Dietary β-glucan (MacroGard®) enhances survival of first feeding turbot (Scophthalmus maximus) larvae by altering immunity, metabolism and microbiota

Fish and Shellfish Immunology

Volumn 48, Issue , 2016, Pages 94-104

  Miest, Joanna J ^a   Arndt, Carmen ^a   Adamek, Mikolaj ^b   Steinhagen, Dieter ^b   Reusch, Thorsten B H ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Beta glucan; Complement component C3; Fish larvae; Immunity; Immunostimulation; Survival; Trypsin; Turbot

Indexed keywords

BACTERIAL DNA; BETA GLUCAN; CHYMOTRYPSIN; COMPLEMENT COMPONENT C3; FISH PROTEIN; HEAT SHOCK PROTEIN 70; IMMUNOLOGIC FACTOR; INTERLEUKIN 1BETA; TRYPSIN; TUMOR NECROSIS FACTOR;

AEROMONAS; ANIMAL; ARTEMIA; DIET; DIETARY SUPPLEMENT; DRUG EFFECTS; FLATFISH; FLAVOBACTERIACEAE; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LIPID METABOLISM; METABOLISM; MICROBIOLOGY; MICROFLORA; ROTIFERA; VIBRIO;

AEROMONAS; ANIMALS; ARTEMIA; BETA-GLUCANS; CHYMOTRYPSIN; COMPLEMENT C3; DIET; DIETARY SUPPLEMENTS; DNA, BACTERIAL; FISH PROTEINS; FLATFISHES; FLAVOBACTERIACEAE; GENE EXPRESSION; HSP70 HEAT-SHOCK PROTEINS; IMMUNOLOGIC FACTORS; INTERLEUKIN-1BETA; LIPID METABOLISM; MICROBIOTA; ROTIFERA; TRYPSIN; TUMOR NECROSIS FACTOR-ALPHA; VIBRIO;

EID: 84949591190     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2015.11.013     Document Type: Article

References (74)

