Oral vaccination against yersinia ruckeri: oxidative stress biomarkers in the gills of rainbow trout (oncorhynchus mykiss walbaum)

DOI: 10.32900/2312-8402-2022-128-45-60

Halyna Tkachenko,
Doctor of Biological Sciences,
https://orcid.org/0000-0003-3951-9005,
Natalia Kurhaluk,
Doctor of Biological Sciences,
https://orcid.org/0000-0002-4669-1092,
Institute of Biology and Earth Sciences, Pomeranian University in Słupsk, Poland,
Joanna Grudniewska,
Ph.D.,
https://orcid.org/0000-0002-4272-8337,
Department of Salmonid Research, Stanislaw Sakowicz Inland Fisheries Institute, Żukowo, Poland,
Agnieszka Pękala-Safińska,
Doctor of Biological Sciences,
https://orcid.org/0000-0002-5515-8329,
Department of Preclinical Sciences and Infectious Diseases, Faculty of Veterinary Medicine and Animal Sciences, Poznań University of Life Sciences, Poznań, Poland

Keywords: rainbow trout Oncorhynchus mykiss, Yersinia ruckeri, immunization, oxidative stress, antioxidant defense, gills


Abstract

The aim of this study was to assess the effect of oral vaccination against Yersinia ruckeri based on oxidative stress biomarkers in the gills of rainbow trout (Oncorhynchus mykiss Walbaum). The vaccine consisted of three Y. ruckeri strains (O1 serotype) that originated from rainbow trout cultured on different farms, where fish exhibited clinical signs of enteric redmouth disease. The concentrated vaccine was incorporated into the fish food; treatment was delivered three times at one-day intervals. Two months after immunization, gills were sampled. The vaccination against Y. ruckeri resulted in non-significant changes in TBARS level as lipid peroxidation marker, aldehydic and ketonic derivatives of oxidatively modified proteins level in the gills of trout at the second month after immunization against Y. ruckeri. A significant decrease in superoxide dismutase activity (by 36%, p = 0.002) compared to untreated controls occurred. The alterations in markers of oxidative stress suggest that antioxidant defenses may contribute to the balance between oxidative modification of proteins and antioxidant defenses in the gills of trout vaccinated against Y. ruckeri. We did not find any alterations in the gills after 60 days of immunization. This is likely a result of long-term adaptation to immunization. Understanding the role of oxidative stress in the tissues of vaccinated trout has important implications for the understanding of the complex physiological changes that occur in immunization and also for improving aquaculture practices to maximize tissue growth and health of vaccinated trout. The oxidative stress biomarkers in the gills were sensitive to vaccination against Y. ruckeri and may potentially be used as biomarkers in evaluating vaccine toxicity in rainbow trout. From a practical point of view, the results may be useful in relation to studies of infections and the development, administration, and uptake of new vaccines applicable to large amounts of fish.

