Gut microbiota changes in rainbow trout, Oncorhynchus mykiss (Walbaum), during organic acid feed supplementation and Yersinia ruckeri infection

Journal of Fish Diseases

Volumn 36, Issue 6, 2013, Pages 599-606

  Jaafar, R M ^a   Kania, P W ^a   Larsen, A H ^b   Nielsen, D S ^c   Fouz, B ^d   Browdy, C ^e   Buchmann, K ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b BioMar Group   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF VALENCIA   (Spain)

^e NOVUS INTERNATIONAL INC   (United States)

Author keywords

Denaturing gradient gel electrophoresis; Gut microbiota; Rainbow trout; Yersinia ruckeri

Indexed keywords

ANIMAL; ANIMAL DISEASE; ARTICLE; DIET SUPPLEMENTATION; FISH DISEASE; GASTROINTESTINAL TRACT; MICROBIOLOGY; MICROFLORA; RAINBOW TROUT; YERSINIA; YERSINIA INFECTION;

ANIMALS; DIETARY SUPPLEMENTS; FISH DISEASES; GASTROINTESTINAL TRACT; MICROBIOTA; ONCORHYNCHUS MYKISS; YERSINIA; YERSINIA INFECTIONS;

ONCORHYNCHUS MYKISS; YERSINIA RUCKERI;

EID: 84877707563     PISSN: 01407775     EISSN: 13652761     Source Type: Journal    
DOI: 10.1111/jfd.12047     Document Type: Article

References (54)

