Skip to main content

Advertisement

SpringerLink
Log in

Fusartricin, a sesquiterpenoid ether produced by an endophytic fungus Fusarium tricinctum Salicorn 19

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

An endophytic fungus Salicorn 19 was isolated from Salicornia bigelovii Torr. and identified as Fusarium tricinctum using a combination of translation elongation factor 1 alpha (EF-1α) and β-tubulin (β-TUB) gene sequence analysis. A bioassay-guided fractionation led to a new sesquiterpenoid ether with unique skeleton fusartricin (1), and two known compounds fusarielin B (2) and enniatin B (3) from the culture of Salicorn 19. Their chemical structures were elucidated based on ESI–MS and NMR analysis, as well as a comparison with the literature data. Antimicrobial experiments revealed that compounds 1 exhibited significant antimicrobial activities against E. aerogenes, M. tetragenu and C. albicans with the MIC values 19, 19 and 19 µM, respectively, and compound 2 showed a broader spectrum antimicrobial activity against M. smegmati, B. subtilis, M. phlei and E.coli with MIC values 19, 19, 10 and 10 µM, respectively, and compound 3 displayed powerful antimicrobial activities toward B. subtilis, E. aerogenes and M. tetragenus with MIC values 13, 13 and 6 µM.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276

    Article  Google Scholar 

  2. Zhao J, Shan T, Mou Y, Zhou L (2011) Plant-derived bioactive compounds produced by endophytic fungi. Mini Rev Med Chem 11(2):159–168

    Article  CAS  Google Scholar 

  3. Kusari S, Spiteller M (2011) Are we ready for industrial production of bioactive plant secondary metabolites utilizing endophytes? Nat Prod Rep 28(7):1203–1207. doi:10.1039/C1NP00030F

    Article  CAS  Google Scholar 

  4. Arnold A, Maynard Z, Gilbert G, Coley P, Kursar T (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3(4):267–274

    Article  Google Scholar 

  5. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67(2):257–268

    Article  CAS  Google Scholar 

  6. Tayung K, Barik B, Jha D, Deka D (2011) Identification and characterization of antimicrobial metabolite from an endophytic fungus, Fusarium solani isolated from bark of Himalayan yew. Mycosphere 2(3):203–213

    Google Scholar 

  7. Zhao Y, Wang X, Wang H, Liu T, Xin Z (2014) Two new noroleanane-type triterpene saponins from the methanol extract of Salicornia herbacea. Food Chem 151:101–109

    Article  CAS  Google Scholar 

  8. Wang X, Zhang M, Zhao Y, Wang H, Liu T, Xin Z (2013) Pentadecyl ferulate, a potent antioxidant and antiproliferative agent from the halophyte Salicornia herbacea. Food Chem 141(3):2066–2074

    Article  CAS  Google Scholar 

  9. Guo LD, Huang GR, Wang Y, He WH, Zheng WH, Hyde KD (2003) Molecular identification of white morphotype strains of endophytic fungi from Pinus tabulaeformis. Mycol Res 107(6):680–688

    Article  CAS  Google Scholar 

  10. O’Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci USA 97(14):7905–7910

    Article  Google Scholar 

  11. Knutsen A, Torp M, Holst-Jensen A (2004) Phylogenetic analyses of the Fusarium poae, Fusarium sporotrichioides and Fusarium langsethiae species complex based on partial sequences of the translation elongation factor-1 alpha gene. Int J Food Microbiol 95(3):287–295

    Article  CAS  Google Scholar 

  12. O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7(1):103–116

    Article  Google Scholar 

  13. Yli-Mattila T, Paavanen-Huhtala S, Bulat SA, Alekhina IA, Nirenberg HI (2002) Molecular, morphological and phylogenetic analysis of the Fusarium avenaceum/F. arthrosporioides/F. tricinctum species complex—a polyphasic approach. Mycol Res 106(6):655–669

    Article  CAS  Google Scholar 

  14. Harrow SA, Farrokhi-Nejad R, Pitman AR, Scott IA, Bentley A, Hide C, Cromey MG (2010) Characterisation of New Zealand Fusarium populations using a polyphasic approach differentiates the F. avenaceum/F. acuminatum/F. tricinctum species complex in cereal and grassland systems. Fungal Biol 114(4):293–311

    Article  CAS  Google Scholar 

  15. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  Google Scholar 

  16. Gomez S, Cosson C, Deschamps A (1997) Evidence for a bacteriocin-like substance produced by a new strain of Streptococcus sp., inhibitory to Gram-positive food-borne pathogens. Res Microbiol 148(9):757–766

    Article  CAS  Google Scholar 

  17. Kobayashi H, Sunaga R, Furihata K, Morisaki N, Iwasaki S (1995) Isolation and structures of an antifungal antibiotic, fusarielin A, and related compounds produced by a Fusarium sp. J Antibiot (Tokyo) 48(1):42–52