References

  1. Afonso, A., Lousada, S., Silva, J., Ellis, A. E., & Silva, M. T. (1998). Neutrophil and macrophage responses to inflammation in the peritoneal cavity of rainbow trout Oncorhynchus mykiss. A light and electron microscopic cytochemical study. Diseases of Aquatic Organisms, 34(1), 27–37. https://doi.org/10.3354/dao034027.
  2. Barnes, A. C. (2011). Enteric Redmouth Disease (ERM) (Yersinia ruckeri). In: Fish Diseases and Disorders, Volume 3: Viral, Bacterial and Fungal Infections, 2nd Ed., P.T.K. Woo, D.W. Bruno (Eds). MPG Books Group, UK.
  3. Bradford M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1006/abio.1976.9999.
  4. Chettri, J. K., Raida, M. K., Kania, P. W., & Buchmann, K. (2012). Differential immune response of rainbow trout (Oncorhynchus mykiss) at early developmental stages (larvae and fry) against the bacterial pathogen Yersinia ruckeriDevelopmental and Comparative Immunology, 36(2), 463–474. https://doi.org/10.1016/j.dci.2011.08.014.
  5. Chevion, M., Berenshtein, E., & Stadtman, E. R. (2000). Human studies related to protein oxidation: protein carbonyl content as a marker of damage. Free Radical Research, 33 Suppl., S99–S108.
  6. Dos Santos, N. M., Taverne-Thiele, J. J., Barnes, A. C., van Muiswinkel, W. B., Ellis, A. E., & Rombout, J. H. (2001). The gill is a major organ for antibody secreting cell production following direct immersion of sea bass (Dicentrarchus labrax, L.) in a Photobacterium damselae ssp. piscicida bacterin: an ontogenetic study. Fish & Shellfish Immunology, 11(1), 65–74. https://doi.org/10.1006/fsim.2000.0295.
  7. Dröge W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews, 82(1), 47–95. https://doi.org/10.1152/physrev.00018.2001.
  8. Dubinina, E. E., Burmistrov, S. O., Khodov, D. A., & Porotov, I. G. (1995). Okislitel’naia modifikatsiia belkov syvorotki krovi cheloveka, metod ee opredeleniia [Oxidative modification of human serum proteins. A method of determining it]. Voprosy Meditsinskoi Khimii, 41(1), 24–26. [in Russian].
  9. Evenhuis, J. P., & Cleveland, B. M. (2012). Modulation of rainbow trout (Oncorhynchus mykiss) intestinal immune gene expression following bacterial challenge. Veterinary Immunology and Immunopathology, 146(1), 8–17. https://doi.org/10.1016/j.vetimm.2012.01.008.
  10. Ewing, W. H., Ross, A. J., Brenner, D. J., & Fanning, G. R. (1978). Yersinia ruckeri sp. nov. redmouth (rm) bacterium. International Journal of Systematic Bacteriology, 28(1), 37–44.
  11. From, J., Rasmussen, G. (1984). A growth model, gastric evacuation, and body composition in rainbow trout, Salmo gaidneri Richardson 1836. Dana, 3, 61–139.
  12. Galaktionova, L. P., Molchanov, A. V., El’chaninova, S. A., & Varshavskiĭ, B. I.a (1998). Sostoianie perekisnogo okisleniia u bol’nykh s iazvennoĭ bolezn’iu zheludka i dvenadtsatiperstnoĭ kishki [Lipid peroxidation in patients with gastric and duodenal peptic ulcers]. Klinicheskaia laboratornaia diagnostika, (6), 10–14. [in Russian].
  13. Ghosh, B., Nguyen, T. D., Crosbie, P. B. B., Nowak, B. F., & Bridle, A. R. (2016). Oral vaccination of first-feeding Atlantic salmon, Salmo salar L., confers greater protection against yersiniosis than immersion vaccination. Vaccine, 34(5), 599–608. https://doi.org/10.1016/j.vaccine.2015.12.044.
  14. Glatzle, D., Vuilleumier, J. P., Weber, F., & Decker, K. (1974). Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in humans. Experientia, 30(6), 665–667. https://doi.org/10.1007/BF01921531.
  15. Grove, S., Johansen, R., Reitan, L. J., & Press, C. M. (2006). Immune- and enzyme histochemical characterisation of leukocyte populations within lymphoid and mucosal tissues of Atlantic halibut (Hippoglossus hippoglossus). Fish & Shellfish Immunology, 20(5), 693–708. https://doi.org/10.1016/j.fsi.2005.08.009.