1. Food, Agriculture Organization of the United N.FISHSTAT Global Aquaculture Production 2014, FAO, Rome, Italy.
2. Vadstein O., Bergh O., Gatesoupe F.J., Galindo-Villegas J., Mulero V., Picchietti S., et al. Microbiology and immunology of fish larvae. Rev. Aquac. 2013, 5:S1-S25.
3. Padrós F., Minkoff G., Sala R., Crespo S. Histopathological events throughout the development of turbot (Scophthalmus maximus L.) larvae. J. Comp. Pathol. 1993, 109:321-334.
4. Magnadóttir B. Innate immunity of fish (overview). Fish Shellfish Immunol. 2006, 20:137-151.
5. Zapata A.G., Chibá A., Varas A. Cells and tissues of the immune system of fish. The Fish Immune System: Organism, Pathogen, and Environment 1997, 1-62. Academic Press. G.K. Iwama, T. Nakanishi (Eds.).
6. Magnadóttir B., Lange S., Gudmundsdottir S., Bøgwald J., Dalmo R. Ontogeny of humoral immune parameters in fish. Fish Shellfish Immunol. 2005, 19:429-439.
7. Magnadottir B., Lange S., Steinarsson A., Gudmundsdottir S. The ontogenic development of innate immune parameters of cod (Gadus morhua L.). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2004, 139:217-224.
8. Vadstein O. The use of immunostimulation in marine larviculture: possibilities and challenges. Aquaculture 1997, 155:401-417.
9. Bricknell I., Dalmo R.A. The use of immunostimulants in fish larval aquaculture. Fish Shellfish Immunol. 2005, 19:457-472.
10. Vetvicka V., Vannucci L., Sima P. The effects of β-glucan on fish immunity. North Am. J. Med. Sci. 2013, 5:580.
11. Sych G., Frost P., Irnazarow I. Influence of β-glucan (MacroGard®) on innate immunity of carp fry. Bull. Vet. Inst. Pulawy 2013, 57:219-223.
12. Skjermo J., Størseth T.R., Hansen K., Handå A., Øie G. Evaluation of β-(1→3, 1→6)-glucans and high-M alginate used as immunostimulatory dietary supplement during first feeding and weaning of Atlantic cod (Gadus morhua L.). Aquaculture 2006, 261:1088-1101.
13. Dalmo R.A., Kjerstad A.A., Arnesen S.M., Tobias P.S., Bogwald J. Bath exposure of Atlantic halibut (Hippoglossus hippoglossus L.) yolk sac larvae to bacterial lipopolysaccharide (LPS): absorption and distribution of the LPS and effect on fish survival. Fish Shellfish Immunol. 2000, 10:107-128.
14. Magnadottir B., Gudmundsdottir B.K., Lange S., Steinarsson A., Oddgeirsson M., Bowden T., et al. Immunostimulation of larvae and juveniles of cod, Gadus morhua L. J. Fish Dis. 2006, 29:147-155.
15. Al-Gharabally H., Al-Marzouk A., Azad I.S. Role of beta-glucans and levamisole on the enhancement of the survival rate, immune response and disease resistance of blue-fin porgy Sparidentax hasta (Sobaity) larvae. Res. J. Biotechnol. 2013, 8:18-23.
16. Ghaedi G., Keyvanshokooh S., Mohammadi Azarm H., Akhlaghi M. Effects of dietary β-glucan on maternal immunity and fry quality of rainbow trout (Oncorhynchus mykiss). Aquaculture 2015, 441:78-83.
17. Robles R., Sorgeloos P., Van Duffel H., Nelis H. Progress in biomedication using live foods. J. Appl. Ichthyol. Z Angew. Ichthyol. 1998, 14:207-212.
18. Soltanian S., Stuyven E., Cox E., Sorgeloos P., Bossier P. Beta-glucans as immunostimulant in vertebrates and invertebrates. Crit. Rev. Microbiol. 2009, 35:109-138.
19. Ringø E., Olsen R.E., Vecino J.L.G., Wadsworth S., Song S.K. Use of immunostimulants and nucleotides in aquaculture: a review. J. Mar. Sci. Res. Dev. 2012, 2.
20. Huang H.B., Ostroff G.R., Lee C.K., Agarwal S., Ram S., Rice P.A., et al. Relative contributions of dectin-1 and complement to immune responses to particulate β-glucans. J. Immunol. 2012, 189:312-317.