    Article  CAS  Google Scholar 

  18. Blais L, ApSimon J, Blackwell B, Greenhalgh R, Miller J (1992) Isolation and characterization of enniatins from Fusarium avenaceum DAOM 196490. Can J Chem 70(5):1281–1287

    Article  CAS  Google Scholar 

  19. Sørensen JL, Akk E, Thrane U, Giese H, Sondergaard TE (2013) Production of fusarielins by Fusarium. Int J Food Microbiol 160(3):206–211

    Article  Google Scholar 

  20. Summerell BA, Leslie JF (2011) Fifty years of Fusarium: how could nine species have ever been enough? Fungal Divers 50(1):135–144

    Article  Google Scholar 

  21. Geiser DM, del Mar Jiménez-Gasco M, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) FUSARIUM-ID v. 1.0: a DNA sequence database for identifying Fusarium. In: Mulè G, Bailey JA, Cooke BM, Logrieco A (eds) Molecular diversity and PCR-detection of toxigenic Fusarium species and ochratoxigenic fungi. Springer, Netherlands, pp 473–479

  22. Gomez E, Riboldi M, Galan A, Medrano JV, Rubio MC, Martinez MC, Martinez-Jabaloyas JM, Pellicer A, Simon C, Riboldi M, Medrano JV, Marques-Mari AI, Gomez E, Poo ME, Aguilar C, Pellicer A, Gil Salom M, Simon C, Kim YY, Ku SY, Oh SK, Kim SH, Moon SY, Choi YM, Pellestor F, Monzo C, Nadal L, De Vos J, Hamamah S, Liang W, Cao Y, Zhao R, Lu C, Carlomagno G, van Bragt MPA, Korver CM, Repping S, de Rooij DG, van Pelt AMM, Sedlackova M, Zakova J, Hampl A, Dvorak P, Yachimovich-Cohen N, Even-Ram S, Shufaro Y, Rachmilewitz J, Reubinoff BE, Akhlaghi AA, Eslaminejad MRB, Falahi F, Nazarian H, Omani Samani R, Shahverdi A, Tavakolifar F, Pirouz M, Baharvand H, Davenport K, Dutton M, Zhao H, Li Y, Haifeng J, Xie L, Chuang L, Feng J, Yaning L, Guowu Y, Yi L, Jun W, Xiaohong W (2010) PostersStem Cells. Hum Reprod 25(suppl 1):i335–i339. doi:10.1093/humrep/de.25.s1.570

    Article  Google Scholar 

  23. Nalim F, Elmer W, McGovern R, Geiser D (2009) Multilocus phylogenetic diversity of Fusarium avenaceum pathogenic on lisianthus. Phytopathology 99(4):462–468

    Article  CAS  Google Scholar 

  24. Sutton J (1982) Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can J Plant Pathol 4(2):195–209

    Article  Google Scholar 

  25. Campos FF, Johann S, Cota BB, Alves TMA, Rosa LH, Caligiorne RB, Cisalpino PS, Rosa CA, Zani CL (2011) Antifungal activity of trichothecenes from Fusarium sp. against clinical isolates of Paracoccidioides brasiliensis. Mycoses 54(4):e122–e129

    Article  Google Scholar 

  26. Solfrizzo M, Visconti A, Savard M, Blackwell B, Nelson P (1994) Isolation and characterization of new chlamydosporol related metabolites of Fusarium chlamydosporum and Fusarium tricinctum. Mycopathologia 127(2):95–101

    Article  CAS  Google Scholar 

  27. Burmeister H, Grove M, Kwolek W (1980) Moniliformin and butenolide: effect on mice of high-level, long-term oral intake. Appl Environ Microbiol 40(6):1142

    CAS  Google Scholar 

  28. Logrieco A, Rizzo A, Ferracane R, Ritieni A (2002) Occurrence of beauvericin and enniatins in wheat affected by Fusarium avenaceum head blight. Appl Environ Microbiol 68(1):82–85

    Article  CAS  Google Scholar 

  29. Tejesvi M, Segura D, Schnorr K, Sandvang D, Mattila S, Olsen P, Neve S, Kruse T, Kristensen H, Pirttilä A (2013) An antimicrobial peptide from endophytic Fusarium tricinctum of Rhododendron tomentosum Harmaja. Fungal Divers 60(1):153–159

    Article  Google Scholar 

  30. Visconti A, Solfrizzo M (1994) Isolation, characterization and biological activity of visoltricin, a novel metabolite of Fusarium tricinctum. J Agric Food Chem 42(1):195–199

