Advertisement

Pre- and Probiotics and Immunostimulants in Siberian Sturgeon: Gut Microbiota and Immunomodulation

  • Zahra Geraylou
Chapter
First Online:

Abstract

The endogenous gut microbiota serves a variety of functions in the host. They protect the host against pathogen invasion to the gastrointestinal tract, in mediating the development, maintenance and effective functionality of the intestinal mucosa and gut-associated lymphoid tissue. Gut microbiota is capable and able to support host digestive function via the production of wide range of exogenous digestive enzymes and vitamins. Therefore, manipulation of the gut microbiota through dietary supplementation of beneficial microbe (probiotics), and non-digestible substances (prebiotics) that selectively stimulate the growth of one or limited health-promoting bacteria in the intestine of the host, not only provides benefit to the host from nutritional point of view but also as an alternate viable therapeutic modality to overcome the adverse effects of antibiotics and drugs.

The use of immunostimulants for the prevention of fish disease has become more promising over the last decades. Immunostimulants enhance the innate defence mechanisms and increase resistance to specific pathogens by conferring the signals to the animal’s neuro-immune-endocrine system or various cell signalling pathways.

The effects of pre- and probiotics or their combination, synbiotic, and immunostimulants on Siberian sturgeon growth performance, intestinal microbiota modulation, innate immune response and health have been discussed in this chapter.

Keywords

Prebiotic Probiotic Symbiotic Immunostimulants Gut microbiota Immune response Siberian sturgeon 
This is a preview of subscription content, log in to check access.

References

  1. Ahmadifar E, Akrami R, Ghelichi A et al (2011) Effects of different dietary prebiotic inulin levels on blood serum enzymes, hematologic, and biochemical parameters of great sturgeon (Huso huso) juveniles. Comp Clin Pathol 20:447–451CrossRefGoogle Scholar
  2. Ai Q, Xu H, Mai K (2011) Effects of dietary supplementation of Bacillus subtilis and fructooligosaccharide on growth performance, survival, non-specific immune response and disease resistance of juvenile large yellow croaker, Larimichthys crocea. Aquaculture 317:155–161CrossRefGoogle Scholar
  3. Akrami R, Abdolmajid H, Matinfar A et al (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of juvenile beluga, Huso huso (Linnaeus, 1758). J World Aquacult Soc 40:771–779CrossRefGoogle Scholar
  4. Akrami R, Iri Y, Rostami HK et al (2013a) Effect of dietary supplementation of fructooligosaccharide (FOS) on growth performance, survival, Lactobacillus bacterial population and hemato-immunological parameters of stellate sturgeon (Acipenser stellatus) juvenile. Fish Shellfish Immunol 35:1235–1239PubMedCrossRefGoogle Scholar
  5. Akrami R, Razeghi Mansour M, Ghobadi S et al (2013b) Effect of prebiotic mannan oligosaccharides on haematological and blood serum biochemical parameters of great sturgeon (Huso huso Linnaeus, 1754). J Appl Ichthyol 29:1214–1218CrossRefGoogle Scholar
  6. Al-Dohail MA, Hashim R, Aliyu-Paiko M (2009) Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African Catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquac Res 40:1642–1652CrossRefGoogle Scholar
  7. Anderson DP (1992) Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annu Rev Fish Dis 2:281–307CrossRefGoogle Scholar
  8. Askarian F, Kousha A, Ringø E (2009) Isolation of lactic acid bacteria from the gastrointestinal tract of beluga (Huso huso) and Persian sturgeon (Acipenser persicus). J Appl Ichthyol 25:91–94CrossRefGoogle Scholar
  9. Askarian F, Kousha A, Salma W (2011) The effect of lactic acid bacteria administration on growth, digestive enzyme activity and gut microbiota in Persian sturgeon (Acipenser persicus) and beluga (Huso huso) fry. Aquac Nutr 17:488–497CrossRefGoogle Scholar
  10. Bacanu GM, Oprea L (2013) Differences in the gut microbiota between wild and domestic Acipenser ruthenus evaluated by denaturing gradient gel electrophoresis. Rom Biotechnol Lett 18:8069–8076Google Scholar
  11. Bauer ON, Pugachev ON, Voronin VN (2002) Study of parasites and diseases of sturgeons in Russia: a review. J Appl Ichthyol 18:420–429CrossRefGoogle Scholar