  16. Harun, N. O., Wang, T., & Secombes, C. J. (2011). Gene expression profiling in naïve and vaccinated rainbow trout after Yersinia ruckeri infection: insights into the mechanisms of protection seen in vaccinated fish. Vaccine, 29(26), 4388–4399. https://doi.org/10.1016/j.vaccine.2011.04.003.
  17. Haugarvoll, E., Bjerkås, I., Nowak, B. F., Hordvik, I., & Koppang, E. O. (2008). Identification and characterization of a novel intraepithelial lymphoid tissue in the gills of Atlantic salmon. Journal of Anatomy, 213(2), 202–209. https://doi.org/10.1111/j.1469-7580.2008.00943.x.
  18. Horne, M. T., & Barnes, A. C. (1999). Enteric redmouth disease (Yersinia ruckeri).In: Woo P.T.K. and Bruno D.W. (eds.), Fish Diseases and Disorders, Vol. 3. CAB International, pp. 456-477.
  19. Kamyshnikov, V.S. (2004). A reference book on the clinic and biochemical researches and laboratory diagnostics, MEDpress-inform, Moscow [in Russian].
  20. Koppang, E. O., Fischer, U., Moore, L., Tranulis, M. A., Dijkstra, J. M., Köllner, B., Aune, L., Jirillo, E., & Hordvik, I. (2010). Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue. Journal of Anatomy, 217(6), 728–739. https://doi.org/10.1111/j.1469-7580.2010.01305.x.
  21. Koroliuk, M. A., Ivanova, L. I., Maĭorova, I. G., & Tokarev, V. E. (1988). Metod opredeleniia aktivnosti katalazy [A method of determining catalase activity]. Laboratornoe Delo, (1), 16–19. [in Russian].
  22. Kostiuk, V. A., Potapovich, A. I., & Kovaleva, Z.hV. (1990). Prostoĭ i chuvstvitel’nyĭ metod opredeleniia aktivnosti superoksid- dismutazy, osnovannyĭ na reaktsii okisleniia kvertsetina [A simple and sensitive method of determination of superoxide dismutase activity based on the reaction of quercetin oxidation]. Voprosy Meditsinskoi Khimii, 36(2), 88–91. [in Russian].
  23. Kumar, G., Menanteau-Ledouble, S., Saleh, M., & El-Matbouli, M. (2015). Yersinia ruckeri, the causative agent of enteric redmouth disease in fish. Veterinary Research, 46(1), 103. https://doi.org/10.1186/s13567-015-0238-4.
  24. Levine, R. L. (2002). Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radical Biology & Medicine, 32(9), 790–796. https://doi.org/10.1016/s0891-5849(02)00765-7.
  25. Levine, R. L., Garland, D., Oliver, C. N., Amici, A., Climent, I., Lenz, A. G., Ahn, B. W., Shaltiel, S., & Stadtman, E. R. (1990). Determination of carbonyl content in oxidatively modified proteins. Methods in Enzymology, 186, 464–478. https://doi.org/10.1016/0076-6879(90)86141-h.
  26. Marnett, L. J. (2000). Oxyradicals and DNA damage. Carcinogenesis, 21(3), 361–370. https://doi.org/10.1093/carcin/21.3.361.
  27. Moin, V. M. (1986). Prostoĭ i spetsificheskiĭ metod opredeleniia aktivnosti glutationperoksidazy v éritrotsitakh [A simple and specific method for determining glutathione peroxidase activity in erythrocytes]. Laboratornoe Delo, (12), 724–727. [in Russian].
  28. Olson, K. R. (2002). Vascular anatomy of the fish gill. The Journal of Experimental Zoology, 293(3), 214–231. https://doi.org/10.1002/jez.10131.
  29. Ormsby, M. J., Caws, T., Burchmore, R., Wallis, T., Verner-Jeffreys, D. W., & Davies, R. L. (2016). Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations. Applied and Environmental Microbiology, 82(19), 5785–5794. https://doi.org/10.1128/AEM.01173-16.
  30. Paiva, C. N., & Bozza, M. T. (2014). Are reactive oxygen species always detrimental to pathogens?. Antioxidants & Redox Signaling, 20(6), 1000–1037. https://doi.org/10.1089/ars.2013.5447.
  31. Pękala, A., & Antychowicz, J. (2010). Yersiniosis of salmonids – epizootiology of the disease, methods of its elimination. Medycyna Weterynaryjna, 66(6), 374–377 (Article in Polish, Abstract in English).
