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Evaluation of salinomycin isolated from Streptomyces albus JSY-2 against the ciliate, Ichthyophthirius multifiliis

Published online by Cambridge University Press:  14 November 2018

Jia-Yun Yao
Affiliation:
College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, China Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
Ming-Yue Gao
Affiliation:
College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, China
Yong-Yi Jia
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
Yan-Xia Wu
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
Wen-Lin Yin
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
Zheng Cao
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
Gui-Lian Yang
Affiliation:
College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, China
Hai-Bin Huang
Affiliation:
College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, China
Chun-Feng Wang*
Affiliation:
College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, China
Jin-Yu Shen
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
Zhi-Min Gu*
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, China
*
Authors for correspondence: Chun-Feng Wang and ĆZhi-Min Gu, E-mail: wangchunfeng@jlau.edu.cn; guzhimin2006@163.com
Authors for correspondence: Chun-Feng Wang and ĆZhi-Min Gu, E-mail: wangchunfeng@jlau.edu.cn; guzhimin2006@163.com

Abstract

The present study was undertaken to investigate the antiparasitic activity of extracellular products of Streptomyces albus. Bioactivity-guided isolation of chloroform extracts affording a compound showing potent activity. The structure of the compound was elucidated as salinomycin (SAL) by EI-MS, 1H NMR and 13C NMR. In vitro test showed that SAL has potent anti-parasitic efficacy against theronts of Ichthyophthirius multifiliis with 10 min, 1, 2, 3 and 4 h (effective concentration) EC50 (95% confidence intervals) of 2.12 (2.22–2.02), 1.93 (1.98–1.88), 1.42 (1.47–1.37), 1.35 (1.41–1.31) and 1.11 (1.21–1.01) mg L−1. In vitro antiparasitic assays revealed that SAL could be 100% effective against I. multifiliis encysted tomonts at a concentration of 8.0 mg L−1. In vivo test demonstrated that the number of I. multifiliis trophonts on Erythroculter ilishaeformis treated with SAL was markedly lower than that of control group at 10 days after exposed to theronts (P < 0.05). In the control group, 80% mortality was observed owing to heavy I. multifiliis infection at 10 days. On the other hand, only 30.0% mortality was recorded in the group treated with 8.0 mg L−1 SAL. The median lethal dose (LD50) of SAL for E. ilishaeformis was 32.9 mg L−1.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Alderman, DJ (1985) Malachite green: a review. Journal of Fish Diseases 8, 289298.Google Scholar
Anderson, AS and Wellington, EM (2001) The taxonomy of Streptomyces and related genera. International Journal of Systematic and Evolutionary Microbiology 51, 797814.Google Scholar
Becker, JO, Zavaleta, ME, Colbert, SF, Schroth, MN, Weinhold, AR, Hancock, JG and Vangundy, SD (1988) Effects of rhizobacteria on root knot nematodes and gall formation. Phytopathology 78, 14661469.Google Scholar
Bisharyan, Y, Chen, Q, Hossain, MM, Papoyan, A and Clark, TG (2003) Cadmium effect on Ichthyophthirius: evidence for metal-sequestration in fish tissues following administration of recombinant vaccines. Parasitology 126, 8793.Google Scholar
Chen, SY and Dickson, DW (1996) Fungal penetration of the cystwall of Heterodera glycines. Phytopathology 86, 319327.Google Scholar
Chen, SY and Liu, XZ (2005) Control of the soybean cyst nematode by the fungi Hirsutella rhossiliensis and Hirsutella minnesotensis in greenhouse studies. Biological Control 32, 208219.Google Scholar
Clark, TG and Dickerson, HW (1997) Antibody-mediated effects on parasite behavior: evidence of a novel mechanism of immunity against a parasitic protist. Parasitology Today 13, 477480.Google Scholar