  12. Bondad-Reantaso MG, Subasinghe RP, Arthur JR et al (2005) Disease and health management in Asian aquaculture. Vet Parasitol 132:249–272PubMedCrossRefGoogle Scholar
  13. Bronzi P, Rosenthal H, Gessner J (2011) Global sturgeon aquaculture production: an overview. J Appl Ichthyol 27:169–175CrossRefGoogle Scholar
  14. Brun R, Nougayrede P, Chene P et al (1991) Bilan sanitaire de 2 ans d’élevage d’Acipenser baerii en piscicultures intensives. In: Williot P (ed) Acipenser. Cemagref Publishers, Antony, France, pp 429–437Google Scholar
  15. Brunetti R, Gasparri F, Marturano S, Prearo M (2006) Pseudomonas fluorescens Infection in farmed Siberian sturgeon (Acipencer baeri). Ittiopatologia 3:221–226Google Scholar
  16. Brunt J, Austin B (2005) Use of a probiotic to control lactococcosis and streptococcosis in rainbow Oncorhynchus mykiss (Walbaum). J Fish Dis 28:693–701PubMedCrossRefGoogle Scholar
  17. Buddington RK, Doroshov SI (1986) Structural and functional relations of the white sturgeon alimentary canal (Acipenser transmontanus). J Morphol 190:201–213CrossRefGoogle Scholar
  18. Buddington RK, Krogdahl A, Bakke-Mckellep AM (1997) The intestines of carnivorous fish: structure and functions and the relations with diet. Acta Physiol Scand Suppl 638:67–80PubMedGoogle Scholar
  19. Burr G, Gatlin D, Ricke S (2005) Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. J World Aquacult Soc 36:425–436CrossRefGoogle Scholar
  20. Cahill MM (1990) Bacterial flora of fishes: a review. Microb Ecol 19:21–41PubMedCrossRefGoogle Scholar
  21. Callman JL, Macy JM (1984) The predominant anaerobe from the spiral intestine of hatchery-raised sturgeon (Acipenser transmontanus), a new Bacteroides species. Arch Microbiol 140:57–65CrossRefGoogle Scholar
  22. Cao HP, He S, Lu LQ et al (2010) Characterization and phylogenetic analysis of the bitrichous pathogenic Aeromonas hydrophila isolated from diseased Siberian sturgeon (Acipenser baerii). Isr J Aquacult Bamidgeh 62:181–186Google Scholar
  23. Catton WT (1951) Blood cell formation in certain teleost fishes. Blood 6:39–60PubMedGoogle Scholar
  24. Cerezuela R, Cuesta A, Meseguer J et al (2012) Increases in immune parameters by inulin and Bacillus subtilis dietary administration to gilthead seabream (Sparus aurata L.) did not correlate with disease resistance to Photobacterium damselae. Fish Shellfish Immunol 32:1032–1040PubMedCrossRefGoogle Scholar
  25. Chen MH, Hung SW, Shyu CL et al (2012) Lactococcus lactis subsp. lactis infection in Bester sturgeon, a cultured hybrid of Huso huso × Acipenser ruthenus, in Taiwan. Res Vet Sci 93:581–588PubMedCrossRefGoogle Scholar
  26. Clements KD (1997) Fermentation and gastrointestinal microorganisms in fishes. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall microbiology series, New York, pp 156–198CrossRefGoogle Scholar
  27. Courtin CM, Delcour JA (2002) Arabinoxylans and endoxylanases in wheat flour bread-making. J Cereal Sci 35:225–243CrossRefGoogle Scholar
  28. Daprà F, Gai F, Palmegiano GB et al (2009) Siberian sturgeon (Acipenser baeri, Brandt JF 1869) gut: anatomic description. Int Aquat Res 1:45–60Google Scholar
  29. De Simone C, Salvadori BB, Negri R (1986) The adjuvant effect of yogurt on production of γ-interferon by Con A-stimulated human peripheral blood lymphocytes. Nutr Rep Int 33:419–433Google Scholar
  30. Defoirdt T, Halet D, Vervaeren H et al (2007a) The bacterial storage compound poly-β-hydroxybutyrate protects Artemia franciscana from pathogenic Vibrio campbellii. Environ Microbiol 9:445–452PubMedCrossRefGoogle Scholar
  31. Defoirdt T, Boon N, Sorgeloos P et al (2007b) Alternatives to antibiotics to control bacterial infections: luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25:472–479PubMedCrossRefGoogle Scholar
  32. Delaedt Y, Diallo MD, Rurangwa E et al (2008) Impact of Arabinoxylooligosaccharides on Microbial Community Composition and Diversity in The Gut of Siberian Sturgeon (Acipenser baeri), pp 183–184. Aquaculture Europe, Krakow, PolandGoogle Scholar
  33. Drzewina A (1905) Contribution a l’étude du tissu lymphoide des Ichthyopsidés. Archives de Zoologie Expérimentale et Générale 3:145–338Google Scholar
