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Nonomuraea phyllanthi sp. nov., an endophytic actinomycete isolated from the leaf of Phyllanthus amarus

  • Nattaporn Klykleung
  • Masahiro Yuki
  • Takuji Kudo
  • Moriya Ohkuma
  • Wongsakorn Phongsopitanun
  • Pattama Pittayakhajonwut
  • Somboon TanasupawatEmail author
Original Paper
First Online:

Abstract

A novel actinomycete, strain PA1-10T, isolated from the leaf of Phyllanthus amarus collected from Bangkok, Thailand, was characterized taxonomically using a polyphasic approach. This strain contained the characteristics consistent with those of members of the genus Nonomuraea. It formed short rugose spore chain on aerial mycelium. The diamino acid in cell wall peptidoglycan was meso-diaminopimelic acid. Galactose, glucose, madurose, mannose, and ribose were found in whole-cell hydrolysates. Predominant menaquinones were MK-9 (H2), MK-9 (H4), and MK-9 (H6). Major cellular fatty acids were iso-C16:0 and C17:0 10-methyl. Phospholipid profiles were composed of phosphatidylinositol mannoside (PIM), lyso-phosphatidylethanolamine (lyso-PE), phosphatidylethanolamine (PE), methylphosphatidylethanolamine (PME), diphosphatidylglycerol (DPG), and phosphatidylglycerol (PG). The G + C content of DNA was 71.2 mol%. Strain PA1-10T showed the highest 16S rRNA gene sequence similarity with Nonomuraea candida JCM 15928T (98.35%) and shared the same node with Nonomuraea maritima JCM 18321T in the phylogenetic tree analysis. Based on the phenotypic characteristics, DNA–DNA relatedness, and average nucleotide identity (ANI), the strain is considered to represent a novel species of the genus Nonomuraea, for which the name Nonomuraea phyllanthi is proposed. The type strain is PA1-10T (= JCM 33073T = NBRC 112774T = TISTR 2497T).

Keywords

Nonomuraea phyllanthi Streptosporangiaceae Phyllanthus amarus Endophytic actinomycetes 
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Notes

Acknowledgements

We would like to thank the Associate Professor Thatree Phadungcharoen, the Faculty of Pharmaceutical Sciences, Chulalongkorn University for the plant sample and the Pharmaceutical Research Instrument Center, Faculty of Pharmaceutical Sciences, Chulalongkorn University, for providing research facilities.

Funding

This study was supported by the Thailand Research Fund for a 2017 Royal Golden Jubilee Ph.D. Program as a scholarship to N. K. and the Grant for International Research Integration, Research Pyramid, Ratchadaphiseksomphot Endowment Fund (GCURP_58_01_33_01), Chulalongkorn University.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

203_2019_1717_MOESM1_ESM.pdf (329 kb)
Supplementary material 1 (PDF 329 kb)