21. Pietretti D., Vera-Jimenez N.I., Hoole D., Wiegertjes G.F. Oxidative burst and nitric oxide responses in carp macrophages induced by zymosan, MacroGard® and selective dectin-1 agonists suggest recognition by multiple pattern recognition receptors. Fish Shellfish Immunol. 2013, 35:847-857.
22. Vadstein O., Bergh Ø., Gatesoupe F.J., Galindo-Villegas J., Mulero V., Picchietti S., et al. Microbiology and immunology of fish larvae. Rev. Aquac. 2013, 5:S1-S25.
23. Skjermo J., Salvesen I., Øie G., Olsen Y., Vadstein O. Microbially matured water: a technique for selection of a non-opportunistic bacterial flora in water that may improve performance of marine larvae. Aquac. Int. 1997, 5:13-28.
24. Andrews S.R., Sahu N.P., Pal A.K., Mukherjee S.C., Kumar S. Yeast extract, brewer's yeast and spirulina in diets for Labeo rohita fingerlings affect haemato-immunological responses and survival following Aeromonas hydrophila challenge. Res. Vet. Sci. 2011, 91:103-109.
25. Hashimoto T., Ohno N., Adachi Y., Yadomae T. Enhanced production of inducible nitric oxide synthase by β-glucans in mice. FEMS Immunol. Med. Microbiol. 1997, 19:131-135.
26. Vetvicka V., Vashishta A., Saraswat-Ohri S., Vetvickova J. Immunological effects of yeast- and mushroom-derived β-glucans. J. Med. Food 2008, 11:615-622.
27. Falco A., Frost P., Miest J., Pionnier N., Irnazarow I., Hoole D. Reduced inflammatory response to Aeromonas salmonicida infection in common carp (Cyprinus carpio L.) fed with β-glucan supplements. Fish Shellfish Immunol. 2012, 32:1051-1057.
28. Miest J.J., Falco A., Pionnier N.P.M., Frost P., Irnazarow I., Williams G.T., et al. The influence of dietary β-glucan, PAMP exposure and Aeromonas salmonicida on apoptosis modulation in common carp (Cyprinus carpio). Fish Shellfish Immunol. 2012, 33:846-856.
29. Vera-Jimenez N.I., Pierretti D., Wiegertjes G.F., Nielsen M.E. Comparative study of beta-glucan induced respiratory burst measured by nitroblue tetrazolium assay and real-time luminol-enhanced chemiluminescence assay in common carp (Cyprinus carpio L.). Fish Shellfish Immunol. 2013, 34:1216-1222.
30. Vera-Jimenez N.J., Nielsen M.E. Carp head kidney leukocytes display different patterns of oxygen radical production after stimulation with PAMPs and DAMPs. Mol. Immunol. 2013, 55:231-236.
31. Pionnier N., Falco A., Miest J., Frost P., Irnazarow I., Shrive A., et al. Dietary β-glucan stimulate complement and C-reactive protein acute phase responses in common carp (Cyprinus carpio) during an Aeromonas salmonicida infection. Fish Shellfish Immunol. 2013, 34:819-831.
32. Pionnier N., Falco A., Miest J.J., Shrive A.K., Hoole D. Feeding common carp Cyprinus carpio with β-glucan supplemented diet stimulates C-reactive protein and complement immune acute phase responses following PAMPs injection. Fish Shellfish Immunol. 2014, 39:285-295.
33. Kühlwein H., Merrifield D.L., Rawling M.D., Foey A.D., Davies S.J. Effects of dietary beta-(1,3)(1,6)-D-glucan supplementation on growth performance, intestinal morphology and haemato-immunological profile of mirror carp (Cyprinus carpio L.). J. Anim. Physiol. Anim. Nutr. 2014, 98:279-289.
34. Ogier de Baulny M., Quentel C., Fournier V., Lamour F., Le Gouvello R. Effect of long-term oral administration of β-glucan as an immunostimulant or an adjuvant on some non-specific parameters of the immune response of turbot Scophthalmus maximus. Dis. Aquat. Org. 1996, 26:139-147.
35. Vadstein O., Oie G., Olsen Y. Particle size dependent feeding by the rotifer Brachionus plicatilis. Rotifer Symposium VI 1993, 261-267. Springer.
36. Chicharo M.A., Chicharo L. RNA:DNA ratio and other nucleic acid derived indices in marine ecology. Int. J. Mol. Sci. 2008, 9:1453-1471.
37. Malzahn A., Clemmesen C., Rosenthal H. Temperature effects on growth and nucleic acids in laboratory-reared larval coregonid fish. Mar. Ecol. Prog. Ser. 2003, 259:285-293.