  34. Duncan L, Lovell RT (1994) Influence of vitamin C on the folate requirement of channel catfish, Ictalurus punctatus, for growth, hematopoiesis, and resistance to Edwardsiella ictalauri infection. Aquaculture 127:233–244CrossRefGoogle Scholar
  35. Ellis AE (1988) Fish vaccination. Academic Press, London, p 255Google Scholar
  36. Ellis AE (1999) Immunity to bacteria in fish. Fish Shellfish Immunol 9:291–308CrossRefGoogle Scholar
  37. Eslamlooa K, Falahatkara B, Yokoyamab S et al (2012) Effects of dietary bovine lactoferrin on growth, physiological performance, iron metabolism and non-specific immune responses of Siberian sturgeon Acipenser baerii. Fish Shellfish Immunol 32(6):976–985CrossRefGoogle Scholar
  38. Faramarzi M, Jafaryan H, Patimar R et al (2011) The effects of different concentrations of probiotic Bacillus spp and different bioencapsulation times on growth performance and survival rate of Persian sturgeon (Acipencer persicus) Larvae. World J Fish Marine Sci 3:145–150Google Scholar
  39. Faramarzi M, Jafaryan H, Roozbehfar R et al (2012a) Influences of probiotic Bacilli on ammonia and urea excretion in two conditions of starvation and satiation in Persian sturgeon (Acipenser persicus) larvae. Global Veterinaria 8:185–189Google Scholar
  40. Faramarzi M, Jafaryan H, Roozbehfar R et al (2012b) Influences of probiotic Bacilli via bioencapsulated Daphnia magna on resistance of Persian sturgeon larvae against challenge tests. Global Veterinaria 8:421–425Google Scholar
  41. Fäuge R (1986) Lymphoid organs in sturgeons (Acipenseridae). Vet Immunol Immunopathol 12:153–161CrossRefGoogle Scholar
  42. Francis-Floyd R (2000) Diseases history of cultured sturgeon in Florida, 1990–1999, Proceedings of the Florida sturgeon culture risk assessment workshop. April 6–7, 2000 Sarasota, Florida pp 33–37Google Scholar
  43. Fuller R (1989) Probiotics in man and animals. A review. J Appl Bacterial 66:365–378CrossRefGoogle Scholar
  44. Ganguly S, Prasad A (2012) Microflora in fish digestive tract plays significant role in digestion and metabolism. Rev Fish Biol Fish 22(1):11–16CrossRefGoogle Scholar
  45. Gao X, Ge L-q, Li M-y et al (2009) Effects of Bacillus spp. on the growth performance and digestibility of juvenile Acipenser baerii. J Hebei Normal Univ 33:377–382Google Scholar
  46. Gatesoupe FJ (1999) The use of probiotics in aquaculture. Aquaculture 180:147–165CrossRefGoogle Scholar
  47. Gatlin DMIII (2002) Nutrition and fish health. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic Press, London, pp 671–702Google Scholar
  48. Geng X, Dong XH, Tan BP et al (2011) Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish Shellfish Immunol 31:400–406PubMedCrossRefGoogle Scholar
  49. Geraylou Z, Souffreau C, Rurangwa E et al (2012) Effects of arabinoxylan-oligosaccharides (AXOS) on juvenile Siberian sturgeon (Acipenser baerii) performance, immune responses and gastrointestinal microbial community. Fish Shellfish Immunol 33:718–724PubMedCrossRefGoogle Scholar
  50. Geraylou Z, Souffreau C, Rurangwa E et al (2013a) Prebiotic effects of arabinoxylan oligosaccharides on juvenile Siberian sturgeon (Acipenser baerii) with emphasis on the modulation of the gut microbiota using 454 pyrosequencing. FEMS Microbiol Ecol 86:357–371PubMedCrossRefGoogle Scholar
  51. Geraylou Z, Souffreau C, Rurangwa E et al (2013b) Effects of dietary arabinoxylanoligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baerii). Fish Shellfish Immunol 35:766–775PubMedCrossRefGoogle Scholar
  52. Geraylou Z, Vanhove MPM, Souffreau C et al (2014) In vitro selection and characterization of putative probiotics isolated from the gut of Acipenser baerii (Brandt, 1869). Aquac Res 45:341–352CrossRefGoogle Scholar
  53. Gerogi TA, Beedle D (1978) The histology of the excretory kidney of the paddlefish (Polyodon spathula). J Fish Biol 12:587–590CrossRefGoogle Scholar
  54. Ghanbari M, Rezaei M, Jami M et al (2009) Isolation and characterization of Lactobacillus species from intestinal contents of beluga (Huso huso) and Persian sturgeon (Acipenser persicus). Iran J Vet Res 10:152–157Google Scholar
  55. Gibson GR (2004) Fibre and effects on probiotics (the prebioticconcept). Clin Nutr Suppl 1:25–31CrossRefGoogle Scholar
