Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Development of a trivalent vaccine for prevention of co-infection by Miamiensis avidus and Tenacibaculum maritimum in farmed olive flounder

  • Hanchang Sohn (Department of Marine Life Sciences, Jeju National University) ;
  • Hyukjae Kwon (Busan Reginal Office, National Fishery Products Quality Management Service) ;
  • Seongdo Lee (General Affairs Division, National Fishery Products Quality Management Service) ;
  • Qiang Wan (Department of Marine Life Sciences, Jeju National University) ;
  • Jehee Lee (Department of Marine Life Sciences, Jeju National University)
  • Received : 2023.06.17
  • Accepted : 2023.09.04
  • Published : 2023.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Scuticociliatosis, caused by the parasitic pathogen Miamiensis avidus, poses a significant threat to olive flounder farms in South Korea. Infected fish suffer from severe systemic infections affecting various organs, with potential secondary bacterial diseases. This study investigated the emergence of different M. avidus serotypes in 20 olive flounder farms on Jeju island, South Korea, from 2015 to 2020. Additionally, we identified Tenacibaculum maritimum as a co-infecting bacteria. Based on serotyping and monitoring data, we developed a trivalent vaccine targeting two serotypes of M. avidus and one strain of T. maritimum. The efficacy of the vaccine was evaluated under laboratory conditions and demonstrated a relative percentage of survival (RPS) of 75%, 80%, and 93% for M. avidus serotype I, M. avidus serotype II and T. maritimum, respectively. Furthermore, successful field trials conducted on four different olive flounder farms resulted in significantly higher survival rates (52%-76% RPS) and weight gains in vaccinated fish. Overall, this study presents an effective vaccine against M. avidus and T. maritimum infections in farmed olive flounder, making a valuable contribution to sustainable aquaculture in South Korea.

Keywords

Acknowledgement

This work was supported by the 2023 education, research and student guidance grant funded by Jeju National University

