Immunology in Sturgeons with a Focus on the Siberian Sturgeon Mechanisms, Responses to Stress and Stimulation

Chapter

Abstract

This chapter aims to explore the state of knowledge about the immune mechanisms in sturgeon with a focus on the Siberian sturgeon (Acipenser baerii), stress factors that can disrupt the immune system and the sources of stimulation. Studies conducted carried out for several decades on sturgeon suggest specificities of their immune system compared to other fish species: special organs (meningeal myeloid tissue, tissues surrounding the heart), particularity of cells and components of immunity (larger white blood cells, lack of myeloperoxidase in neutrophils that are classified as heterophils). Other features have also been shown, i.e. the slow development of organs of immunity, the rapid response to acute stress, but also the great capacity for recovery from stress, all of which give a particular character to the sturgeon in the family of farmed fishes. Stress factors that can influence the immune system of sturgeons have also been researched in the last decade, with strong certainties about the influence of temperature, oxygen levels, pathogens and the presence in water of chemical substances. More and more programs on the research of solutions to boost the immune system have been implemented in recent years, with proven stimulatory actions on immunity factors (vaccines, probiotics, prebiotics, symbiotics, certain vitamins polysaccharides, plants and their components) and more mixed results (proteins, amino acids and certain vitamins). However, it seems that one domain is much less explored: the correlation between the pathogen, the host immunity and its environment. Nevertheless, this correlation is essential in the choice of solutions, which can be proposed, in particular in the field of immunostimulation.

Keywords

Acipenser baerii Innate immunity Acquired immunity Immunity boosters Stress factors 

Notes

Acknowledgments

The authors wish to thank Dr. Karine Pichavant-Rafini (ORPHY laboratory, EA4324) and Michel Rafini (professor at the Language Dept.) of Brest University (France), for their numerous constructive comments and for their help in improving the quality of the English language.