  56. Gibson R, Roberfroid MR (1995) Dietary modulation of the human colonic microbiota introducing the concept of prebiotics. J Nutr 125:1401–1412PubMedGoogle Scholar
  57. Gomez GD, Balcazar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154PubMedCrossRefGoogle Scholar
  58. Grootaert C, Van den Abbeele P, Marzorati M et al (2009) Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol Ecol 69:231–242PubMedCrossRefGoogle Scholar
  59. Gutowska MA, Drazen JC, Robison BH (2004) Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp Biochem Physiol A 139:351–358CrossRefGoogle Scholar
  60. Halet D, Defoirdt T, Van Damme P et al (2007) Poly-β-hydroxybutyrate-accumulating bacteria protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. FEMS Microbiol Ecol 60:363–369PubMedCrossRefGoogle Scholar
  61. Hamlin HJ, Moore BC, Edwards TM et al (2008) Nitrate-induced elevations in circulating sex steroid concentrations in female Siberian sturgeon (Acipenser baerii) in commercial aquaculture. Aquaculture 281:118–125CrossRefGoogle Scholar
  62. Hardie LJ, Fletcher TC, Secombes CJ (1991) The effect of dietary vitamin C on the immune response of the Atlantic salmon (Salmo salar L.) Aquaculture 95:201CrossRefGoogle Scholar
  63. He S, Xu G, Wu Y (2003) Effects of IMO and FOS on the growth performance and non-specific immunity in hybrid tilapia. Chinese Feed 23:14–15Google Scholar
  64. Hoseinifar SH, Mirvaghefi A, Merrifield DL (2011a) The effects of dietary inactive brewer’s yeast Saccharomyces cerevisiae var. ellipsoideus on the growth, physiological responses and gut microbiota of juvenile beluga (Huso huso). Aquaculture 318:90–94CrossRefGoogle Scholar
  65. Hoseinifar SH, Mirvaghefi A, Merrifield DL et al (2011b) The study of some haematological and serum biochemical parameters of juvenile beluga (Huso huso) fed oligofructose. Fish Physiol Biochem 37:91–96PubMedCrossRefGoogle Scholar
  66. Hoseinifar SH, Mirvaghefi A, Mojazi Amiri B et al (2011c) The effects of oligofructose on growth performance, survival and autochthonous intestinal microbiota of beluga (Huso huso) juveniles. Aquac Nutr 17:498–504CrossRefGoogle Scholar
  67. Iranshahi F, Faramarzi M, Kiaalvandi S et al (2011) The Enhancement of Growth and Feeding Performance of Persian Sturgeon (Acipenser persicus) Larvae by Artemia urmiana Nauplii Bioencapsulated via Baker’s Yeast (Saccharomyces cerevisiae). J Anim Vet Adv 10:2730–2735Google Scholar
  68. Irianto A, Austin B (2002) Use of probiotics to control furunculosis in rainbow trout Oncorhynchus mykiss (Walbaum). J Fish Dis 25:333–342CrossRefGoogle Scholar
  69. Jeney G, Anderson DP (1993) Glucan injection or bath exposure given alone or in combination with a bacterin enhance the nonspecific defence mechanisms in rainbow trout (Oncorhynchus mykiss). Aquaculture 116:315–329CrossRefGoogle Scholar
  70. Jeney G, Jeney ZS (2002a) Application of immunostimulants for modulation of the non-specific defense mechanisms in sturgeon hybrid: Acipenser ruthenus × Acipenser. baerii. J Appl Ichthyol 18:416–419CrossRefGoogle Scholar
  71. Jeney G, Jeney ZS (2002b) Application of immunostimulants for modulation of the non-specific defense mechanisms in sturgeon hybrid: Acipenser ruthenus × Acipenser. baerii. J Appl Ichthyol 18:416–419CrossRefGoogle Scholar
  72. Jeney G, Galeotti M, Volpatti D et al (1997) Prevention of stress in rainbow trout (Oncorhynchus mykiss) fed diets containing different doses of glucan. Aquaculture 154:1–15CrossRefGoogle Scholar
  73. Kalia S, Kaith BS, Kaur I (2011) Cellulose fibers: bio- and nano-polymer composites: green chemistry and technology. Springer, Berlin, p 750. ISBN 978-3-642-17369-1CrossRefGoogle Scholar
  74. Karatas S, Ercan D, Steinum TM et al (2010) First isolation of a Flavobacterium johnsoniae like bacteria from cultured Russian sturgeon in Turkey. J Anim Vet Adv 9(14):1943–1946CrossRefGoogle Scholar
  75. Kato N, Konishi H, Shimao M, Sakazawa C (1992) Production of 3-hydroxybutyric acid trimer by Bacillus megaterium B-124. J Ferment Bioeng 73:246–247CrossRefGoogle Scholar
  76. Kesarcodi-Watson A, Kaspar H, Lategan MJ et al (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274:1–14CrossRefGoogle Scholar