38. Houde E.D., Schekter R.C. Growth Rates, Rations and Cohort Consumption of Marine Fish Larvae in Relation to Prey Concentrations 1981.
39. Ueberschär B. The use of tryptic enzyme activity measurement as a nutritional condition index: laboratory calibration data and field application. ICES Marine Science Symposia 1995, 119-129. ICES.
40. Hermann B.T., Reusch T.B.H., Hanel R. Effects of dietary purified rapeseed protein concentrate on hepatic gene expression in juvenile turbot (Psetta maxima). Aquac. Nutr. 2015, 10.1111/anu.12251.
41. Pereiro P., Figueras A., Novoa B. A novel hepcidin-like in turbot (Scophthalmus maximus L.) highly expressed after pathogen challenge but not after iron overload. Fish Shellfish Immunol. 2012, 32:879-889.
42. -δδCT method. Methods 2001, 25:402-408.
43. Jung-Schroers V., Adamek M., Jung A., Harris S., Dóza Ö.-S., Baumer A., et al. Feeding of β-1,3/1,6-glucan increases the diversity of the intestinal microflora of carp (Cyprinus carpio). Aquac. Nutr. 2015, 10.1111/anu.12320.
44. Muyzer G., de Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59:695-700.
45. Steinum T., Sjastad K., Falk K., Kvellestad A., Colquhoun D.J. An RT PCR-DGGE survey of gill-associated bacteria in Norwegian seawater-reared Atlantic salmon suffering proliferative gill inflammation. Aquaculture 2009, 293:172-179.
46. Sambrook J., Russel D. Molecular Cloning: a Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York City, NY, USA.
47. Garcia-Vallve S., Palau J., Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol. Biol. Evol. 1999, 16:1125-1134.
48. Adamek M., Syakuri H., Harris S., Rakus K.Ł., Brogden G., Matras M., et al. Cyprinid herpesvirus 3 infection disrupts the skin barrier of common carp (Cyprinus carpio L.). Vet. Microbiol. 2013, 162:456-470.
49. R Development Core Team R: a Language and Environment for Statistical Computing 2010, R Foundation for Statistical Computing, Vienna, Austria.
50. Rich J.T., Neely J.G., Paniello R.C., Voelker C.C.J., Nussenbaum B., Wang E.W. A practical guide to understanding Kaplan-Meier curves. Otolaryngol. Head Neck Surg. 2010, 143:331-336.
51. Daniels H.V., Watanabe W.O. Practical Flatfish Culture and Stock Enhancement 2011, : Wiley Online Library.
52. Anderson J.T. A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J. Northwest Atl. Fish. Sci. 1988, 8:55-66.
53. Yoo G., Lee S., Kim Y.C., Okorie O.E., Park G.J., Han Y.O., et al. Effects of dietary β-1,3 glucan and feed stimulants in juvenile olive flounder, Paralichthys olivaceus. J. World Aquac. Soc. 2007, 38:138-145.
54. Fuchs V.I., Schmidt J., Slater M.J., Zentek J., Buck B.H., Steinhagen D. The effect of supplementation with polysaccharides, nucleotides, acidifiers and Bacillus strains in fish meal and soy bean based diets on growth performance in juvenile turbot (Scophthalmus maximus). Aquaculture 2015, 437:243-251.
55. Li J., Li D.F., Xing J.J., Cheng Z.B., Lai C.H. Effects of β-glucan extracted from Saccharomyces cerevisiae on growth performance, and immunological and somatotropic responses of pigs challenged with Escherichia coli lipopolysaccharide. J. Animal Sci. 2006, 84:2374-2381.
56. Wang Z., Guo Y., Yuan J., Zhang B. Effect of dietary β-1,3/1,6-glucan supplementation on growth performance, immune response and plasma prostaglandin E-2, growth hormone and ghrelin in weanling piglets. Asian-Australasian J. Anim. Sci. 2008, 21:707-714.
57. Lamari F., Castex M., Larcher T., Ledevin M., Mazurais D., Bakhrouf A., et al. Comparison of the effects of the dietary addition of two lactic acid bacteria on the development and conformation of sea bass larvae, Dicentrarchus labrax, and the influence on associated microbiota. Aquaculture 2013, 376-379:137-145.