References

  1. Abdelsalam M, Asheg A, Eissa AE (2013) Streptococcus dysgalactiae: an emerging pathogen of fishes and mammals. Int J Vet Sci Med 1:1–6CrossRefGoogle Scholar
  2. Adel M, Nayak V, Lazado CC, Yeganeh S (2016) Effects of dietary prebiotic GroBiotic®-a on growth performance, plasma thyroid hormones and mucosal immunity of great sturgeon, Huso huso (Linnaeus, 1758). J Appl Ichthyol 32:825–831CrossRefGoogle Scholar
  3. Adela M, Yeganehb S, Dadarc M, Sakaid M, Dawoode MAO (2016) Effects of dietary Spirulina platensis on growth performance, humoral and mucosal immune responses and disease resistance in juvenile great sturgeon (Huso huso Linnaeus, 1754). Fish Shellfish Immunol 56:436–444CrossRefGoogle Scholar
  4. Akrami R, Hajimoradloo A (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of juvénile beluga, Huso huso (Linnaeus, 1758). J World Aquacult Soc 40:771–779Google Scholar
  5. Aramli MS, Kamangarb B, Nazari RM (2015) Effects of dietary β-glucan on the growth and innate immune response of juvenile Persian sturgeon, Acipenser persicus. Fish Shellfish Immunol 47:606–610CrossRefGoogle Scholar
  6. Balm PHM, Lambert JDG, Wendelaar Bonga SE (1989) Corticosteroides biosynthesis in the interregnal cells of teleost fish, Oreochromis mossambicus. Gen Comp Endocrinol 76:53–62CrossRefGoogle Scholar
  7. Berthet J (2011) Les plaquettes sanguines: cellules inflammatoires de l'immunité. Rôle fonctionnel du Toll-Like Receptor 4 exprimé par les plaquettes sanguines en tant que cellules inflammatoires de l'immunité. Editions Universitaires Europeennes EUEGoogle Scholar
  8. Bigarré L, Lesne M, Lautraite A, Chesneau V, Leroux A, Jamin M, Boitard PM, Toffan A, Prearo M, Labrut S, Daniel P (2016) Molecular identification of iridoviruses infecting various sturgeon species in Europe. J Fish Dis. doi: 10.1111/jfd.12498 CrossRefPubMedGoogle Scholar
  9. Bishkoul GR, Halimi M, Norousta R (2015) The anesthetic effects of MS-222 (tricaine methanesulfonate) on some hematological parameters of sterlet, Acipenser ruthenus. Comp Clin Pathol 24:89–92CrossRefGoogle Scholar
  10. Castillo A, Razquin B, Villena AJ, Zapata AG, López-Fierro P (1998) Thymic barriers to antigen entry during the post-hatching development of the thymus of rainbow trout, Oncorhynchus mykiss. Fish Shellfish Immunol 8:157–170CrossRefGoogle Scholar
  11. Chinese Herbal Medicine Immunopotentiator for Sturgeon Fingerling. CN 102552411 A. http://www.google.us/patents/CN102552411A?cl=en
  12. Dabrowski K (1994) Primitive Actinopterigian fishes can synthesize ascorbic acid. Cell Mol Life Sci 50:745–748CrossRefGoogle Scholar
  13. Das S, Hirano M, Tako R, McCallister C, Nikolaidis N (2012) Evolutionary genomics of immunoglobulin-encoding loci in vertebrates. Curr Genomics 13(2):95–102CrossRefGoogle Scholar
  14. De Kinkelin P, Michel CH, Ghittino P (1985) Précis de Pathologie des poissons INRA–OIE, Paris, p 348Google Scholar
  15. De Schryver P, Sinha AK, Kunwar PS, Baruah K, Verstraete W, Boon N, De Boeck G, Bossier P (2010) Poly-β-hydroxybutyrate (PHB) increases growth performance and intestinal bacterial range-weighted richness in juvenile European sea bass, Dicentrarchus labrax. Appl Microbiol Biotechnol 86:1535–1541CrossRefGoogle Scholar
  16. Docan A, Dediu L, Cristea V (2012) Effect of feeding with different dietary protein level on leukocytes population in juvenile Siberian sturgeon, Acipenser baerii Brandt. Arch Zootech 15(4):59–67Google Scholar
  17. Dove ADM, Arnold J, Clauss TM (2010) Blood cells and serum chemistry in the world’s largest fish: the whale shark Rhincodon typus. Aquat Biol 9:177–183CrossRefGoogle Scholar
  18. Drennan JD, Lapatra SE, Swan CM, Ireland S, Cain KD (2007) Characterization of serum and mucosal antibody responses in white sturgeon (Acipenser transmontanus Richardson) following immunization with WSIV and a protein hapten antigen. Fish Shellfish Immunol 23(3):657–669CrossRefGoogle Scholar