  77. Kolman H (2002) Primary humoral response in Siberian sturgeon after exposure to anti-furunculosis bacterin. Czech J Anim Sci 47(5):183–188Google Scholar
  78. Kolman H, Kolman R, Siwicki AK (1999) Influence of bacterial antigens on specific and non-specific immune response in bester (Huso huso ×Acipenser ruthenus) fry F3. Czech J Anim Sci 44:255–261Google Scholar
  79. Larsen AM, Mohammed HH, Arias CR (2014) Characterization of the gut microbiota of three commercially valuable warm water fish species. J Appl Microbiol 116(6):1396–1404PubMedCrossRefGoogle Scholar
  80. Leadbetter EA, Rifkin IR, Hohlbaum AM et al (2002) Chromatin-IgG complexes activate B cells by dual engagement of Ig M and toll-like receptors. Nature 416:603–607PubMedCrossRefGoogle Scholar
  81. Liu Y, De Schryver P, Van Delsen B et al (2010) PHB-degrading bacteria isolated from the gastrointestinal tract of aquatic animals as protective actors against luminescent vibriosis. FEMS Microbiol Ecol 74:196–204PubMedCrossRefGoogle Scholar
  82. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci 104:11436–11440PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lukyanenko V I (1971) Immunobiologia ryb, Logk. i pishch. Prom., Moscow, 364 (in Russian)Google Scholar
  84. Lukyanenko V I (1989) Immunobiology in fishes: innate immunity Agropromizdat, Moskva, II, pp: 272 (in Russian)Google Scholar
  85. Lundqvist M, Bengten E, Stromberg S et al (1996) Light chain gene in the Siberian sturgeon (Acipenser baerii). J Immunol 157:2031–2038PubMedGoogle Scholar
  86. Lundqvist M, Stromberg S, Pilstrom L (1998) Ig heavy chain gene in the Siberian sturgeon (Acipenser baerii): cDNA sequence and diversity. Immunogenetics 48:372–338PubMedCrossRefGoogle Scholar
  87. Ma Z, Yang H, Li T et al (2009) Isolation and identification of pathogenic Aeromonas veronii isolated from infected Siberian sturgeon (Acipenser baerii). Wei Sheng Wu Xue Bao 49(10):1289–1294PubMedGoogle Scholar
  88. Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20(2):137–151PubMedCrossRefGoogle Scholar
  89. 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). World Aquaculture Society Aqua 2006, Florence, Meeting Abstract, p. 709Google Scholar
  90. McNeil NI (1984) The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39:338–342PubMedCrossRefGoogle Scholar
  91. Medzhitov R, Janeway C (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295–298PubMedCrossRefGoogle Scholar
  92. Meijer K, de Vos P, Priebe MG (2010) Butyrate and other short-chain fatty acids as modulators of immunity: what relevance for health? Curr Opin Clin Nutr Metab Care 13:715–721PubMedCrossRefGoogle Scholar
  93. Meng Y, Xiao HB, Zeng LB (2011) Isolation and identification of the hemorrhagic septicemia pathogen from Amur sturgeon, Acipenser schrenckii. J Appl Ichthyol 27:799–803CrossRefGoogle Scholar
  94. Merrifield L, Dimitroglou A, Foey A et al (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302:1–18CrossRefGoogle Scholar
  95. Mickeniene L (1999) Bacterial flora in the digestive tract of native and alien species of cray fish in Lithuania. Freshwater Cray fish 12:279–287Google Scholar
  96. Najdegerami EH, Tran TN, Defoirdt T et al (2012) Effects of poly-b-hydroxybutyrate (PHB) on Siberian sturgeon (Acipenser baerii) fingerlings performance and its gastrointestinal tract microbial community. FEMS Microbiol Ecol 79:25–33PubMedCrossRefGoogle Scholar
  97. Najdegerami EH, Baruah K, Shiri A et al (2015) Siberian sturgeon (Acipenser baerii) larvae fed Artemia nauplii enriched with poly-b-hydroxybutyrate (PHB): effect on growth performance, body composition, digestive enzymes, gut microbial community, gut histology and stress tests. Aquac Res 46(4):801–812CrossRefGoogle Scholar
  98. Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14PubMedCrossRefGoogle Scholar
  99. Nayak SK, Swain P, Mukherjee SC (2007) Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham). Fish Shellfish Immunol 23:892–896PubMedCrossRefGoogle Scholar
  100. Nhan D, Wille M, De Schryver P et al (2010) The effect of poly β-hydroxybutyrate on larviculture of the giant freshwater prawn (Macrobrachium rosenbergii). Aquaculture 302:76–81CrossRefGoogle Scholar
