Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Isolation, purification and chemical characterization of a new angucyclinone compound produced by a new halotolerant Nocardiopsis sp. HR-4 strain

Abstract

A halotolerant Actinobacteria strain HR-4 was isolated from a salt lake soil sample in Algerian Sahara. Analysis of 16S rDNA gene sequence showed that strain HR-4 belonged to the genus Nocardiopsis. The similarity level ranges between 97.45 and 99.20% with Nocardiopsis species and Nocardiopsis rosea being the most closely related one. Morphological, physiological and phylogenetic characteristics comparisons showed significant differences with the nearest species. These data strongly suggest that strain HR-4 represents novel species. The antimicrobial activity of strain HR-4 showed an antibacterial activity against Gram-positive bacteria as well as an antifungal one. Two major natural products including a new one were isolated from the culture broth using various separation and purification procedures. The chemical structure established on the basis of spectroscopic studies NMR and by comparing with spectroscopic data from the literature of the two compounds affirm that they are classified in the group of Angucyclinones. This is the first report of a production of this type of molecules by the genus Nocardiopsis. The new natural compound was established as (−)-7-deoxy-8-O-methyltetrangomycin with a new configuration.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Addou NA, Schumann P, Sproer C, Hacène H, Cayol JL, Fardeau ML (2012) Melghirimyces algeriensis gen. Nov., sp. nov. A member of the family Thermoactinomycetaceae, isolated from a salt lake. Int J Syst Evol Microbiol 62:1491–1498

  2. Addou NA, Schumann P, Sproer C, Bouanane Darenfed A, Amarouche Yala S, Hacène H, Cayol JL, Fardeau ML (2013) Melghirimyces thermohalophilus sp. nov., a thermoactinomycete isolated from an Algerian salt lake. Int J Syst Evol Microbiol 63:1717–1722

  3. Al-Tai AM, Ruan JS (1994) Nocardiopsis halophila sp. nov., a new halophilic actinomycete isolated from soil. Int J Syst Bacteriol 44:474–478

  4. Augustine N, Wilson PA, Kerkar S, Thomas S (2012) Arctic actinomycetes as potential inhibitors of Vibrio cholerae biofilm. Curr Microbiol 64:338–342

  5. Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49:10–24

  6. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clément C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43

  7. Becerril-Espinosa A, Freel KC, Jensen PR, Soria-Mercado IE (2013) Marine actinobacteria from the Gulf of California: diversity, abundance and secondary metabolite biosynthetic potential. Antonie Van Leeuwenhoek 103:809–819

  8. Bennur T, Kumar AR, Zinjarde S, Javdekar V (2014) Nocardiopsis species as potential sources of diverse and novel extracellular enzymes. Appl Microbiol Biotechnol 98:9173–9185

  9. Bennur T, Kumar AR, Zinjarde S, Javdekar V (2015) Nocardiopsis species: incidence, ecological roles and adaptations. Microbiol Res 174:33–47

  10. Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26

  11. Cai Y (2009) Classification and salt-tolerance of actinomycetes in the Qinghai lake water and lake side saline soil. J Sustain Develop 2:107–110

  12. Chater KF (2006) Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Phil Trans Roy Soc London B Biol Sci 361:761–768

  13. Dashti Y, Grkovic T, Abdelmohsen UR, Hentschel U, Quinn RJ (2014) Production of induced secondary metabolites by a co-culture of sponge-associated actinomycetes, Actinokineospora sp. EG49 and Nocardiopsis sp. RV163. Mar Drugs 12:3046–3059

  14. Davies J (2006) Are antibiotics naturally antibiotics? J Ind Microbiol Biotechnol 33:496–499

  15. Ding ZG,  Zhao JY,  Li MG, Huang R, Li QM, Cui XL, Zhu HJ, Wen ML (2012) Griseusins F and G, Spiro-Naphthoquinones from a Tin Mine Tailings-Derived Alkalophilic Species. J Nat Prod 75(11):1994–1998

  16. Dolak LA, Castle TM, Laborde AL (1980) 3-Trehalosamine, a new disaccharide antibiotic. J Antibiot 7:690–694

  17. Engelhardt K, Degnes KF, Kemmler M, Bredholt H, Fjaervik E, Klinkenberg G et al (2010) Production of a new thiopeptide antibiotic TP-1161, by a marine Nocardiopsis species. Appl Environ Microbiol 76:4969–4976

  18. Felsenstein J (1981) Evolutionary trees from DNA 235 sequences: a maximum likelihood approach. J Mol Evol 17:368–376

  19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolut Int J org Evolut 39:783–791

  20. Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nat 111:223–257

  21. Fotso S, Taifo M, Zabriskie TM, Santosa DA, Sulastri Proteau PJ (2008) Rearranged and unrearranged angucyclonones from Indonesian Streptomyces spp. J Antibiot 61:449–456