  19. Eslamloo K, Falahatkar B (2014) Variation of some physiological and immunological parameters in Siberian sturgeon (Acipenser baeri, Brandt, 1869) subjected to an acute stressor. J Appl Anim Welf Sci 17:29–42CrossRefGoogle Scholar
  20. Eslamloo K, Falahatkar B, Yokoyama S (2012) Effects of dietary bovine lactoferrin on growth, physiological performance, iron metabolism and non-specific immune responses of Siberian sturgeon Acipenser baeri. Fish Shellfish Immunol 32:976–985CrossRefGoogle Scholar
  21. Evans BI, Li MIJ (2014) Investigations on the function of immune-like cell clusters in the larval lake sturgeon brain. Paper presented at the 144th annual meeting of American Fisheries Society, Quebec City Canada, August 17–21, 2014Google Scholar
  22. Falahatkar B (2005) The effect of dietary vitamin C on some of hematologhc biochemistry and growth indexes of great sturgeon (Huso huso). Ph.D. Thesis, Tarbiat Modaarres University, Tehran, Iran (Persian)Google Scholar
  23. Falahatkar B, Poursaeid S (2013) Stress responses of great sturgeon Huso huso subjected to husbandry stressors. Aquac Int 21(4):947–959CrossRefGoogle Scholar
  24. Fan C, Wang J, Zhang X, Song J (2015) Functional C1q is present in the skin mucus of Siberian sturgeon (Acipenser baerii). Integr Zoolog 10:102–110CrossRefGoogle Scholar
  25. Fänge R (1986) Lymphoid organs in sturgeons (Acipenseridae). Veterinary Immunology and immunopathology. Fish. Immunology 12:153–161Google Scholar
  26. Feng GP, Zhuang P, Zhang LZ, Duan M, Liu JY (2012) Effects of temperature on oxidative stress biomarkers in juvenile Chinese sturgeon (Acipenser Sinensis) under laboratory conditions. Adv Mater Res 343-344:497–504CrossRefGoogle Scholar
  27. Gatesoupe FJ (2008) Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotic treatments. J Mol Microbiol Biotechnol 14:107–114CrossRefGoogle Scholar
  28. Genten F, Terwinghe E, Danguy A (2010) Histologie illustrée du poisson. Quae, FranceGoogle Scholar
  29. Geraylou Z, Vanhove MPM, Souffreau C, Rurangwa E, Buyse J, Ollevier F (2012) In vitro selection and characterization of putative probiotics isolated from the gut of Acipenser baeri (Brandt, 1869). Aquac Res 45(2):341–352CrossRefGoogle Scholar
  30. Geraylou Z et al (2013a) Prebiotic effects of arabinoxylan oligosaccharides on juvenile Siberian sturgeon (Acipenser baeri) with emphasis on the modulation of the gut microbiota using 454 pyrosequencing. FEMS Microbiol Ecol 86:357–371CrossRefGoogle Scholar
  31. Geraylou Z et al (2013b) Effects of dietary arabinoxylan-oligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baeri). Fish Shellfish Immunol 35:766–775CrossRefGoogle Scholar
  32. Geraylou Z, Rurangwa E, Van De Wiele T, Courtin CM, Delcour JA, Buyse J, Ollevier F (2014) Fermentation of arabinoxylan-oligosaccharides, Oligofructose and their monomeric sugars by hindgut bacteria from Siberian sturgeon and African catfish in batch culture in vitro. J Aquac Res Developm 5:230Google Scholar
  33. Gradil AM, Wright GM, Speare DJ, Wadowska DW, Purcell S, Fast MD (2014a) The effects of temperature and body size on immunological development and responsiveness in juvenile shortnose sturgeon (Acipenser brevirostrum). Fish Shellfish Immunol 40:545–555CrossRefGoogle Scholar
  34. Gradil AM, Wright GM, Wadowska DW, Mark D (2014b) Ontogeny of the immune system in Acipenserid juveniles. Dev Comp Immunol 44:303–314CrossRefGoogle Scholar
  35. Hoseini SM, Mirghaed AT, Mazandarani M, Zoheiri F (2016a) Serum cortisol, glucose, thyroid hormones’ and non-specific immune responses of Persian sturgeon, Acipenser persicus to exogenous tryptophan and acute stress. Aquaculture 462:17–23CrossRefGoogle Scholar