  32. Poljsak, B., Šuput, D., & Milisav, I. (2013). Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxidative Medicine and Cellular Longevity, 2013, 956792. https://doi.org/10.1155/2013/956792.
  33. Puertollano, M. A., Puertollano, E., de Cienfuegos, G. Á., & de Pablo, M. A. (2011). Dietary antioxidants: immunity and host defense. Current Topics in Medicinal Chemistry, 11(14), 1752–1766. https://doi.org/10.2174/156802611796235107.
  34. Rahal, A., Kumar, A., Singh, V., Yadav, B., Tiwari, R., Chakraborty, S., & Dhama, K. (2014). Oxidative stress, prooxidants, and antioxidants: the interplay. BioMed Research International, 2014, 761264. https://doi.org/10.1155/2014/761264.
  35. Raida, M. K., Nylén, J., Holten-Andersen, L., & Buchmann, K. (2011). Association between plasma antibody response and protection in rainbow trout Oncorhynchus mykiss immersion vaccinated against Yersinia ruckeri. PloS One, 6(6), e18832. https://doi.org/10.1371/journal.pone.0018832.
  36. Ross, A. J., Rucker, R. R., & Ewing, W. H. (1966). Description of a bacterium associated with redmouth disease of rainbow trout (Salmo gairdneri). Canadian Journal of Microbiology, 12(4), 763–770. https://doi.org/10.1139/m66-103.
  37. Salinas, I., Zhang, Y. A., & Sunyer, J. O. (2011). Mucosal immunoglobulins and B cells of teleost fish. Developmental and Comparative Immunology, 35(12), 1346–1365. https://doi.org/10.1016/j.dci.2011.11.009.
  38. Stadtman, E. R., & Levine, R. L. (2000). Protein oxidation. Annals of the New York Academy of Sciences, 899, 191–208. https://doi.org/10.1111/j.1749-6632.2000.tb06187.x.
  39. Thompson, K.D., & Adams, A. (2004). Current Trends in Immunotherapy and Vaccine Development for Bacterial Diseases of Fish. In: Current trends in the study of bacterial and viral fish and shrimp diseases / Ed. Ka Yin Leung. (Molecular aspects of fish and marine biology; V. 3), World Scientific Publishing Co. Pte. Ltd., Singapore, pp. 313-362.
  40. Tkachenko H., Grudniewska J., Pękala A., Terech-Majewska E. (2016a). Oxidative stress and antioxidant defense markers in muscle tissue of rainbow trout (Oncorhynchus mykiss) after vaccination against Yersinia ruckeriJournal of Veterinary Research, 60, 25–33. https://doi.org/10.1111/10.1515/jvetres-2016-0005.
  41. Tkachenko, H., Grudniewska, J., & Pękala, A. (2016b). Muscle biochemistry in rainbow trout Oncorhynchus mykiss following Yersinia ruckeri vaccination. Baltic Coastal Zone – Journal of Ecology and Protection of the Coastline, 20, 137–159.
  42. Tkachenko, H., Grudniewska, J., Pękala, A., & Paździor, E. (2016c). Effects of vaccination against Yersinia ruckeri on oxidative stress biomarkers and liver and heart biochemistry in rainbow trout (Oncorhynchus mykiss). Archives of Polish Fisheries, 24, 33–46. https://doi.org/10.1111/10.1515/aopf-2016-0004.
  43. Tkachenko, H., Komorowski, I., Grudniewska, J., & Kurhaluk, N. (2015). Przemiany metaboliczne w wątrobie pstrąga tęczowego (Oncorhynchus mykiss, Walbaum) immunizowanego szczepionką przeciwko Yersinia ruckeri [Metabolic changes in the liver of rainbow trout (Oncorhynchus mykiss, Walbaum) immunized with the Yersinia ruckeri vaccine]. Słupskie Prace Biologiczne, 12, 367–391.
  44. Welch, T. J., & LaPatra, S. (2016). Yersinia ruckeri lipopolysaccharide is necessary and sufficient for eliciting a protective immune response in rainbow trout (Oncorhynchus mykiss, Walbaum). Fish & Shellfish Immunology, 49, 420–426. https://doi.org/10.1016/j.fsi.2015.12.037.
  45. Wiens, G. D., & Vallejo, R. L. (2010). Temporal and pathogen-load dependent changes in rainbow trout (Oncorhynchus mykiss) immune response traits following challenge with biotype 2 Yersinia ruckeri. Fish & Shellfish Immunology, 29(4), 639–647. https://doi.org/10.1016/j.fsi.2010.06.010.
  46. Zar, J. H. (1999). Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey.