Advertisement

Parasitology Research

, Volume 114, Issue 4, pp 1425–1431 | Cite as

Evaluation of nystatin isolated from Streptomyces griseus SDX-4 against the ciliate, Ichthyophthirius multifiliis

  • Jia-Yun Yao
  • Yang Xu
  • Wen-Lin Yin
  • Xue-Mei Yuan
  • Ling-Yun Lin
  • Ting Xu
  • Meng-Li Zuo
  • Xiao-Yi Pan
  • Jin-Yu ShenEmail author
Original Paper

Abstract

The present study was conducted to evaluate the in vitro and in vivo antiparasitic efficacy of active compounds from the bacterial extracellular products of Streptomyces griseus SDX-4 against Ichthyophthirius multifiliis. Bioassay-guided fractionation and isolation of compounds with antiparasitic activity were performed on n-butanol extract of S. griseus yielding a pure bioactive compound, nystatin (Nys), identified by comparing spectral data (EI-MS, 1H NMR, and 13C NMR) with literature values. Results from in vitro antiparasitic assays revealed that Nys could be 100 % effective against I. multifiliis theronts and encysted tomonts at the concentration of 6.0 mg L−1, with the median effective concentration (EC50) values of 3.1 and 2.8 mg L−1 for theronts and encysted tomonts (4 h), respectively. Results of in vivo test demonstrated that the number of I. multifiliis trophonts on the gold fish treated with Nys was markedly lower than the control group at 10 days after exposed to theronts (p < 0.05). In the control group, 85.7 % mortality was observed owing to heavy I. multifiliis infection at 10 days after the exposure. On the other hand, only 23.8 % mortality owing to parasite infection was recorded in the groups treated with the Nys (4.0 and 6.0 mg L−1). In addition, our results showed that the survival and reproduction of I. multifiliis tomont exited from the fish were significantly reduced after treated with the 6.0 mg L−1 Nys. The median lethal dose (LD50) of Nys for goldfish was 16.8 mg L−1. This study firstly demonstrated that Nys has potent antiparasitic efficacy against I. multifiliis, and it can be a good candidate drug for chemotherapy and control of I. multifiliis infections.

Keywords

Ichthyophthirius multifiliis Nystatin Streptomyces griseus Antiparasitic 

Notes

Acknowledgments

The research was supported by the National Natural Science Foundation of China (31302211), the Commonness and Commonweal Technology Application project program of Zhejiang province (2014C32055), and the key project program of Huzhou City (2012GN12).