References

  1. Avendano-Herrera R, Magarinos B, Toranzo AE, Beaz R, Romalde JL. Species-specific polymerase chain reaction primer sets for the diagnosis of Tenacibaculum maritimum infection. Dis Aquat Organ. 2004;62:75-83.  https://doi.org/10.3354/dao062075
  2. Calabro S, Tritto E, Pezzotti A, Taccone M, Muzzi A, Bertholet S, et al. The adjuvant effect of MF59 is due to the oilin-water emulsion formulation, none of the individual components induce a comparable adjuvant effect. Vaccine. 2013;31:3363-9.  https://doi.org/10.1016/j.vaccine.2013.05.007
  3. Dykova I, Tyml T, Kostka M, Peckova H. Strains of Uronema marinum (Scuticociliatia) co-isolated with amoebae of the genus Neoparamoeba. Dis Aquat Org. 2010;89:71-7.  https://doi.org/10.3354/dao02168
  4. Harikrishnan R, Balasundaram C, Heo MS. Poly d,l-lactide-co-glycolic acid (PLGA)-encapsulated vaccine on immune system in Epinephelus bruneus against Uronema marinum. Exp Parasitol. 2012;131:325-32.  https://doi.org/10.1016/j.exppara.2012.04.017
  5. Iglesias R, Parama A, Alvarez MF, Leiro J, Sanmartin ML. Antiprotozoals effective in vitro against the scuticociliate fish pathogen Philasterides dicentrarchi. Dis Aquat Org. 2002;49:191-7.  https://doi.org/10.3354/dao049191
  6. Iglesias R, Parama A, Alvarez M, Leiro J, Ubeira FM, Sanmartin ML. Philasterides dicentrarchi (Ciliophora:Scuticociliatida) expresses surface immobilization antigens that probably induce protective immune responses in turbot. Parasitology. 2003;126:125-34.  https://doi.org/10.1017/S0031182002002688
  7. Jee BY, Jo MR. Trials for the control of scuticociliatosis in the cultured olive flounder (Paralichthys olivaceus) by bath treatment. J Fish Pathol. 2002;15:93-7. 
  8. Jin CN, Kang HS, Moon YG, Lee CH, Lee YD, Lee J, et al. Scuticociliatosis in flounder farms of Jeju island. J Fish Pathol. 2007;20:93-8. 
  9. Jung MH, Jung SJ. Assessment of microorganism-derived adjuvants for scuticociliate Miamiensis avidus vaccine. Korean J Fish Aquat Sci. 2021;54:652-9. 
  10. Jung SJ, Im EY, Struder-Kypke MC, Kitamura SI, Woo PTK. Small subunit ribosomal RNA and mitochondrial cytochrome c oxidase subunit 1 gene sequences of 21 strains of the parasitic scuticociliate Miamiensis avidus (Ciliophora, Scuticociliatia). Parasitol Res. 2011;108:1153-61.  https://doi.org/10.1007/s00436-010-2157-7
  11. Jung SJ, Kitamura SI, Song JY, Oh MJ. Miamiensis avidus (Ciliophora: Scuticociliatida) causes systemic infection of olive flounder Paralichthys olivaceus and is a senior synonym of Philasterides dicentrarchi. Dis Aquat Org. 2007;73:227-34.  https://doi.org/10.3354/dao073227
  12. Kang YJ, Kim KH. Therapeutic potential of CpG-ODN 1668 against scuticociliatosis in olive flounder (Paralichthys olivaceus). Aquaculture. 2014;430:17-20.  https://doi.org/10.1016/j.aquaculture.2014.03.035
  13. Kim H, Baek KW, Kim A, Luan NT, Lim Y, Roh HJ, et al. Genome based quantification of Miamiensis avidus in multiple organs of infected olive flounder (Paralichthys olivaceus) by real-time PCR. Genes Genomics. 2019;41:567-72.  https://doi.org/10.1007/s13258-019-00792-z
  14. Kole S, Shin SM, Kwak IS, Cho SH, Jung SJ. Efficacy of chitosan-PLGA encapsulated trivalent oral vaccine against viral haemorrhagic septicemia virus, Streptococcus parauberis, and Miamiensis avidus in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2022;127:843-54.  https://doi.org/10.1016/j.fsi.2022.07.029
  15. Lamas J, Sanmartin ML, Parama AI, Castro R, Cabaleiro S, de Ocenda MVR, et al. Optimization of an inactivated vaccine against a scuticociliate parasite of turbot: effect of antigen, formalin and adjuvant concentration on antibody response and protection against the pathogen. Aquaculture. 2008;278:22-6.  https://doi.org/10.1016/j.aquaculture.2008.03.015
  16. Leon-Rodriguez L, Luzardo-Alvarez A, Blanco-Mendez J, Lamas J, Leiro J. A vaccine based on biodegradable microspheres induces protective immunity against scuticociliatosis without producing side effects in turbot. Fish Shellfish Immunol. 2012;33:21-7.  https://doi.org/10.1016/j.fsi.2012.03.028
  17. Mabrok M, Algammal AM, Sivaramasamy E, Hetta HF, Atwah B, Alghamdi S, et al. Tenacibaculosis caused by Tenacibaculum maritimum: updated knowledge of this marine bacterial fish pathogen. Front Cell Infect Microbiol. 2023;12:1068000. 
  18. Moustafa EMM, Naota M, Morita T, Tange N, Shimada A. Pathological study on the scuticociliatosis affecting farmed Japanese flounder (Paralichthys olivaceus) in Japan. J Vet Med Sci. 2010;72:1359-62.  https://doi.org/10.1292/jvms.10-0026
  19. Nguyen-Contant P, Sangster MY, Topham DJ. Squalene-based influenza vaccine adjuvants and their impact on the hemagglutinin-specific B cell response. Pathogens. 2021;10:355. 
  20. Palenzuela O, Sitja-Bobadilla A, Riaza A, Silva R, Aran J, Alvarez-Pellitero P. Antibody responses of turbot Psetta maxima against various antigen formulations of scuticociliates Ciliophora. Dis Aquat Org. 2009;86:123-34.  https://doi.org/10.3354/dao02102
  21. Piazzon MC, Leiro J, Lamas J. Reprint of "fish immunity to scuticociliate parasites". Dev Comp Immunol. 2014;43:280-9.  https://doi.org/10.1016/j.dci.2013.11.015
  22. Rahman MH, Ototake M, Iida Y, Yokomizo Y, Nakanishi T. Efficacy of oil-adjuvanted vaccine for coldwater disease in ayu Plecoglossus altivelis. Fish Pathol. 2000;35:199-203.  https://doi.org/10.3147/jsfp.35.199
  23. Rodrigues MS, Morelli KA, Jansen AM. Cytochrome c oxidase subunit 1 gene as a DNA barcode for discriminating Trypanosoma cruzi DTUs and closely related species. Parasit Vectors. 2017;10:488. 
  24. Sanmartin M, Parama A, Castro R, Cabaleiro S, Leiro J, Lamas J, et al. Vaccination of turbot, Psetta maxima (L.), against the protozoan parasite Philasterides dicentrarchi: effects on antibody production and protection. J Fish Dis. 2008;31:135-40.  https://doi.org/10.1111/j.1365-2761.2007.00876.x
  25. Song JY, Kitamura SI, Oh MJ, Kang HS, Lee J, Tanaka SJ, et al. Pathogenicity of Miamiensis avidus (syn. Philasterides dicentrarchi), Pseudocohnilembus persalinus, Pseudocohnilembus hargisi and Uronema marinum (Ciliophora, Scuticociliatida). Dis Aquat Org. 2009a;83:133-43.  https://doi.org/10.3354/dao02017
  26. Song JY, Sasaki K, Okada T, Sakashita M, Kawakami H, Matsuoka S, et al. Antigenic differences of the scuticociliate Miamiensis avidus from Japan. J Fish Dis. 2009b;32:1027-34.  https://doi.org/10.1111/j.1365-2761.2009.01089.x
  27. Vinay TN, Kim YJ, Jung MH, Kim WS, Kim DH, Jung SJ. Inactivated vaccine against viral hemorrhagic septicemia (VHS) emulsified with squalene and aluminum hydroxide adjuvant provides long term protection in olive flounder (Paralichthys olivaceus). Vaccine. 2013;31:4603-10.  https://doi.org/10.1016/j.vaccine.2013.07.036
  28. Whang I, Kang HS, Lee J. Identification of scuticociliates (Pseudocohnilembus persalinus, P. longisetus, Uronema marinum and Miamiensis avidus) based on the cox1 sequence. Parasitol Int. 2013;62:7-13.  https://doi.org/10.1016/j.parint.2012.08.002
  29. Wilson-Welder JH, Torres MP, Kipper MJ, Mallapragada SK, Wannemuehler MJ, Narasimhan B. Vaccine adjuvants: current challenges and future approaches. J Pharm Sci. 2009;98:1278-316.  https://doi.org/10.1002/jps.21523
  30. Wise AL, LaFrentz BR, Kelly AM, Khoo LH, Xu T, Liles MR, et al. A review of bacterial co-infections in farmed catfish: components, diagnostics, and treatment directions. Animals. 2021;11:3240.