  36. Hoseini SM, Tort L, Abolhasani MH, Rajabiesterabadi H (2016b) Physiological, ionoregulatory, metabolic and immune responses of Persian sturgeon, Acipenser persicus (Borodin, 1897) to stress. Aquac Res 47:3729–3739CrossRefGoogle Scholar
  37. Hoseinifar SH, Mirvaghefi A, Merrifield DL, Amiri B, Yelghi S, Bastami K (2011) The effects of oligofructose on growth performance, survival and autochthonous intestinal microbiota of beluga (Huso huso) juveniles. Aquac Nutr 17:498–504CrossRefGoogle Scholar
  38. Huang SY, Li JS, Guan RZ (2014) The effect of sturgeon chondroitin sulfate on the number of mast cells in immune organ of mice. J Fujian Fisheries 1006–5601(6):442–445Google Scholar
  39. Icardo JM, Colvee E, Cerra MC, Tota B (2002) The structure of the conus arteriosus of the sturgeon (Acipenser naccarii) heart: II. The myocardium, the Subepicardium, and the conus-aorta transition. Anat Rec 268:388–398Google Scholar
  40. Jafarzadeh E, Khara H, Ahmadnezhad M (2015) Effects of symbiotic (Biomin IMBO) on haematological and immunological components of Russian sturgeon, Acipenser guldenstadti. Comp Clin Pathol 24:1317–1323CrossRefGoogle Scholar
  41. Kalbassi MR, Soltani M, Pourbakhsh SA, Adams A (2000) Humoral immune response of cultures Persian sturgeon (Acipenser persicus) to four different Aeromonas hydrophila antigens. Arch Razi Ins 51:75–84Google Scholar
  42. Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274:1–14CrossRefGoogle Scholar
  43. Khoshbavar-Rostami HA, Soltani M, Hassan HMD (2006) Immune response of great sturgeon (Huso huso) subjected to long-term exposure to sublethal concentration of the organophosphate, diazinon. Aquaculture 256:88–94CrossRefGoogle Scholar
  44. Kieffer MC, Kynard B (1993) Annual movements of shortnose and Atlantic sturgeons in the Merrimack river, Massachusetts. Trans Am Fish Soc 122:1088–1103CrossRefGoogle Scholar
  45. Kolida S, Gibson GR (2011) Symbiotics in health and disease. Annu Rev Food Sci Technol 2:373–393CrossRefGoogle Scholar
  46. Kolman H (2001) The humoral effects of EPIN in Siberian sturgeon (Acipenser Baerii Brandt). Arch Pol Fish 9(1):61–69Google Scholar
  47. Kolman H, Siwicki AK, Kolman R (1999a) Influence of O-antigen Aeromonas salmonicida on non-specific and specific immune responses in Siberian sturgeon, Acipenser baerii Brandt. Arch Polish Fish 7(1):93–102Google Scholar
  48. Kolman H, Kolman R, Siwicki AK (1999b) Influence of bacterial antigens on specific and non-specific immune response in bester (Huso huso L. × Acipenser ruthenus L.) fry F3. Czech J Anim Sci 44:255–261Google Scholar
  49. Kolman H, Kolman R, Krzysztof Siwicki A (2000) Non-specific defense mechanisms of russian sturgeon (Acipenser Guldenstaedti brant) reared in cages. Archives of polish. Fisheries 8(2):181–192Google Scholar
  50. Korneva ZV, Bednyakov DA (2011) Comparative characterization of the ultrastructure of intestinal epithelium of various sturgeon species. Inland Water Biol 4:446–454CrossRefGoogle Scholar
  51. Krayushkina LS, Semenova OG, Vyushina AV (2006) Level of serum cortisol and Na+/K+ ATP-ase activity of gills and kidneys in different acipenserids. J Appl Ichthyol 22:182–187CrossRefGoogle Scholar
  52. Kum C, Sekkin S (2011) The immune system drugs in fish: immune function, immunoassay, drugs. INTECH Open Access Publisher. doi:  10.5772/26869 CrossRefGoogle Scholar
  53. Lange MA, Govyadinova AA, Khrushchev NG (2000) Study on localization of haemopoietic tissue in sturgeon. Russ J Dev Biol 31:372–376CrossRefGoogle Scholar
  54. Lundqvist M, Pilstrom L, Strömberg S (1998) Ig heavy chain of the sturgeon (Acipenser baerii): cDNA sequence and diversity. Immunogenetics 48:372–382CrossRefGoogle Scholar