Conway, DP, Johnson, JK, Guyonnet, V, Long, PL and Smothers, CD (1993) Efficacy of semduramicin and salinomycin against different stages of Eimeria tenella and E. acervulina in the chicken. Veterinary Parasitology 45, 215229.Google Scholar
Crump, DH, Sayre, RM and Young, LD (1983) Occurrence of nematophagous fungi in cysts. Plant Disease 67, 6364.Google Scholar
Dickerson, HW (2006) Ichthyophthirius multifiliis and C ryptocaryon irritans (Phylum). In Woo, PTK (ed.), Fish Diseases and Disorders. Protozoan and Metazoan Infections, vol. 1, 2nd Edn. Wallingford, UK: CAB International, pp. 116153.Google Scholar
Dickerson, HW and Dawe, DL (1995) Ichthyophthirius multifiliis and Cryptocaryon irritans (Phylum Ciliophora). In Woo, PTK (ed.), Fish Diseases and Disorders, vol 1. Protozoan and Metazoan Infections. Wallingford: CAB International.Google Scholar
Gao, XG, Zheng, YN, Ruan, XC, Ji, H, Lin, P, Guo, DW and Jiang, SX (2018) Salinomycin induces primary chicken cardiomyocytes death via mitochondria mediated apoptosis. Chemico-Biological Interactions 282, 4554.Google Scholar
Goven, B, Gilbert, J and Gratzek, J (1980) Apparent drug resistance to the organophosphate dimethyl (2, 2, 2-trichloro-1-hydroxyethyl) phosphonate by monogenetic trematodes. Journal of Wildlife Diseases 16, 343346.Google Scholar
Kim, JH, Chae, M, Kim, WK, Kim, YJ, Kang, HS, Kim, HS and Yoon, S (2011) Salinomycin sensitizes cancer cells to the effects of doxorubicin and etoposide treatment by increasing DNA damage and reducing p21 protein. British Journal of Pharmacology 162, 773784.Google Scholar
Klinger, R and Floyd, RF (2002) Introduction to freshwater fish parasites. Document CIR716. Institute of Food and Agricultural Science, University of Florida, Florida.Google Scholar
Lemasters, JJ, Qian, T, Bradham, CA, Brenner, DA, Cascio, WE, Trost, LC, Nishimura, Y, Nieminen, AL and Herman, B (1999) Mitochondrial dysfunction in the pathogenesis of necrotic and apoptotic cell death. Journal of Bioenergetics and Biomembranes 31, 305319.Google Scholar
Li, AH and Buchmann, K (2001) Temperature and salinity dependent development of a Nordic strain of Ichthyophthirius multifiliis from rainbow trout. Journal of Applied Ichthyology 17, 273276.Google Scholar
Li, MH, Wise, DJ and Robinson, EH (1996) Chemical prevention and treatment of winter saprolegniosis (‘winter kill’) in channel catfish Ictaluruspunctatus. Journal of the World Aquaculture Society 27, 16.Google Scholar
Ling, F, Wang, JG, Wang, GX and Gong, XN (2011) Effect of potassium ferrate (VI) on survival and reproduction of Ichthyophthirius multifiliis tomonts. Parasitology Research 109, 14231428.Google Scholar
Ling, F, Wang, JG, Lu, C, Wang, GX, Lui, YH and Gong, XN (2012) Effects of aqueous extract of Capsicum frutescens (Solanaceae) against the fish ectoparasite Ichthyophthirius multifiliis. Parasitology Research 111, 841848.Google Scholar
Matthews, RA (2005) Ichthyophthirius multifiliis Fouquet and ichthyophthiriosis in freshwater teleosts. Advances in Parasitology 59, 159241.Google Scholar
Mccallum, HI (1985) Population effects of parasite survival of host death: experimental studies of the interaction of Ichthyophthirius multifiliis and its fish host. Parasitology 90, 529547.Google Scholar
Mccallum, HI (1986) Acquired resistance of black mollies Poecilia latipinna to infection by Ichthyophthirius multifiliis. Parasitology 93, 251261.Google Scholar
Mitani, M, Yamanishi, T and Miyazaki, Y (1975) Salinomycin: a new monovalent cation ionophore. Biochemical and Biophysical Research Communications 66, 12311236.Google Scholar
Mitani, M, Yamanishi, T, Miyazaki, Y and Otake, N (1976) Salinomycin effects on mitochondrial on translocation and respiration. Antimicrobial Agents and Chemotherapy 9, 655660.Google Scholar
Miyazaki, Y, Shibuya, M, Sugawara, H, Kawaguchi, O and Hirsoe, C (1974) Salinomycin, a new polyether antibiotic. Journal of Antibiotics 27, 814821.Google Scholar
Osman, HAM, El-Bana, LF, Noor El Deen, AE and Abd El-Hady, OK (2009) Investigations on white spots disease (Ichthyophthriasis) in catfish (Clarias gariepinus) with special reference to the immune response. Global Veterinaria 3, 113119.Google Scholar