  101. Niewold TA, Schroyen M, Geens MM et al (2012) Dietary inclusion of arabinoxylan oligosaccharides (AXOS) down regulates mucosal responses to a bacterial challenge in a piglet model. J Funct Foods 4:626–635CrossRefGoogle Scholar
  102. Nikoskelainen S, Salminen S, Bylund G et al (2001) Characterisation of the properties of human- and dairy-derived probiotics for prevention of infectious diseases in fish. Appl Environ Microbiol 67:2430–2435PubMedPubMedCentralCrossRefGoogle Scholar
  103. Nilson BH, Solomon A, Bjorck L et al (1992) Protein L from Peptostreptococcus magnus binds to the light chain variable domain. J Biol Chem 267:2234–2239PubMedGoogle Scholar
  104. Ogbondeminu FS (1993) The occurrence and distribution of enteric bacteria in fish and water of tropical aquaculture ponds in Nigeria. J Aquacult Trop 8:61–66Google Scholar
  105. Ojeda JL, Icardo JM, Domezain A (2003) Renal corpuscle of the sturgeon kidney: an ultrastructural, chemical dissection and lectin-binding study. Anat Rec 272:563–573CrossRefGoogle Scholar
  106. Panigrahi A, Kiron V, Kobayashi T et al (2004) Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet Immunol Immunopathol 102:379–388PubMedCrossRefGoogle Scholar
  107. Patnaik P (2005) Perspectives in the modeling and optimization of PHB production by pure and mixed cultures. Crit Rev Biotechnol 25:153–171PubMedCrossRefGoogle Scholar
  108. Pond MJ, Stone DM, Alderman DJ (2006) Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Aquaculture 261:194–203CrossRefGoogle Scholar
  109. Pratt VC, Tappenden KA, McBurney MI et al (1996) Short chain fatty acid supplemented total parenteral nutrition improves nonspecific immunity after intestinal resection in rats. J Parent Enteral Nutr 20:264–271CrossRefGoogle Scholar
  110. Pryor GS, Royes JB, Chapman FA, Miles RD (2003) Mannanoligosaccharides in fish nutrition: effects of dietary supplementation on growth and gastrointestinal villi structure in gulf of Mexico sturgeon. N Am J Aquac 65:106–111CrossRefGoogle Scholar
  111. Raa J; Roerstadt G; Engstadt R et al (1992) The use of immunostimulants to increase resistance of aquatic organisms to microbial infections. In: Diseases in Asian aquaculture. I. Proceedings of the 1st Symposium On Diseases in Asian Aquaculture, 26–29 November 1990Google Scholar
  112. Rafatnezhad S, Falahatkar B (2011) Nitrogenous compounds and oxygen concentration as the key density dependent factors to optimize growth of beluga, Huso huso (Actinopterygii: Acipenseriformes: Acipenseridae), in circular fiberglass tanks. Acta Ichthyol Piscat 41(4):285–291CrossRefGoogle Scholar
  113. Ramirez RF, Dixon BA (2003) Enzyme production by obligate intestinal anaerobic bacteria isolated fromoscars (Astronotus ocellatus), angel fish (Pterophyllum scalare) and Southern founder (Paralichthys lethostigma). Aquaculture 227:417–426CrossRefGoogle Scholar
  114. Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci U S A 101:4596–4601PubMedPubMedCentralCrossRefGoogle Scholar
  115. Razeghi-Mansour M, Akrami R, Ghobadi SH et al (2012) Effect of dietary mannan oligosaccharide(MOS) on growth performance, survival, body composition and some hematological parameters in giant sturgeon juvenile (Huso huso Linnaeus, 1754). J Fish Physiol Biochem 38:829–835CrossRefGoogle Scholar
  116. Reddy CSK, Ghai R, Rashmi et al (2003) Polyhydroxyalkanoates: an overview. Bioresour Technol 87(2):137–146PubMedCrossRefGoogle Scholar
  117. Refstie S, Landsverk T, Ringø E et al (2006) Digestive responses of 1- and 2-year-old Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. Aquaculture 261:269–284CrossRefGoogle Scholar
  118. Rekecki A, Dierckens K, Laureau S et al (2009) Effect of germ-free rearing environment on gut development of larval sea bass (Dicentrarchus labrax L.) Aquaculture 293:8–15CrossRefGoogle Scholar
  119. Rhee KJ, Sethupathi P, Driks A et al (2004) Role of commensal bacteria in development of gut associated lymphoid tissues and preimmune antibody repertoire. J Immunol 172:1118–1124PubMedCrossRefGoogle Scholar
  120. Ringø E, Olsen RE, Gifstad TØ et al (2010) Prebiotics in aquaculture: a review. Aquac Nutr 16:117–136CrossRefGoogle Scholar