1. Ai Q., Mai K., Zhang L., Tan B. & Zhang W. (2007) Effects of dietary β-1, 3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish & Shellfish Immunology 22, 394-402.
2. Austin B. (2006) The bacterial microflora of fish, revised. The Scientific World Journal 6, 934-945.
3. Bagni M., Romano N., Finoia M.G., Abelli L. & Scapigliati G. (2005) 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 Immunology 18, 311-325.
4. Bakke-McKellep A.M., Penn M.H., Salas P.M., Refstie S., Sperstad S., Landsverk T., Ringø E. & Krogdahl Å. (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). British Journal of Nutrition 97, 699-713.
5. Balcázar J.L., Blas I.D., Ruiz-Zarzuela I., Vendrell D., Calvo A.C., Márquez I., Gironés O. & Muzquiz J.L. (2007) Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). British Journal of Nutrition 97, 522-527.
6. Bates J.M., Mittge E., Kuhlman J., Baden K.N., Cheesman S. & Guillemin K. (2006) Distinct signals from the microbiota promote different aspects of zebra fish gut differentiation. Developmental Biology 297, 374-386.
7. Biziulevicius G.A. (2004) Nutrition discussion forum. British Journal of Nutrition 92, 1009-1012.
8. Broom L.J., Miller H.M., Kerr K.G. & Knapp J.S. (2006) Effects of zinc oxide and Enterococcus faecium SF68 dietary supplementation on the performance, intestinal microbiota and immune status of weaned piglets. Research in Veterinary Science 80, 45-54.
9. Chettri J.K., Holten-Andersen L., Raida M.K., Kania P.W. & Buchmann K. (2011) PAMP induced expression of immune relevant genes in head kidney leukocytes of rainbow trout (Oncorhynchus mykiss). Developmental and Comparative Immunology 35, 476-482.
10. Deshmukh S., Raida M.K., Dalsgaard I., Chettri J.K., Kania P.W. & Buchmann K. (2012) Comparative protection of two different commercial vaccines against Yersinia ruckeri serotype O1 and biotype 2 in rainbow trout (Oncorhynchus mykiss). Veterinary Immunology & Immunopathology 145, 379-385.
11. Dimitroglou A., Merrifield D.L., Moate R., Davies S.J., Spring P., Sweetman J. & Bradley G. (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Animal Science 87, 3226-3234.
12. Eckburg P.B., Bik E.M., Bernstein C.N., Purdom E., Dethlefsen L., Sargent M., Gill S.R., Nelson K.E. & Relman D.A. (2005) Diversity of the human intestinal microbial flora. Science 308, 1635-1638.
13. Engstad R.E., Robertsen B. & Frivold E. (1992) Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish & Shellfish Immunology 2, 287-297.
14. Fernández L., Méndez J. & Guijarro J.M. (2007) Molecular virulence mechanisms of the fish pathogen Yersinia ruckeri. Veterinary Microbiology 125, 1-10.
15. Fouz B., Zarza C. & Amaro C. (2006) First description of non-motile Yersinia ruckeri serovar I strains causing diseases in rainbow trout, Oncorhynchus mykiss (Waldbaum), cultured in Spain. Journal of Fish Diseases 29, 339-346.
16. Fry J. (2000) Bacterial diversity and unculturables. Microbiology Today 27, 186-188.
17. Fujiwara R., Watanabe J. & Sonoyama K. (2008) Assessing changes in composition of intestinal microbiota in neonatal BALB/c mice through cluster analysis of molecular markers. British Journal of Nutrition 99, 1174-1177.
18. Fushuku S. & Fukuda K. (2008) Gender differences in the composition of faecal flora in laboratory mice, as detected by denaturing gradient gel electrophoresis (DGGE). Experimental Animals 57, 489-493.
19. Gómez G.D. & Balcázar J.L. (2007) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology & Medical Microbiology 52, 145-154.
20. González C.J., López-Diáz T.M., García-López M.L., Prieto M. & Otero A. (1999) Bacterial microflora of wild brown trout (Salmo trutta), wild pike (Esox lucius), and aquacultured rainbow trout (Oncorhynchus mykiss). Journal of Food Protection 62, 1270-1277.
21. Gunal M., Yayli G., Kaya O., Karahan N. & Sulak O. (2006) The effect of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. International Journal of Poultry Science 5, 149-155.
22. Hovda M.B., Lunestad B.T., Fontanillas R. & Rosnes J.T. (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 272, 581-588.
23. Huber I., Spanggaard B., Appel K.F., Rossen L., Nielsen T. & Gram L. (2004) Phylogenetic analysis and in situ identification of the intestinal microbial community of rainbow trout (Oncorhynchus mykiss, Walbaum). Journal of Applied Microbiology 96, 117-132.
24. Hufeldt M.R., Nielsen D.S., Vogensen F.K., Midtvedt T. & Hansen A.K. (2010a) Family relationship of female breeders reduce the systematic inter-individual variation in the gut microbiota of inbred laboratory mice. Laboratory Animals 44, 283-289.
25. Hufeldt M.R., Nielsen D.S., Vogensen F.K., Midtvedt T. & Hansen A.K. (2010b) Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comparative Medicine 60, 336-342.
26. Ispir U. & Dorucu M. (2010) Effect of immersion booster vaccination with Yersinia ruckeri extracellular products (ECP) on rainbow trout Oncorhynchus mykiss. International Aquatic Research 2, 127-130.
27. Jeney G., Galeotti M., Volpatti D. & Anderson D.P. (1997) Prevention of stress in rainbow trout (Oncorhynchus mykiss) fed diets containing different doses of glucan. Aquaculture 154, 1-15.