    Article  CAS  Google Scholar 

  31. Takagi M, Motohashi K, Nagai A, Izumikawa M, Tanaka M, Fuse S, Doi T, Iwase K, Kawaguchi K, Nagata K (2010) Anti-influenza virus compound from Streptomyces sp. RI18. Org Lett 12(20):4664–4666

    Article  CAS  Google Scholar 

  32. Zafrir Ilan E, Torres MR, Prudhomme J, Le Roch K, Jensen PR, Fenical W (2013) Farnesides A and B, sesquiterpenoid nucleoside ethers from a marine-derived Streptomyces sp., strain CNT-372 from Fiji. J Nat Prod 76(9):1815–1818

    Article  CAS  Google Scholar 

  33. Gai Y, Zhao LL, Hu CQ, Zhang HP (2007) Fusarielin E, a new antifungal antibiotic from Fusarium sp. Chin Chem Lett 18(8):954–956

    Article  CAS  Google Scholar 

  34. Nenkep V, Yun K, Zhang D, Choi HD, Kang JS, Son BW (2010) Induced production of bromomethylchlamydosporols A and B from the marine-derived fungus Fusarium tricinctum. J Nat Prod 73(12):2061–2063

    Article  CAS  Google Scholar 

  35. Nguyen HP, Zhang D, Lee U, Kang JS, Choi HD, Son BW (2007) Dehydroxychlorofusarielin B, an antibacterial polyoxygenated decalin derivative from the marine-derived fungus Aspergillus sp. J Nat Prod 70(7):1188–1190

    Article  CAS  Google Scholar 

  36. Kumagai H, Someno T, Dobashi K, Isshiki K, Ishizuka M, Ikeda D (2004) ICM0301s, new angiogenesis inhibitors from Aspergillus sp. F-1491. I. Taxonomy, fermentation, isolation and biological activities. J Antibiot (Tokyo) 57(2):97–103

    Article  CAS  Google Scholar 

  37. Someno T, Kumagai H, Ohba S, Amemiya M, Naganawa H, Ishizuka M, Ikeda D (2004) ICM0301s, new angiogenesis inhibitors from Aspergillus sp. F-1491. II. Physico-chemical properties and structure elucidation. J Antibiot (Tokyo) 57(2):104–109

    Article  CAS  Google Scholar 

  38. Ivanova L, Egge-Jacobsen W, Solhaug A, Thoen E, Fæste C (2012) Lysosomes as a possible target of enniatin B-induced toxicity in Caco-2 cells. Chem Res Toxicol 25(8):1662–1674

    Article  CAS  Google Scholar 

  39. Sy-Cordero AA, Pearce CJ, Oberlies NH (2012) Revisiting the enniatins: a review of their isolation, biosynthesis, structure determination and biological activities. J Antibiot (Tokyo) 65(11):541–549

    Article  CAS  Google Scholar 

  40. Cuomo V, Randazzo A, Meca G, Moretti A, Cascone A, Eriksson O, Novellino E, Ritieni A (2013) Production of enniatins A, A1, B, B1, B4, J1 by Fusarium tricinctum in solid corn culture: structural analysis and effects on mitochondrial respiration. Food Chem 140(4):784–793

    Article  CAS  Google Scholar 

  41. Tomoda H, Huang X, Cao J, Nishida H, Nagao R, Okuda S, Tanaka H, Omura S, Arai H, Inoue K (1992) Inhibition of acyl-CoA: cholesterol acyltransferase activity by cyclodepsipeptide antibiotics. J Antibiot 45(10):1626–1632

    Article  CAS  Google Scholar 

  42. Jestoi M (2008) Emerging fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin: a review. Crit Rev Food Sci Nutr 48(1):21–49

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Chinese National Natural Science Fund (No. 31071586), the Fundamental Research Funds for the Central Universities (KYZ201118), the project funded by special funds of agro-product quality safety risk assessment of Ministry of Agriculture of the People's Republic of China and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Conflict of interest

None.

Compliance with Ethics Requirements

This article does not contain any studies with human or animal subjects.

Author information

Authors and Affiliations

  1. Key Laboratory of Food Processing and Quality Control, College of Food Science and Technology, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Junnan Zhang, Hui Wang, Tianxing Liu & Zhihong Xin

  2. Shenzhen Key Laboratory of Fermentation, Purification and Analysis, Shenzhen Polytechnic, Shenzhen, 518055, Guangdong, People’s Republic of China

    Junnan Zhang & Dong Liu

Authors
  1. Junnan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tianxing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhihong Xin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhihong Xin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1174 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Liu, D., Wang, H. et al. Fusartricin, a sesquiterpenoid ether produced by an endophytic fungus Fusarium tricinctum Salicorn 19. Eur Food Res Technol 240, 805–814 (2015). https://doi.org/10.1007/s00217-014-2386-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-014-2386-6

Keywords

Search

Navigation