F, Semenkov Y et al. Purpuromycin: an antibiotic inhibiting tRNA aminoacylation. RNA 1997; 3:905–913 [PubMed]
    [Google Scholar]
  23. Tamura T, Ishida Y, Suzuki K-I. Descriptions of Actinoplanes ianthinogenes nom. rev. and Actinoplanes octamycinicus corrig. comb. nov., nom. rev. Int J Syst Evol Microbiol 2011; 61:2916–2921 [View Article] [PubMed]
    [Google Scholar]
  24. McCafferty DG, Cudic P, Frankel BA, Barkallah S, Kruger RG et al. Chemistry and biology of the ramoplanin family of peptide antibiotics. Biopolym - Pept Sci Sect 2002; 66:261–284 [View Article] [PubMed]
    [Google Scholar]
  25. Vértesy L, Ehlers E, Kogler H, Kurz M, Meiwes J et al. Friulimicins: novel lipopeptide antibiotics with peptidoglycan synthesis inhibiting activity from Actinoplanes friuliensis sp. nov. II. Isolation and structural characterization. J Antibiot 2000; 53:816–827 [View Article] [PubMed]
    [Google Scholar]
  26. Hamill RL, Ross N, Haney ME, Lafayette W, Stark WM. Antibiotic A477 and Process for Preparation Thereof United States Patent Office; 1973
    [Google Scholar]
  27. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Evol Microbiol 1966; 16:313–340 [View Article]
    [Google Scholar]
  28. Parenti F, Coronelli C. Members of the genus Actinoplanes and their antibiotics. Annu Rev Microbiol 1979; 33:389–411 [View Article] [PubMed]
    [Google Scholar]
  29. Palleroni NJ. Chemotaxis in Actinoplanes. Arch Microbiol 1976; 110:13–18 [View Article] [PubMed]
    [Google Scholar]
  30. Gandolfi R, Jovetic S, Marinelli F, Molinari F. Biotransformations of lipoglycopeptides to obtain novel antibiotics. J Antibiot 2007; 60:265–271 [View Article] [PubMed]
    [Google Scholar]
  31. Yushchuk O, Vior NM, Andreo-Vidal A, Berini F, Rückert C et al. Genomic-led discovery of a novel glycopeptide antibiotic by Nonomuraea coxensis DSM 45129. ACS Chem Biol 2021; 16:915–928 [View Article] [PubMed]
    [Google Scholar]
  32. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
    [Google Scholar]
  33. Miller JR, Koren S, Sutton G. Assembly algorithms for next-generation sequencing data. Genomics 2010; 95:315–327 [View Article] [PubMed]
    [Google Scholar]
  34. GitHub - nanoporetech/medaka: Sequence correction provided by ONT Research. n.d https://github.com/nanoporetech/medaka accessed 5 June 2023
  35. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  36. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  37. Gordon D, Green P. Consed: a graphical editor for next-generation sequencing. Bioinformatics 2013; 29:2936–2937 [View Article] [PubMed]
    [Google Scholar]
  38. Li W, O’Neill KR, Haft DH, DiCuccio M, Chetvernin V et al. RefSeq: expanding the prokaryotic genome annotation pipeline reach with protein family model curation. Nucleic Acids Res 2021; 49:D1020–D1028 [View Article] [PubMed]
    [Google Scholar]
  39. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  40. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  41. Yoon S-H, Ha S-M, 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 [View Article] [PubMed]
    [Google Scholar]
  42. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  43. 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]
  44. 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]
  45. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 1971; 20:406 [View Article]
    [Google Scholar]
  46. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  47. 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]
  48. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  49. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  50. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces Genetics Norwich: John Innes Centre; 2000
    [Google Scholar]
  51. Waksman SA. Classification, Identification, and Description of Genera and Species. The Actinomycetes Baltimore, MD: The Williams & Wilkins Company; 1961 pp 328–334
    [Google Scholar]
  52. Maerz A, Paul MR. A Dictionary of Color, 2nd edn New York: McGraw-Hill; 1950
    [Google Scholar]
  53. Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 2021; 49:W29–W35 [View Article] [PubMed]
    [Google Scholar]
  54. 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]
  55. Schumann P. Peptidoglycan structure. Methods Microbiol 2011; 38:101–129
    [Google Scholar]
  56. Vieira S, Huber KJ, Neumann-Schaal M, Geppert A, Luckner M et al. Usitatibacter rugosus gen. nov., sp. nov. and Usitatibacter palustris sp. nov., novel members of Usitatibacteraceae fam. nov. within the order Nitrosomonadales isolated from soil. Int J Syst Evol Microbiol 2021; 71:004631
    [Google Scholar]
  57. Schumann P, Kalensee F, Cao J, Criscuolo A, Clermont D et al. Reclassification of Haloactinobacterium glacieicola as Occultella glacieicola gen. nov., comb. nov., of Haloactinobacterium album as Ruania alba comb. nov, with an emended description of the genus Ruania, recognition that the genus names Haloactinobacterium and Ruania are heterotypic synonyms and description of Occultella aeris sp. nov., a halotolerant isolate from surface soil sampled at an ancient copper smelter. Int J Syst Evol Microbiol 2021; 71:004769
    [Google Scholar]
  58. Vilchèze C, Jacobs WR. Isolation and analysis of Mycobacterium tuberculosis mycolic acids. Curr Protoc Microbiol 2007; 10:Unit 10A.3 [View Article] [PubMed]
    [Google Scholar]
  59. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37:911–917 [View Article] [PubMed]
    [Google Scholar]
  60. Tindall BJ, Sikorski J, Smibert RM, Krieg NR. Phenotypic characterization and the principles of comparative systematics. In Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM. eds Methods for General and Molecular Microbiology, 3rd. edn Washington, DC: American Society for Microbiology; 2007 pp 330–393 [View Article]
    [Google Scholar]
  61. Sasser M. Technical Note No. 101 Microbial Identification by Gas Chromatographic Analysis of Fatty Acid Methyl Esters (GC-FAME) MIDI; 2009
    [Google Scholar]
  62. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  63. Göker M. What can genome analysis offer for bacteria. In Bridge P, Smith D, Stackebrandt E. eds Trends in the Systematics of Bacteria and Fungi, CABI Digital Library, CABI Publishing 2021 pp 255–281 [View Article]
    [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. Yim G, Kalan L, Koteva K, Thaker MN, Waglechner N et al. Harnessing the synthetic capabilities of glycopeptide antibiotic tailoring enzymes: characterization of the UK-68,597 biosynthetic cluster. Chembiochem 2014; 15:2613–2623 [View Article] [PubMed]
    [Google Scholar]
  66. Li T-L, Huang F, Haydock SF, Mironenko T, Leadlay PF et al. Biosynthetic gene cluster of the glycopeptide antibiotic teicoplanin: characterization of two glycosyltransferases and the key acyltransferase. Chem Biol 2004; 11:107–119 [View Article] [PubMed]
    [Google Scholar]
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