Pressman, BC (1976) Biological applications of ionophores. Annual Review of Biochemistry 45, 501530.Google Scholar
Rintamäki-Kinnunen, P, Rahkonen, M, Mannermaa-Keränen, AL, Suo-malainen, LR, Mykrä, H and Valtonen, ET (2005) Treatment of ichthyophthiriasis after malachite green. I. Concrete tanks at salmonid farms. Diseases of Aquatic Organisms 64, 6976.Google Scholar
Rowland, SJ, Mifsud, C, Nixon, M, Read, P and Landos, M (2009) Use of formalin and copper to control ichthyophthiriosis in the Australian freshwater fish silver perch (Bidyanus bidyanus mitchell). Aquaculture Research 40, 4454.Google Scholar
Shinn, P, Camacho, AP, Bron, SM, Conway, JE, Yoon, D, Guo, GH, Taylor, FC and Ni, GH (2012) The anti-protozoal activity of bronopol on the key life-stages of Ichthyophthirius multifiliis Fouquet, 1876 (Cilio-phora). Veterinary Parasitology 186, 229236.Google Scholar
Straus, DL and Griffin, BR (2002) Efficacy of potassium permanganate in treating ichthyophthiriasis in channel catfish. Journal of Aquatic Animal Health 14, 145148.Google Scholar
Sudová, E, David, LS, Wienke, A and Meinelt, T (2010) Evaluation of continuous 4-day exposure to peracetic acid as a treatment for Ichthyophthirius multifiliis. Parasitology Research 106, 539542.Google Scholar
Sun, MH, Gao, L, Shi, YX, Li, BJ and Liu, XZ (2006) Fungi and actinomycetes associated with Meloidogyne spp. eggs and in China and their biocontrol potential. Journal of Invertebrate Pathology 93, 2228.Google Scholar
Tieman, DM and Goodwin, AE (2001) Treatments for Ich infestations in channel catfish evaluated under static and flow-through water conditions. North American Journal of Aquaculture 63, 293299.Google Scholar
Wahli, T, Schmitt, M and Meier, W (1993) Evaluation of alternatives to malachite green oxalate as a therapeutant for ichthyophthiriosis in rainbow-trout, Oncorhynchus mykiss. Journal of Applied Ichthyology 9, 237249.Google Scholar
Watve, MG, Tickoo, R, Jog, MM and Bhole, BD (2001) How many antibiotics are produced by the genus Streptomyces. Archives of Microbiology 176, 386390.Google Scholar
Wohllebe, S, Richter, P and Häder, DP (2012) .Chlorophyllin for the control of Ichthyophthirius multifiliis (Fouquet). Parasitology Research 111, 729733.Google Scholar
Xu, DH, Shoemaker, CA and Klesius, PH (2008) Effect of tricaine methanesulfonate on survival and reproduction of the fish ectoparasite Ichthyophthirius multifiliis. Parasitology Research 103, 979982.Google Scholar
Yao, JY, Shen, JY, Li, XL, Xu, Y, Hao, GJ, Pan, XY, Wang, GX and Yin, WL (2010) Effect of sanguinarine from the leaves of Macleaya cordata against Ichthyophthirius multifiliis in grass carp (Ctenopharyngodon idella). Parasitology Research 107, 10351042.Google Scholar
Yao, JY, Zhou, ZM, Li, XL, Yin, WL, Ru, HS, Pan, XY, Hao, GJ, Xu, Y and Shen, JY (2011) Antiparasitic efficacy of dihydrosanguinarine and dihydrochelerythrine from Macleaya microcarpa against Ichthyophthirius multifiliis in richadsin (Squaliobarbus curriculus). Veterinary Parasitology 183, 813.Google Scholar
Yao, JY, Li, XC, Li, G, Xu, Y, Ai, WM and Shen, JY (2014) Anti-parasitic activities of specific bacterial extracellular products of Streptomyces griseus SDX-4 against Ichthyophthirius multifiliis. Parasitology Research 113, 31113117.Google Scholar
Yao, JY, Li, XC, Li, G, Xu, Y, Ai, WM and Shen, JY (2015) Evaluation of nystatin isolated from Streptomyces griseus SDX-4 against the ciliate, Ichthyophthirius multifiliis. Parasitology Research 114, 14251431.Google Scholar
Yi, YL, Lu, C, Hu, XG, Ling, F and Wang, GX (2012) Antiprotozoal activity of medicinal plants against Ichthyophthirius multifiliis in goldfish (Carassius auratus). Parasitology Research 111, 17711778.Google Scholar
Zhang, GN, Liang, Y, Zhou, LJ, Chen, SP, Chen, G, Zhang, TP, Kang, T and Zhao, YP (2011) Combination of salinomycin and gemcitabine eliminates pancreatic cancer cells. Cancer Letters 313, 137144.Google Scholar