  55. Mahious AS, Van Loo J., Ollevier F (2006) Impact of the prebiotics, inulin and oligofructose on microbial fermentation in the spiral valve of Siberian sturgeon (Acipenser baerii), In Proceedings of World Aquaculture Society Meeting. World Aquaculture Society, Florence, Italy, p 709Google Scholar
  56. Maxime V, Nonnotte G, Peyraud C, Williot P, Truchot JP (1995) Circulatory and respiratory effects on hypoxia stress in Siberian sturgeon. Respir Physiol 100:203–212CrossRefGoogle Scholar
  57. Mayer G, Hudrisier D (2016) Response to antigen: processing and presentation MHC restriction and rôle of thymus. In: Microbiology et Immunology On-line. http://www.microbiologybook.org/bowers/ant-pres.htm. Accessed 22 July 2016
  58. Meng N, Haishen W, Jifang L, Meili C, Yan B, Yuanyuan R, Mo Z, Zhifei S (2014) The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenchii) to stocking density and hypoxia stress. Fish Sellfish Immunol 36:325–335Google Scholar
  59. Merlot E (2004) Conséquences du stress sur la fonction immunitaire chez les animaux d’élevage. INRA Prod Anim 17(4):255–264Google Scholar
  60. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J et al (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302:1–18CrossRefGoogle Scholar
  61. Method for Evaluating Immunization Effect of Sturgeon Bacterial Disease Whole-Cell Inactivated Vaccine. http://www.technology-x.net/G01N/200810202810.html
  62. Mohajer Esterabadi M, Vahabzadeh H, Zamani AA, Soudagar M, Ghorbani Nasrabadi R (2010) Effect of dietary immunogen prebiotics on growth and survival indices of giant sturgeon (Huso huso Linne, 1758) juveniles. J Fisheries 4:610–672Google Scholar
  63. Mohammadizarejabad A, Bastami KD, Sudagar M, Motlagh SP (2010) Haematology of great sturgeon (Huso huso Linnaeus, 1758) juvenile exposed to clove powder as an anaesthetic. Comp Clin Pathol 19(5):465–468CrossRefGoogle Scholar
  64. Najdegerami EH, Tran TN, Defoirdt T, Marzorati M, Sorgeloos P, Boon N, Bossier P (2012) Effects of poly-b-hydroxybutyrate (PHB) on Siberian sturgeon (Acipenser baerii) fingerlings performance and its gastrointestinal tract microbial community. FEMS Microbiol Ecol 79:25–33CrossRefGoogle Scholar
  65. Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14CrossRefGoogle Scholar
  66. Palić D, Beck LS, Palić J, Andreasen CB (2011) Use of rapid cytochemical staining to characterize fish blood granulocytes in species of special concern and determine potential for function testing. Fish Shellfish Immunol 30:646–652CrossRefGoogle Scholar
  67. Piper RG, McElwain IB, Orme LE, McCraren JP, Fowler LG, Leonard JR (1982) Fish hatchery management. U.S. Department of the Interior, U.S. Fish and Wildlife Service, Washington, D.C.Google Scholar
  68. Pourgholam MA, Khara H, Safari R, Yazdani Sadati MA, Aramli MS (2015) Influence of lactobacillus plantarum inclusion in the diet of Siberian sturgeon (Acipenser baerii) on performance and hematological parameters. Turk J Fish Aquat Sci. doi: 10.4194/1303-2712-v17_1_01
  69. Pourgholam MA, Khara H, Safari R, Yazdani Sadati MA, Aramli MS (2016) Dietary administration of lactobacillus plantarum enhanced growth performance and innate immune response of Siberian sturgeon, Acipenser baerii. Probiotics Antimicrob Proteins 8(1):1–7CrossRefGoogle Scholar
  70. Ringø E, Olsen R, Gifstad T, Dalmo R, Amlund H, Hemre GL, Bakke AM (2010) Prebiotic in aquaculture: a review. Aquac Nutr 16:117–136CrossRefGoogle Scholar
  71. Safarpour Amlashi A, Falahatkar B, Sattari M, Tolouei Gilani MH (2011) Effect of dietary vitamin E on growth, muscle composition, haematological and immunological parameters of sub-yearling beluga Huso huso L. Fish Shellfish Immunol 30:807–814CrossRefGoogle Scholar
  72. Scharrer E (1944) The histology of the meningeal myeloid tissue in the ganoids Amia and Lepisosteus. Anat Rec 88:291–310CrossRefGoogle Scholar