28. Kim D. & Austin B. (2006) Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish & Shellfish Immunology 21, 513-524.
29. Kim D.H., Brunt J. & Austin B. (2007) Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). Journal of Applied Microbiology 102, 1654-1664.
30. Ley R.E., Peterson D.A. & Gordon J.I. (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837-848.
31. Licht T.R., Hansen M., Poulsen M. & Dragsted L.O. (2006) Dietary carbohydrate source influences molecular fingerprints of the rat faecal microbiota. Bio Medicine Central Microbiology 6, 98.
32. Liu Y., Zhou Z., Yao B., Shi P., He S., Hølvold L.B. & Ringø E. (2008) Effect of intraperitoneal injection of immunostimulatory substances on allochthonous gut microbiota of Atlantic salmon (Salmo salar L.) determined using denaturing gradient gel electrophoresis. Aquaculture Research 39, 635-646.
33. Macpherson A.J. & Harris N.L. (2004) Interactions between commensal intestinal bacteria and the immune system. Nature Reviews Immunology 4, 478-485.
34. Matsuyama H., Mangindaan R.E.P. & Yano T. (1992) Protective effect of schizophyllan and scleroglucan against Streptococcus sp. infection in yellowtail (Seriola quinqueradiata). Aquaculture 101, 197-203.
35. Merrifield D.L., Dimitroglou A., Bradley G., Baker R.T.M. & Davies S.J. (2009) Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 32, 755-766.
36. Misra C.K., Das B.K., Pradhan J., Pattnaik P. & Sethi S. (2004) Changes in lysosomal enzyme activity and protection against Vibrio infection in Macrobrachium rosenbergii (De Man) post larvae after bath immunostimulation with β-glucan. Fish & Shellfish Immunology 17, 389-395.
37. Misra C.K., Das B.K., Mukherjee S.C. & Pattnaik P. (2006) Effect of long term administration of dietary β-glucan on immunity, growth and survival of Labeo rohita fingerlings. Aquaculture 255, 82-94.
38. Navarre O. & Halver J.E. (1989) Disease resistance and humoral antibody production in rainbow trout fed high levels of vitamin C. Aquaculture 79, 207-221.
39. Nicholson J.K., Holmes E. & Wilson I.D. (2005) Gut microorganisms, mammalian metabolism and personalized health care. Nature Reviews Microbiology 3, 431-438.
40. Ortuño J., Cuesta A., Esteban M.A. & Meseguer J. (2001) Effect of oral administration of high vitamin C and E dosages on the gilthead seabream (Sparus aurata L.) innate immune system. Veterinary Immunology and Immunopathology 79, 167-180.
41. Paulsen S.M., Lunde H., Engstad R.E. & Robertsen B. (2003) In vivo effects of β-glucan and LPS on regulation of lysozyme activity and mRNA expression in Atlantic salmon (Salmo salar L.). Fish & Shellfish Immunology 14, 39-54.
42. Ringø E., Myklebust R., Mayhew T.M. & Olsen R.E. (2007) Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268, 251-264.
43. Samuel M., Lam T.J. & Sin Y.M. (1996) Effect of Laminaran [β(1, 3)-D-Glucan] on the protective immunity of blue gourami, Trichogaster trichopterus against Aeromonas hydrophila. Fish & Shellfish Immunology 6, 443-454.
44. Savage D.C. (1977) Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology 31, 107-133.
45. Selvaraj V., Sampath K. & Sekar V. (2005) Administration of yeast glucan enhances survival and some non-specific and specific immune parameters in carp (Cyprinus carpio) infected with Aeromonas hydrophila. Fish & Shellfish Immunology 19, 293-306.
46. Siwicki A.K., Anderson D.P. & Rumsey G.L. (1994) Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Veterinary Immunology & Immunopathology 41, 125-139.
47. Skov J., Kania P.W., Holten-Andersen L., Fouz B. & Buchmann K. (2012) Immunomodulatory effects of dietary β-1, 3-glucan from Euglena gracilis in rainbow trout (Oncorhynchus mykiss) immersion vaccinated against Yersinia ruckeri. Fish & Shellfish Immunology 33, 111-120.
48. Spanggaard B., Huber I., Nielsen J., Nielsen T., Appel K.F. & Gram L. (2000) The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 182, 1-15.
49. Sugita H., Tanaka K., Yoshinami M. & Deguchi Y. (1995) Distribution of Aeromonas species in the intestinal tracts of river fish. Applied & Environmental Microbiology 61, 4128.
50. Tobback E., Decostere A., Hermans K., Haesebrouck F. & Chiers K. (2007) Yersinia ruckeri infections in salmonid fish. Journal of Fish Diseases 30, 257-268.
51. Torrecillas S., Makol A., Caballero M.J., Montero D., Dhanasiri A.K.S., Sweetman J. & Izquierdo M. (2012) Effects of mortality and stress response in European sea bass, Dicentrarchus labrax (L.), fed mannan oligosaccharides (MOS) after Vibrio anguillarum exposure. Journal of Fish Diseases 35, 591-602.
52. Xu J., Bjursell M.K., Himrod J., Deng S., Carmichael L.K., Chiang H.C., Hooper L.V. & Gordon J.I. (2003) A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299, 2074-2076.
53. Xueqin J., Kania P.W. & Buchmann K. (2012) Comparative effects of four feed types on white spot disease susceptibility and skin immune parameters in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 35, 127-135.
54. Yano T., Mangindaan R.E.P. & Matsuyama H. (1989) Enhancement of the resistance of carp Cyprinus carpio to experimental Edwardsiella tarda infection, by some β-1, 3-glucans. Bulletin of the Japanese Society of Scientific Fisheries 55, 1815-1819.