  121. Ringø E, Dimitroglou A, Hoseinifar SH, Davies SJ (2014) Prebiotics in finfish: an update. In: Merrifield D, Ringø E (eds) Aquaculture nutrition: gut health, probiotics and prebiotics. Wiley-Blackwell Publishing, Oxford, pp 360–400Google Scholar
  122. Rodriguez-Estrada U, Satoh S, Haga Y et al (2009) Effects of single and combined supplementation of Enterococcus faecalis, mannan oligosaccharide and polyhydroxybutyrate acid on growth performance and immune response of rainbow trout Oncorhynchus mykiss. Aquacult Sci 57:609–617Google Scholar
  123. Ruchin AB (2007) Effect of photoperiod on growth, physiological and hematological indices of juvenile Siberian sturgeon Acipenser baerii. Biol Bull 34:583–589CrossRefGoogle Scholar
  124. Rurangwa E, Delaedt Y, Geraylou Z, et al (2008) Dietary effect of Arabinoxylan Oligosaccharides on zootechnical performance and hindgut microbial fermentation in siberian sturgeon and African Catfish, pp 569–570. Aquaculture Europe, Krakow, PolandGoogle Scholar
  125. Sadati MAY, Pourkazemi M, Shakurian M et al (2011) Effects of daily temperature fluctuations on growth and hematology of juvenile Acipenser baerii. J Appl Ichthyol 27:591–594CrossRefGoogle Scholar
  126. Saha S, Roy RN, Sen KS et al (2006) Characterization of cellulose-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, (tenopharyngodon idella Valenciennes). Aquac Res 37:380–388CrossRefGoogle Scholar
  127. Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172:63–92CrossRefGoogle Scholar
  128. Salma W, Zhou Z, Wang W et al (2011) Histological and bacteriological changes in intestine of beluga (Huso huso) following ex vivo exposure to bacterial strains. Aquaculture 314:24–33CrossRefGoogle Scholar
  129. Sanchez JI, Marzorati M, Grootaert C et al (2009) Arabinoxylan-oligosaccharides (AXOS) affect the protein/carbohydrate fermentation balance and microbial population dynamics of the simulator of human intestinal microbial ecosystem. Microb Biotechnol 2:101–113PubMedCrossRefGoogle Scholar
  130. Scatizzi I (1933) L’organo linfomieloide pericardico dello storione. Archivio Zoologico Italiano 18:1–26Google Scholar
  131. Scharrer E (1944) The histology of the meningeal myeloid tissue in the ganoids Amia and Lepisosteus. Anat Rec 88:291–310CrossRefGoogle Scholar
  132. Schley PD, Field CJ (2002) The immune-enhancing effects of dietary fibres and prebiotics. Br J Nutr 87:221–230CrossRefGoogle Scholar
  133. Shaowua L, Di W, Hongbai L et al (2013) Isolation of Yersinia ruckeri strain H01 from farm-raised amur sturgeon Acipenser schrencki in China. J Aquat Anim Health 25:9–14CrossRefGoogle Scholar
  134. Silverman GJ, Goodyear CS (2002) A model B-cell superantigen and the immunobiology of B lymphocytes. Clin Immunol 102:117–134PubMedCrossRefGoogle Scholar
  135. Siwicki AK (1989a) Immunostimulating influence of levamisole on nonspecific immunity in carp (Cyprinus carpio). Dev Comp Immunol 13:87–91PubMedCrossRefGoogle Scholar
  136. Siwicki AK (1989b) Immunostimulating influence of levamisole on non-specific immunity in carp (Cyprinas carpio). Dev Comp Immunol 13:87–91PubMedCrossRefGoogle Scholar
  137. Skrodenyte-Arbaciauskiene V, Sruoga A, Butkauskas D (2006) Assessment of microbial diversity in the river trout Salmo trutta fario L. intestinal tract identified by partial 16S rRNA gene sequence analysis. Fish Sci 72:597–602CrossRefGoogle Scholar
  138. Skrodenyte-Arbaciauskiene V, Sruoga A, Butkauskas D et al (2008) Phylogenetic analysis of intestinal bacteria of freshwater salmon Salmo salar and sea trout Salmo trutta and diet. Fish Sci 74:1307–1314CrossRefGoogle Scholar
  139. Soltani M, Kalbassi MR (2001) Protection of Persian surgeon (Acipenser persicus) fingerling against Aeromonas hydrophila septicemia using three different antigens. Bull Eur Assoc Fish Pathol 21(6):235–240Google Scholar
  140. Soltani M, Pourkazemi M, Ahmadi MR, Taherimirghead A, Merrifield DL, Masouleh AS (2013) Genetic diversity of lactic acid bacteria in the intestine of Persian sturgeon fingerlings. J Appl Ichthyol 29:494–498CrossRefGoogle Scholar
  141. Spanggaard B, Huber I, Nielsen J et al (2000) The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 182:1–15CrossRefGoogle Scholar
  142. Staykov Y, Spring P, Denev S et al (2007) Effect of a mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquac Int 15:153–161CrossRefGoogle Scholar