References

  1. Ara I, Kudo T, Matsumoto A, Takahashi Y, Omura S (2007) Nonomuraea maheshkhaliensis sp. nov., a novel actinomycete isolated from mangrove rhizosphere mud. J Gen Appl Microbiol 53:159–166CrossRefPubMedGoogle Scholar
  2. Arai T (1975) Culture media for actinomycetes. The Society for Actinomycetes, TokyoGoogle Scholar
  3. Aziz RK, Bartels D, Best AA, Dejongh M, Disz T et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  4. Aziz RK, Devoid S, Disz T, Edwards RA, Henry CS et al (2012) SEED servers: high-performance access to the SEED genomes, annotations, and metabolic models. PLoS One 7:e48053CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477CrossRefPubMedPubMedCentralGoogle Scholar
  6. Camas M, Sazak A, Spröer C, Klenk HP, Cetin D, Guven K, Sahin N (2013) Nonomuraea jabiensis sp. nov., isolated from arid soil. Int J Syst Evol Microbiol 63(1):212–218CrossRefPubMedGoogle Scholar
  7. Chiba S, Suzuki M, Ando K (1999) Taxonomic re-evaluation of ‘Nocardiopsis’ sp. K-252T (= NRRL 15532T): a proposal to transfer this strain to the genus Nonomuraea as Nonomuraea longicatena sp. nov. Int J Syst Bacteriol 49:1623–1630CrossRefPubMedGoogle Scholar
  8. Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230CrossRefPubMedGoogle Scholar
  9. Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229CrossRefGoogle Scholar
  10. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefPubMedGoogle Scholar
  11. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416CrossRefGoogle Scholar
  13. Huang H, Liu M, Zhong W, Mo K, Zhu J et al (2018) Nonomuraea mangrovi sp. nov., an actinomycete isolated from mangrove soil. Int J Syst Evol Microbiol 68:3144–3148CrossRefPubMedGoogle Scholar
  14. Kämpfer P (2012) Genus VI. Nonomuraea corrig. Zhang, Wang and Ruan 1998b, 149VP. In: Goodfellow M, Kampfer P, Busse H-J, Trujillo ME, Suzuki K et al (eds) Bergey’s manual of systematic bacteriology, part B, vol 5, 2nd edn. Springer, New York, pp 1844–1861Google Scholar
  15. Kämpfer P, Kroppenstedt RM, Grün-Wollny I (2005) Nonomuraea kuesteri sp. nov. Int J Syst Evol Microbiol 55(2):847–851CrossRefPubMedGoogle Scholar
  16. Kelly KL (1964) Inter-society color council: National Bureau of Standards Color Name Charts Illustrated with Centroid Colors. US Government Printing Office, WashingtonGoogle Scholar
  17. Klykleung N, Tanasupawat S, Pittayakhajonwut P, Ohkuma M, Kudo T (2015) Amycolatopsis stemonae sp. nov., isolated from a Thai medicinal plant. Int J Syst Evol Microbiol 65:3894–3899CrossRefPubMedGoogle Scholar
  18. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–148Google Scholar
  19. Le Roes M, Meyers PR (2008) Nonomuraea candida sp. nov., a new species from South African soil. Antonie van Leeuwenhoek 3(1–2):133–139CrossRefGoogle Scholar
  20. Meier-Kolthoff PJ, Alexander FA, Klenk HP, Göker M (2013) Genome sequence based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60CrossRefGoogle Scholar
  21. Mikami H, Ishida Y (1983) Post-column fluorometric detection of reducing sugar in high-performance liquid chromatography using arginine. Bunseki Kagaku 32:E207–E210CrossRefGoogle Scholar
  22. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241CrossRefGoogle Scholar
  23. Niemhom N, Chutrakul C, Suriyachadkun C, Thawai C (2017) Nonomuraea stahlianthi sp. nov., an endophytic actinomycete isolated from the stem of Stahlianthus campanulatus. Int J Syst Evol Microbiol 67:2879–2884CrossRefPubMedGoogle Scholar
  24. Nonomura H, Ohara Y (1971) Distribution of actinomycetes in soil. XI. Some new species of the genus Actinomadura. J Ferment Technol 49:904–912Google Scholar
  25. Quadri SR, Tian XP, Zhang J, Li J, Nie GX et al (2015) Nonomuraea indica sp. nov., novel actinomycetes isolated from lime-stone open pit mine, India. J Antibiot 68:491–495CrossRefPubMedGoogle Scholar
  26. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131CrossRefPubMedGoogle Scholar
  27. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) J SpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:929–931CrossRefPubMedGoogle Scholar
  28. Rosselló-Móra R, Trujillo ME, Sutcliffe IC (2017) Introducing a digital protologue: a timely move towards a database-driven systematics of archaea and bacteria. Antonie Van Leeuwenhoek 110:455–456CrossRefPubMedGoogle Scholar
  29. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  30. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note 101. MIDI Inc., Newark, p 1990Google Scholar
  31. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16(6):313–340CrossRefGoogle Scholar
  32. Sripreechasak P, Phongsopitanun W, Supong K, Pittayakhajonwut P, Kudo T, Ohkuma M, Tanasupawat S (2017) Nonomuraea rhodomycinica sp. nov., isolated from peat swamp forest soil. Int J Syst Evol Microbiol 67:1683–1687CrossRefPubMedGoogle Scholar
  33. Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231PubMedPubMedCentralGoogle Scholar
  34. Sungthong R, Nakaew N (2015) The genus Nonomuraea: a review of a rare actinomycete taxon for novel metabolites. J Basic Microbiol 55:554–565CrossRefPubMedGoogle Scholar
  35. Tamaoka J (1994) Determination of DNA base composition. In: Goodfellow M, O’Donnell AG (eds) Chemical methods in prokaryotic systematics. Wiley, Chichester, pp 463–470Google Scholar
  36. Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128CrossRefGoogle Scholar
  37. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  38. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wang F, Shi J, Huang Y, Wu Y, Deng X (2017) Nonomuraea ceibae sp. nov., an actinobacterium isolated from Ceiba speciosa rhizosphere. Int J Syst Evol Microbiol 67:1158–1162CrossRefPubMedGoogle Scholar
  40. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al (1987) International committee on Systematic Bacteriology. Report of the ad hoc committee on the reconciliation of approaches to bacterial systematic. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  41. Williams ST, Cross T (1971) Chapter XI actinomycetes. Methods Microbiol 4:295–334CrossRefGoogle Scholar
  42. Xi L, Zhang L, Ruan J, Huang Y (2011) Nonomuraea maritima sp. nov., isolated from coastal sediment. Int J Syst Evol Microbiol 61:2740–2744CrossRefPubMedGoogle Scholar
  43. Yoon SH, Ha SM, Kown S, Lim J, Kim Y et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequence and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zhang Z, Wang Y, Ruan J (1998) Reclassification of Thermomonospora and Microtetraspora. Int J Syst Bacteriol 48:411–422CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nattaporn Klykleung
    • 1
  • Masahiro Yuki
    • 2
  • Takuji Kudo
    • 2
  • Moriya Ohkuma
    • 2
  • Wongsakorn Phongsopitanun
    • 3
  • Pattama Pittayakhajonwut
    • 4
  • Somboon Tanasupawat
    • 1
    Email author
  1. 1.Department of Biochemistry and Microbiology, Faculty of Pharmaceutical SciencesChulalongkorn UniversityBangkokThailand
  2. 2.Japan Collection of MicroorganismsRIKEN BioResource CenterIbarakiJapan
  3. 3.Department of Biology, Faculty of ScienceRamkhamhaeng UniversityBangkokThailand
  4. 4.National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA)Thailand Science ParkPathum ThaniThailand

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