  22. Fu P, Liu P, Qu H, Wang Y, Chen D, Wang H et al (2011) A-pyrones and diketopiperazine derivatives from the marine-derived actinomycete Nocardiopsis dassonvillei HR10-5. J Nat Prod 74:2219–2223

  23. Hacène H, Boudjellal F, Lefebvre G (1998) AH7, a non-polyenic antifungal antibiotic produced by a new strain of Streptosporangium roseum. Microbios 96:103–109

  24. Hacène H, Kebir K, Sid Othmane D, Lefebvre G (1994) HM17, a new polyene antifungal antibiotic produced by a new strain of Spirillospora. J Appl Bacteriol 77:484–489

  25. Hacène H, Daoudi-Hamdad F, Bhatnagar T, Baratti JC, Lefebvre G (2000) H107, a new aminoglycoside anti-Pseudomonas antibiotic produced by a new strain of Spirillospora. Microbios 102:69–77

  26. Hacène H, Rafa F, Chebhouni N, Boutaiba S, Bhatnager T, Baratti JC, Olivier B (2004) Biodiversity of prokaryotic microflora in el Golea salt lake: Algerian sahara. J Arid Environ 58:273–284

  27. Hamedi J, Mohammadipanah F, Ventosa A (2013) Systematic and biotechnological aspects of halophilic and halotolerant actinomycetes. Extremophiles 17:1–13

  28. Igarashi M, Watanabe T, Hashida T, Umekita M, Hatano M, Yanagida Y, Kino H, Kimura T, Kinoshita N, Inoue K, Sawa R, Nishimura Y, Utsumi R, Nomoto AJ (2013) Waldiomycin, a novel Walk histidine kinase inhibitor from Streptomyces sp. MK844-mf10. J Antibiot 66:45–464

  29. Ilic S, Konstantinovic S, Todorovic Z, Lazic M, Veljkovic V, Jokovic N, Radovanovic B (2007) Characterization and antimicrobial activity of the bioactive metabolites in streptomycete isolates. Mikrobiologiia 76:480–487 (in Russian)

  30. Jakeman DL, Bandi S, Graham CL, Reid TR, Wentzell JR, Douglas SE (2009) Antimicrobial activities of jodamycin B and structurally related analogues. Antimicrob Agents Chemother 53:1245–1247

  31. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, Academic Press, New York, pp 21–132

  32. Kalinovskaya NI, Kalinovsky AI, Romanenko LA, Pushilin MA, Dmitrenok PS, Kuznetsova TA (2008) New angucyclinones from the marine mollusk associated actinomycete Saccharothrix espanaensis An 113. Nat Prod Commun 3:1611–1616

  33. Kelly KL, Judd DB (1976) Color universal language and dictionary of names (National Bureau of Standards Special Publication 440). US Department of Commerce, Washington, DC

  34. Kesenheimer C, Groth U (2006) Total Synthesis of (–)-8-O-Methyltetrangomycin (MM 47755). Org Lett 8:6116–6126

  35. Kesenheimer C, Kalogerakis A, Mei β ner A, Groth U (2010) The cobalt way to angucyclonones : asymetric total synthesis of the antibiotics (+)-rubiginone B2, (−)-tetrangomycin, and (−)-8-O-methyltetrangomycin. Chem Eur J 16:8805–8821

  36. Kharel MK, Pahari P, Shepherd MD, Tibrewal N, Nybo SE, Shaaban KA, Rohr J (2012) Angucyclines: biosynthesis, mode of action, new natural products and synthesis. J Nat Prod Rep 29:264–325

  37. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH et al (2012) Introducing EzTaxon-e: a prokaryotic 16 S rRNA genesequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

  38. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

  39. Komaki H, Ichikawa N, Hosoyama A, Fujita N, Igarashi Y (2014) Draft genome sequence of marine derived Actinomycete Nocardiopsis sp. strain TP-A0876, a producer of polyketide pyrones. Genome Announc 2: e00665–14

  40. Lazzarini A, Cavaletti L, Toppo G, Marinelli F (2001) Rare genera of actinomycetes as potential producers of new antibiotics. Antonie Van Leeuwenhoek 78:399–405

  41. Li WJ, Kroppenstedt RM, Wang D, Tang SK, Lee JC, Park DJ et al (2006) Five novel species of the genus Nocardiopsis isolated from hypersaline soils and emended description of Nocardiopsis salina Li et al 2004. Int J Syst Evol Microbiol 56:1089–1096

  42. Li HW, Zhi XY, Yao JC, Zhou Y, Tang SK, Klenk HP et al (2013) Comparative genomic analysis of the genus Nocardiopsis provides new insights into its genetic mechanisms of environmental adaptability. PLoS ONE 8:e61528