References

  1. Alderman DJ (1985) Malachite green: a review. J Fish Dis 8:289–298CrossRefGoogle Scholar
  2. Anderson AS, Wellington EM (2001) The taxonomy of Streptomyces and related genera. Int J Syst Evol Microbiol 51:797–814CrossRefPubMedGoogle Scholar
  3. Becker JO, Zavaleta ME, Colbert SF, Schroth MN, Weinhold AR, Hancock JG, Vangundy SD (1988) Effects of rhizobacteria on root knot nematodes and gall formation. Phytopathology 78:1466–1469CrossRefGoogle Scholar
  4. Buchmann K, Sigh J, Nielsen CV, Dalgaard M (2001) Host responses against the fish parasitizing ciliate Ichthyophthirius multifiliis. Vet Parasitol 100:105–116CrossRefPubMedGoogle Scholar
  5. Buchmann K, Jensen PB, Kruse KD (2003) Effects of sodium percarbonate and garlic extract on Ichthyophthirius multifiliis theronts and tomocysts: in vitro experiments. N Am J Aquacult 65:21–24CrossRefGoogle Scholar
  6. Campos FF, Calpena Campmany AC, Delgado GR, Serrano OL, Naveros BC (2012) Development and characterization of a novel nystatin-loaded nanoemulsion for the buccal treatment of candidosis: ultrastructural effects and release studies. J Pharm Sci 101:739–3752CrossRefGoogle Scholar
  7. Chen SY, Dickson DW (1996) Fungal penetration of the cyst wall of Heterodera glycines. Phytopathology 86:319–327CrossRefGoogle Scholar
  8. Chen SY, Liu XZ (2005) Control of the soybean cyst nematode by the fungi Hirsutella rhossiliensis and Hirsutella minnesotensis in greenhouse studies. Biol Control 32:208–219CrossRefGoogle Scholar
  9. Coutinho A, Prieto M (2003) Cooperative partition model of nystatin interaction with phospholipid vesicles. Biophys J 84:3061–3078CrossRefPubMedCentralPubMedGoogle Scholar
  10. Crump DH, Sayre RM, Young LD (1983) Occurrence of nematophagous fungi in cysts. Plant Dis 67:63–64CrossRefGoogle Scholar
  11. Dickerson HW (2006) Ichthyophthirius multifiliis and Cryptocaryon irritans (Phylum). In: Woo PTK (ed) Fish diseases and disorders. Protozoan and metazoan infections, vol 1, 2nd edn. CAB International, Wallingford, pp 116–153CrossRefGoogle Scholar
  12. Ellepola AN, Samaranayake LP (1999) The in vitro post-antifungal effect of nystatin on Candida species of oral origin. J Oral Pathol Med 28:112–116CrossRefPubMedGoogle Scholar
  13. Goven B, Gilbert J, Gratzek J (1980) Apparent drug resistance to the organophosphate dimethyl (2,2,2-trichloro-1-hydroxyethyl) phosphonate by monogenetic trematodes. J Wildl Dis 16(3):343–346CrossRefPubMedGoogle Scholar
  14. Hazen EL, Brown R (1950) Two antifungal agents produced by a soil actinomycete. Science 112:423PubMedGoogle Scholar
  15. Klinger R, Floyd RF (2002) Introduction to freshwater fish parasites. Document CIR716. Institute of Food and Agricultural Science, University of Florida, FloridaGoogle Scholar
  16. Li AH, Buchmann K (2001) Temperature and salinity dependent development of a Nordic strain of Ichthyophthirius multifiliis from rainbow trout. J Appl Ichthyol 17:273–276CrossRefGoogle Scholar
  17. Ling DK, Chen S, Wang SW, SUN ZP, Ma JW (1986) Identification of two major components in Chinese nystatin. Acta Pharm Sin 21(6):454–457Google Scholar
  18. Ling F, Wang JG, Liu QF, Li M, Ye LT, Gong XN (2010) Prevention of Ichthyophthirius multifiliis infestation in goldfish (Carassius auratus) by potassium ferrate (VI) treatment. Vet Parasitol 168:212–216Google Scholar
  19. Ling F, Wang JG, Lu C, Wang GX, Lui YH, Gong XN (2012) Effects of aqueous extract of Capsicum frutescens (Solanaceae) against the fish ectoparasite Ichthyophthirius multifiliis. Parasitol Res 111:841–848CrossRefPubMedGoogle Scholar
  20. Ling F, Wang JG, Wang GX, Gong XN (2011) Effect of potassium ferrate(VI) on survival and reproduction of Ichthyophthirius multifiliis tomonts. Parasitol Res 109:1423–1428CrossRefPubMedGoogle Scholar
  21. Matthews RA (2005) Ichthyophthirius multifiliis Fouquet and ichthyophthiriosis in freshwater teleosts. Adv Parasitol 59:159–241CrossRefPubMedGoogle Scholar