  143. Sugita H, Ito Y (2006) Identification of intestinal bacteria from Japanese founder (Paralichthys olivaceus) and their ability to digest chitin. Lett Appl Microbiol 43:336–342PubMedCrossRefGoogle Scholar
  144. Sugita H, Miyajima C, Deguchi Y (1990) The vitamin B12, producing ability of the intestinal bacteria isolated from tilapia and channel cat fish. Nippon Suisan Gakkaishi 56:701CrossRefGoogle Scholar
  145. Sugita H, Matsuo N, Hirose Y et al (1997) Vibrio sp. strain NM 10 with an inhibitory effect against Pasteurella piscicida from the intestine of Japanese coastal fish. Appl Environ Microbiol 63:4986–4989PubMedPubMedCentralGoogle Scholar
  146. Sullam KE, Essinger SD, Lozupone CA et al (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21:3363–3378PubMedCrossRefGoogle Scholar
  147. Syvokiene J (1989) Simbiontnoe Pishchevarenie u Gidrobiontov Inasekomykh (Symbiotic digestion in hydrobionts and insects). Mokslas, VilniusGoogle Scholar
  148. Ta’ati R, Soltani M, Bahmani M et al (2011) Effects of the prebiotics Immunoster and Immunowall on growth performance of juvenile beluga (Huso huso). J Appl Ichthyol 27:796–798CrossRefGoogle Scholar
  149. Timur G, Akayli T, Korun J et al (2010) A study on bacterial haemorrhagic septicemia in farmed young Russian sturgeon in Turkey (Acipencer gueldenstaedtii). Turk J Fish Aquat Sci 25:19–27Google Scholar
  150. Van Cam DT, Hao NV, Dierckens K (2009) Novel approach of using homoserine lactone degrading and poly-β-hydroxybutyrate accumulating bacteria to protect Artemia from the pathogenic effects of Vibrio harveyi. Aquaculture 291:23–30CrossRefGoogle Scholar
  151. Verschuere L, Rombaut G, Sorgeloos P et al (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671PubMedPubMedCentralCrossRefGoogle Scholar
  152. Vuillaume A, Brun R, Chene P et al (1987) First isolation of Yersinia ruckeri from sturgeon, Acipenser baerii Brandt, in south west of France. Bull Eur Assoc Fish Pathol 7:18–19Google Scholar
  153. Wang YB, Li JR, Lin J (2008) Probiotics in aquaculture: challenges and outlook. Aquaculture 281:1–4CrossRefGoogle Scholar
  154. Ward NL, Steven B, Penn K et al (2009) Characterization of the intestinal microbiota of two Antarctic notothenioid fish species. Extremophiles 13(4):679–685PubMedCrossRefGoogle Scholar
  155. Warr GW (1997) The adaptive immune system of fish. Dev Biol Stand 90:15–21PubMedGoogle Scholar
  156. Wei QW, Zou Y, Li P, Li L (2011) Sturgeon aquaculture in China: progress, strategies and prospects assessed on the basis of nation-wide surveys (2007–2009). J Appl Ichthyol 27:162–168CrossRefGoogle Scholar
  157. Williot P, Sabeau L, Gessner J et al (2001) Sturgeon farming in Western Europe: recent developments and perspectives. Aquat Living Resour 14:367–374Google Scholar
  158. Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21(13):3100–3102PubMedPubMedCentralCrossRefGoogle Scholar
  159. Xie Z, Niu C, Zhang Z et al (2006) Dietary ascorbic acid may be necessary for enhancing the immune response in Siberian sturgeon (Acipenser baerii), a species capable of ascorbic acid biosynthesis. Comp Biochem Physiol 145:152–157CrossRefGoogle Scholar
  160. Yazdani Sadati MA, Sayed Hassani MH, Pourkazemi M et al (2014) Influence of different levels of dietary choline on growth rate, body composition, hematological indices and liver lipid of juvenile Siberian sturgeon Acipenser baerii Brandt, 1869. J Appl Ichthyol 30(6):1632–1636CrossRefGoogle Scholar
  161. Ye JD, Wang K, Li FD et al (2011) Single or combined effects of fructo- and mannan oligosaccharide supplements and Bacillus clausii on the growth, feed utilization, body composition, digestive enzyme activity, innate immune response and lipid metabolism of the Japanese flounder Paralichthys olivaceus. Aqua Nutr 17:902–911CrossRefGoogle Scholar
  162. Zapata A, Amemiya CT (2000) Phylogeny of lower vertebrates and their immunological structures. Curr Top Microbiol Immunol 248:67–107PubMedGoogle Scholar
  163. Zapata A, Diez B, Cejalvo T et al (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20(2):126–136PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of MicrobiologyFaculty of ScienceUGentBelgium

Personalised recommendations

Cite chapter