58. Guzman-Villanueva L.T., Ascencio-Valle F., Macias-Rodriguez M.E., Tovar-Ramirez D. Effects of dietary β-1,3/1,6-glucan on the antioxidant and digestive enzyme activities of Pacific red snapper (Lutjanus peru) after exposure to lipopolysaccharides. Fish Physiol. Biochem. 2014, 40:827-837.
59. Ronnestad I., Kamisaka Y., Conceicao L.E.C., Morais S., Tonheim S.K. Digestive physiology of marine fish larvae: hormonal control and processing capacity for proteins, peptides and amino acids. Aquaculture 2007, 268:82-97.
60. Kim Y-s, Ke F., Zhang Q.-Y. Effect of β-glucan on activity of antioxidant enzymes and Mx gene expression in virus infected grass carp. Fish Shellfish Immunol. 2009, 27:336-340.
61. Peters L.D., Livingstone D.R. Antioxidant enzyme activities in embryologic and early larval stages of turbot. J. Fish Biol. 1996, 49:986-997.
62. Padrós F., Crespo S. Ontogeny of the lymphoid organs in the turbot Scophthalmus maximus: a light and electron microscope study. Aquaculture 1996, 144:1-16.
63. Falco A., Miest J.J., Pionnier N., Pietretti D., Forlenza M., Wiegertjes G.F., et al. β-Glucan-supplemented diets increase poly(I: C)-induced gene expression of Mx, possibly via Tlr3-mediated recognition mechanism in common carp (Cyprinus carpio). Fish Shellfish Immunol. 2014, 36:494-502.
64. Chettri J.K., Kania P.W., Buchmann K. Immunomodulation of rainbow trout (Oncorhynchus mykiss) fry by bath exposure to β-glucan from Euglena gracilis. Aquac. Res. 2013, 44:1407-1415.
65. Rawls J.F., Samuel B.S., Gordon J.I. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4596-4601.
66. Zanuzzo F., Urbinati E., Nash G., Gamperl A. Steelhead trout Oncorhynchus mykiss metabolic rate is affected by dietary Aloe vera inclusion but not by mounting an immune response against formalin-killed Aeromonas salmonicida. J. Fish Biol. 2015, 87:43-53.
67. Jung K.H., Kim M.-J., Ha E., Kim H.K., Kim Y.O., Kang S.A., et al. The suppressive effect of β-glucan on the production of tumor necrosis factor-alpha in BV2 microglial cells. Biosci. Biotechnol. Biochem. 2007, 71:1360-1364.
68. Biswas G., Korenaga H., Takayama H., Kono T., Shimokawa H., Sakai M. Cytokine responses in the common carp, Cyprinus carpio L. treated with baker's yeast extract. Aquaculture 2012, 356-57:169-175.
69. Zhang Z., Swain T., Bøgwald J., Dalmo Ra, Kumari J. Bath immunostimulation of rainbow trout (Oncorhynchus mykiss) fry induces enhancement of inflammatory cytokine transcripts, while repeated bath induce no changes. Fish Shellfish Immunol. 2009, 26:677-684.
70. Bagni M., Romano N., Finoia M.G., Abelli L., Scapigliati G., Tiscar P.G., et al. Short- and long-term effects of a dietary yeast β-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax). Fish Shellfish Immunol. 2005, 18:311-325.
71. Tanaka K., Tanaka Y., Suzuki T., Mizushima T. Protective effect of β-(1,3→1,6)-D-glucan against irritant-induced gastric lesions. Br. J. Nutr. 2011, 106:475-485.
72. Kühlwein H., Emery M.J., Rawling M.D., Harper G.M., Merrifield D.L., Davies S.J. Effects of a dietary beta-(1,3)(1,6)-D-glucan supplementation on intestinal microbial communities and intestinal ultrastructure of mirror carp (Cyprinus carpio L.). J. Appl. Microbiol. 2013, 115:1091-1106.
73. Marques A., Dhont J., Sorgeloos P., Bossier P. Immunostimulatory nature of β-glucans and Baker's yeast in gnotobiotic Artemia challenge tests. Fish Shellfish Immunol. 2006, 20:682-692.
74. Soltanian S. Protection of Gnotobiotic Artemia against Vibrio campbellii Using Baker's Yeast Strains and Extracts 2007, Ghent University.