  22. Pathom-aree W, Stach JEM, Ward AC, Horikoshi K, Bull AT, Goodfellow M (2006) Diversity of actinomycetes isolated from challenger deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10:181–189CrossRefPubMedGoogle Scholar
  23. Recamier KS, Hernandez-Gomez A, Gonzalez-Damian J, Ortega-Blake I (2010) Effect of membrane structure on the action of polyenes: I. Nystatin action in cholesterol and ergosterol-containing membranes. J Membr Biol 237:31–40CrossRefPubMedGoogle Scholar
  24. Rintamäki-Kinnunen P, Rahkonen M, Mannermaa-Keränen AL, Suo-malainen LR, Mykrä H, Valtonen ET (2005) Treatment of ichthyophthiriasis after malachite green. I. Concrete tanks at salmonid farms. Dis Aquat Organ 64:69–76CrossRefPubMedGoogle Scholar
  25. Rowland SJ, Mifsud C, Nixon M, Read P, Landos M (2009) Use of formalin and copper to control ichthyophthiriosis in the Australian freshwater fish silver perch (Bidyanus bidyanus Mitchell). Aquacult Res 40:44–54CrossRefGoogle Scholar
  26. Shinn P, Camacho AP, Bron SM, Conway JE, Yoon D, Guo GH, Taylor FC, Ni GH (2012) The anti-protozoal activity of bronopol onthe key life-stages of Ichthyophthirius multifiliis Fouquet, 1876 (Cilio-phora). Vet Parasitol 186:229–236CrossRefPubMedGoogle Scholar
  27. Straus DL, Griffin BR (2002) Efficacy of potassium permanganate in treating ichthyophthiriasis in channel catfish. J Aquat Anim Health 14(2):145–148CrossRefGoogle Scholar
  28. Sun MH, Gao L, Shi YX, Li BJ, Liu XZ (2006) Fungi and actinomycetes associated with Meloidogyne spp. eggs and in China and their biocontrol potential. J Invertebr Pathol 93:22–28CrossRefPubMedGoogle Scholar
  29. Thomas AH (1982) The heterogeneous composition of pharmaceutical grade nystatin. Analyst 20:294Google Scholar
  30. Traxler GS, Richard J, McDonald TE (1998) Ichthyophthirius multifiliis (Ich) epizootics in spawning sockeye salmon in British Columbia, Canada. J Aquat Anim Health 10:143–151CrossRefGoogle Scholar
  31. Wahli T, Schmitt M, Meier W (1993) Evaluation of alternatives to malachite green oxalate as a therapeutant for ichthyophthiriosis in rainbow-trout, Oncorhynchus mykiss. J Appl Ichthyol 9:237–249CrossRefGoogle Scholar
  32. Watve MG, Tickoo R, Jog MM, Bhole BD (2001) How many antibiotics are produced by the genus Streptomyces. Arch Microbiol 176:386–390CrossRefPubMedGoogle Scholar
  33. Wohllebe S, Richter P, Häder DP (2012) Chlorophyllin for the control of Ichthyophthirius multifiliis (Fouquet). Parasitol Res 111:729–733CrossRefPubMedGoogle Scholar
  34. Xu DH, Shoemaker CA, Klesius PH (2008) Effect of tricaine methanesulfonate on survival and reproduction of the fish ectoparasite Ichthyophthirius multifiliis. Parasitol Res 103:979–982CrossRefPubMedGoogle Scholar
  35. Yao JY, Shen JY, Li XL, Xu Y, Hao GJ, Pan XY, Wang GX, Yin WL (2010) Effect of sanguinarine from the leaves of Macleaya cordata against Ichthyophthirius multifiliis in grass carp (Ctenopharyngodon idella). Parasitol Res 107:1035–1042CrossRefPubMedGoogle Scholar
  36. Yao JY, Zhou ZM, Li XL, Yin WL, Ru HS, Pan XY, Hao GJ, Xu Y, Shen JY (2011) Antiparasitic efficacy of dihydrosanguinarine and dihydrochelerythrine from Macleaya microcarpa against Ichthyophthirius multifiliis in richadsin (Squaliobarbus curriculus). Vet Parasitol 183:8–13CrossRefPubMedGoogle Scholar
  37. Yao JY, Li XC, Li G, Xu Y, Ai WM, Shen JY (2014) Anti-parasitic activities of specific bacterial extracellular products of Streptomyces griseus SDX-4 against Ichthyophthirius multifiliis. Parasitol Res 113(8):3111–3117CrossRefPubMedGoogle Scholar
  38. Yi YL, Lu C, Hu XG, Ling F, Wang GX (2012) Antiprotozoal activity of medicinal plants against Ichthyophthirius multifiliis in goldfish (Carassius auratus). Parasitol Res 111:1771–1778CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jia-Yun Yao
    • 1
  • Yang Xu
    • 1
  • Wen-Lin Yin
    • 1
  • Xue-Mei Yuan
    • 1
  • Ling-Yun Lin
    • 1
  • Ting Xu
    • 1
  • Meng-Li Zuo
    • 1
    • 2
  • Xiao-Yi Pan
    • 1
  • Jin-Yu Shen
    • 1
    Email author
  1. 1.Zhejiang Institute of Freshwater FisheriesHuzhouChina
  2. 2.Shanghai Ocean UniversityShanghaiChina

Personalised recommendations