  73. Sfacteriaa A, Brinesb M, Blankc U (2015) The mast cell plays a central role in the immune system of teleost fish. Mol Immunol 63:3–8CrossRefGoogle Scholar
  74. Shamova OV, Orlov DS, Balandin SV, Shramova EI, Tsvetkova EV, Panteleev PV, Leonova YF, Tagaev AA, Kokryakov VN, Ovchinnikova TV (2014) Acipensins novel antimicrobial peptides from leukocytes of the Russian sturgeon Acipenser gueldenstaedtii. Acta Nat 4(23):99–109Google Scholar
  75. Silphaduang U, Colorni A, Noga EJ (2006) Evidence for widespread distribution of piscidin antimicrobial peptides in teleost fish. Dis Aquat Org 72:241–252CrossRefGoogle Scholar
  76. Sokolowski MS, Allam BA, Dunton KJ, Clark MA, Kurtz EB, Fast MD (2012) Immunophysiology of Atlantic sturgeon, Acipenser oxyrinchus oxyrinchus (Mitchill), and the relationship to parasitic copepod, Dichelesthium oblongum (Abilgaar) infection. J Fish Dis 35(9):649–660CrossRefGoogle Scholar
  77. Song C, Niu C, Zhu H (2009) Effects of polysaccharides injection on the non-specific immune responses of Amur sturgeon Acipenser Schrenkii. Acta Hydrobiol Sin 33(3):455–460Google Scholar
  78. Stet RJM, Appelkvist P, Lundqvist ML, Appelkvist P, Hermsen T, Pilström L, Stet RJM (1999) Characterization of beta2-microglobulin in a primitive fish, the Siberian sturgeon (Acipenser baeri). Immunogenetics 50:79–83CrossRefGoogle Scholar
  79. Subbotkina TA, Subbotkin MF (2003) Lysozyme content in organs and blood serum in various species in the Volga river. J Evol Biochem Physiol 39:537–546CrossRefGoogle Scholar
  80. Ta’ati R, Soltani M, Bahmani M, Zamini AA (2011) Effects of the prebiotics Immunoster and Immunowall on growth performance of juvenile beluga (Huso huso). J Appl Ichthyol 27:796–798CrossRefGoogle Scholar
  81. Tatina M, Bahmani M, Soltani M, Abtahi B, Gharibkhani M (2010) Effects of different levels of dietary vitamins C and E on some of hematological and biochemical parameters of Sterlet (Acipenser ruthenus). J Fish Aquat Sci 5:1–11CrossRefGoogle Scholar
  82. Tort L, Balasch JC, Mackenzie S (2003) Fish immune system. A crossroads between innate and adaptive responses. Inmunología 22(3):277–286Google Scholar
  83. Vinolo MAR, Rodrigues HG, Nachbar RT, Curi R (2011) Regulation of inflammation by short chain fatty acids. Forum Nutr 3(10):858–876Google Scholar
  84. Xie Z, Niu C, Zhang Z, Bao L (2006) Dietary ascorbic acid may be necessary for enhancing the immune response in Siberian sturgeon (Acipenser baeri), a species capable of ascorbic acid biosynthesis. Comp Biochem Physiol Part A 145:152–157CrossRefGoogle Scholar
  85. Yousefan M, Amiris MS (2009) A review of prebiotic in aquaculture for fish and shrimp. Afr J Biotechnol 8:7313–7318Google Scholar
  86. Zarejabad AM, Sudagar M, Pouralimotlagh S, Bastami KD (2010) Effects of rearing temperature on hematological and biochemical parameters of great sturgeon (Huso huso Linnaeus, 1758) juvenile. Comp Clin Pathol 19(4):367–371CrossRefGoogle Scholar
  87. Zexia G, Weimin W, Yi Y, Abbas K, Dapeng L, Guiwei Z, Diana JS (2007) Morphological studies of peripheral blood cells of the Chinese sturgeon, Acipenser sinensis. Fish Physiol Biochem 33:213–222CrossRefGoogle Scholar
  88. Zhou J, Nagarkatti P, Zhong Y, Nagarkatti M (2010) Immune modulation by chondroitin sulfate and its degraded disaccharide product in the development of an experimental model of multiple sclerosis. J Neuroimmunol 223(1–2):55–64CrossRefGoogle Scholar
  89. Zhu L, Yan Z, Feng M, Peng D, Guo Y, Hu X, Ren L, Sun Y (2014) Identification of sturgeon IgD bridges the evolutionary gap between elasmobranchs and teleosts. Dev Comp Immunol 42:138–147CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Prunier Manufacture et Les Esturgeons de L’AdourMontpon MénestérolFrance

Personalised recommendations