  43. Linares JF, Gustafsson I, Baquero F, Martinez JL (2006) Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA 103:19484–19489

  44. Locci R (1989) Streptomycetes and related genera. In: Williams ST, Sharpe ME, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 4. Williams & Wilkins, Baltimore, pp 2451–2508

  45. Lu CH, Li YY, Wang HX, Wang BM, Shen YM (2013) A new phenoxazine derivative isolated from marine sediment actinomycetes Nocardiopsis sp. 236. Drug Discov Ther 7:101–104

  46. Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mantsala¨ P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6

  47. Meyer J (1976) Nocardiopsis, a new genus of the order Actinomycetales. Int J Syst Bacteriol 26:487–493

  48. Okazaki T, Kitahara T, Okami Y (1975) Studies on marine microorganisms. A new antibiotic SS-228 Y produced by Chainia isolated from shallow sea mud. J Antibiot 28:176–184

  49. Rohr J, Thiericke R (1992) Angucycline group antibiotics. Nat Prod Rep 9:103–137

  50. Romanenko LA, Tanaka N, Kalinovskaya NI, Mikhailov VV (2013) Antimicrobial potential of deep surface sediment associated bacteria from the Sea of Japan. World J Microbiol Biotechnol 29:1169–1177

  51. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

  52. Selvin J, Shanmughapriya S, Gandhimathi R, Seghal KG, Rajeetha RT, Natarajaseeni-vasan K et al (2009) Optimization and production of novel antimicrobial agents from sponge associated marine actinomycetes Nocardiopsis dassonvillei MAD08. Appl Microbiol Biotechnol 83:435–445

  53. Sheng Q, Jie L, Hua-Hong C, Guo-Zhen Z, Wen-Yong Z, Cheng-Lin J, Li-Hua X, Wen-Jun L (2009) Isolation, diversity, and antimicrobial activity of rare actinobacteria from medicinal plants of tropical rain forests in Xishuangbanna, China. Appl Environ Microbiol 75:6176–6186

  54. Shigihara Y, Koisumi Y, Tamamura T, Homma Y, Isshiki K, Dobashi K, Naganawa H, Takeuchi T (1988) 6-Deoxy-8-O-methylrabelomycin and 8-O-methylrabelomycin from a Streptomyces species. J Antibiot 41:1260–1264

  55. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

  56. Takahashi A, Hotta K, Saito N, Morioka M, Okami Y, Umezawa H (1986) Production of novel antibiotic, dopsisamine, by a new subspecies of Nocardiopsis mutabilis with multiple antibiotic resistance. J Antibiot 39:175–183

  57. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

  58. Tarkka MT, Lehr NA, Hampp R, Schrey SD (2008) Plant behavior upon contact with Strep tomycetes. Plant Signal Behav 3:917–919

  59. Theriault RJ, Rasmussen RR, Kohl WL, Prokop JF, Hutch TB, Barlow GJ (1986) Bezanthrins A and B a new class of quinone antibiotics: discovery, fermentation and antimicrobial activity. J Antibiot 39:1509–1514

  60. 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 22:4673–4680

  61. Tian SZ, Pu X, Luo G, Zhao LX, Xu LH, Li WJ et al (2013) Isolation and characterization of new p-Terphenyls with antifungal, antibacterial, and antioxidant activities from halophilic actinomycete Nocardiopsis gilva YIM 90087. J Agric Food Chem 61:3006–3012

  62. Tian S, Yang Y, Liu K, Xiong Z, Xu L, Zhao L (2014) Antimicrobial metabolites from a novel halophilic actinomycete Nocardiopsis terrae YIM 90022. Nat Prod Res 28:344–346

  63. Vimal V, Rajan BM, Kannabiran K (2009) Antimicrobial activity of marine actinomycete Nocardiopsis sp. VITSVK 5 (FJ973467). Asian J Med Sci 1:57–63

  64. Waksman SA, Schatz A, Reynolds DM (2010) Production of antibiotic substances by Actinomycetes. Ann N Y Acad Sci 1213:112–124

  65. Wang Z, Fu P, Liu P, Wang P, Hou J, Li W et al (2013) New pyran-2-ones from alkalophilic actinomycete Nocardiopsis alkaliphila sp. Nov. YIM-80379. Chem Biodivers 10:281–287

Download references

Author information

Correspondence to Hocine Hacène.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 5206 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hadj Rabia-Boukhalfa, Y., Eveno, Y., Karama, S. et al. Isolation, purification and chemical characterization of a new angucyclinone compound produced by a new halotolerant Nocardiopsis sp. HR-4 strain. World J Microbiol Biotechnol 33, 126 (2017). https://doi.org/10.1007/s11274-017-2292-8

Download citation

Keywords

  • Halotolerant
  • Nocardiopsis
  • Taxonomy
  • Antimicrobial activity
  • Angucyclinone