The effect of dietary chitin on the autochthonous gut bacteria of Atlantic cod (Gadus morhua L.)

Aquaculture Research

Volumn 44, Issue 12, 2013, Pages 1889-1900

  Zhou, Zhigang ^a   Karlsen, Ørjan ^b   He, Suxu ^a   Olsen, Rolf Erik ^b   Yao, Bin ^a   Ringø, Einar ^c  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Adherent gut bacteria; Atlantic cod; Chitin; DGGE

Indexed keywords

ARTIFICIAL DIET; BACTERIUM; CHITIN; ELECTROKINESIS; FISH CULTURE; FOOD SUPPLEMENTATION; GADOID; MICROBIAL COMMUNITY; MICROBIOLOGY;

ANAERORHABDUS FURCOSA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GADUS MORHUA; SUIDAE;

EID: 84887154459     PISSN: 1355557X     EISSN: 13652109     Source Type: Journal    
DOI: 10.1111/j.1365-2109.2012.03194.x     Document Type: Article

References (59)

1. Askarian F., Zhou Z., Olsen R.E., Sperstad S. & Ringø E. (2012) Culturable autochthonous gut bacteria in Atlantic salmon (Salmo salar L.) fed diets with or without chitin. Characterization by 16S rRNA gene sequencing, ability to produce enzymes and in vitro growth inhibition of four fish pathogens. Aquaculture 326-329, 1-8.
2. Askarian F., Sperstad S., Merrifield D.L., Ray A.K. & Ringø E. (2012) The effect of different feeding regimes on enzymatic activity of Atlantic cod (Gadus morhua L.) gut microbiota. Aquaculture Research, 1-6. doi: 10.1111/j.1365-2109.2011.03079.x.
3. Bano N., DeRae Smith A., Bennett W., Vasquez L. & Hollibaugh J.T. (2007) Dominance of Mycoplasma in the guts of the long-jawed mudsucker, Gillichthys mirabilis, from five California salt marshes. Environmental Microbiology 9, 2636-2641.
4. Bjornsdottir R., Johannsdottir J., Coe J., Smaradottir H., Agustsson T., Sigurgisladottir S. & Gudmundsdottir B.K. (2009) Survival and quality of halibut larvae (Hippoglossus hippoglossus L.) in intensive farming: possible impact of the intestinal bacterial community. Aquaculture 286, 53-63.
5. Caipang C.M.A., Brinchmann M.F. & Kiron V. (2010) Antagonistic activity of bacterial isolates from intestinal microbiota of Atlantic cod, Gadus morhua, and an investigation of their immunomodulary capabilities. Aquaculture Research 41, 249-256.
6. Danulat E. (1986) Role of bacteria with regard to chitin degradation in the digestive tract of the cod Gadus morhua. Marine Biology 90, 335-343.
7. Danulat E. (1987) Digestibility of chitin in cod, Gadus morhua, in vivo. Helgolander Meeresuntersuch 41, 425-436.
8. Danulat E. & Kausch H. (1984) Chitinase activity in the digestive tract of the cod, Gadus morhua (L.). Journal of Fish Biology 24, 125-133.
9. Dillon R.J., Vennard C.T., Buckling A. & Charnley A.K. (2005) Diversity of locust gut bacteria protects against pathogen invasion. Ecology Letters 8, 1291-1298.
10. Dos Santos J. & Falk-Petersen S. (1989) Feeding ecology of cod (Gadus morhua L.) in Balsfjord and Ullsfjord, northern Norway, 1982-1983. Journal du Conseil International pour l Exploration de la Mer 45, 190-199.
11. Fänge R., Lundblad G. & Lind J. (1976) Lysozyme and chitinase in blood and lymphomyeloid tissues of marine fish. Marine Biology 36, 277-282.
12. Fjellheim A.J., Playfoot K.J., Skjermo J. & Vadstein O. (2007) Vibrionaceae dominates the microflora antagonistic towards Listonella anguillarum in the intestine of cultured Atlantic cod (Gadus morhua L.) larvae. Aquaculture 269, 98-106.
13. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N. & Pace N.R. (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences U.S.A. 104, 13780-13785.
14. Gatesoupe F.-J. (2008) Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotic treatments. Journal of Molecular Microbiology and Biotechnology 14, 107-114.
15. Griffiths R.I., Whiteley A.S., O'Donnel A.G. & Bailey M.J. (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA - and rRNA - based microbial community composition. Applied and Environmental Microbiology 66, 5488-5491.
16. Gutowska M.A., Drazen J.C. & Robinson B.H. (2004) Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comparative Biochemistry and Physiology 139, 351-358.
17. Hagi T., Tanaka D., Iwamura Y. & Hoshino T. (2004) Diversity and seasonal changes in lactic acid bacteria in the intestinal tract of cultured freshwater fish. Aquaculture 234, 335-346.
18. ®) on growth performance, intestinal autochthonous bacterial community and non-specific immunity of hybrid tilapia (Oreochromis niloticus ♀ x O. aureus ♂) cultured in cages. Aquaculture 294, 99-107.
19. He S., Zhou Z., Liu Y., Cao Y., Meng K., Shi P., Yao B. & Ringø E. (2010) Effects of the antibiotic growth promoters flavomycin and florfenicol on the autochthonous intestinal microbiota of hybrid tilapia (Oreochromis niloticus ♀ x O. aureus ♂). Archives in Microbiology 192, 985-994.
20. 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.
21. Jensen S., Frost P. & Torsvik V.L. (2009) The nonrandom microheterogeneity of 16S rRNA genes in Vibrio splendidus may reflect adaptation to versatile lifestyles. FEMS Microbiology Letters 294, 207-215.
22. Kim D., Brunt J. & Austin B. (2007) Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). Journal of Applied Microbiology 102, 1654-1664.
23. Korsnes K., Nicolaisen O., Skar C.K., Nerland A.H. & Bergh Q. (2006) Bacteria in the gut of juvenile cod Gadus morhua fed live feed enriched with four different diets. ICES Journal of Marine Science 63, 296-301.
24. Kuz'mina V.V., Skvortsova E.G., Zolotareva G.V. & Sheptitskiy V.A. (2011) Influence of pH upon the activity of glycosidases and proteinases of intestinal mucosa, chime and microbiota in fish. Fish Physiology and Biochemistry 37, 345-353.
25. Lauzon H.L. & Ringø E. (2011) Prevalence and application of lactic acid bacteria in aquatic environments. In: Lactic Acid Bacteria: Microbiological and Functional Aspects, 4th Edn (ed. by S. Lahtinen, A. Ouwehand, S. Salminen & A. von Wright), pp. 593-632. CRC Press, Taylor and Francis Group, New York.
26. Lauzon H.L., Gudmundsdottir S., Petursdottir S.K., Reynisson E., Steinarsson A., Oddgeirsson M., Bjornsdottir R. & Gudmundsdottir B.K. (2010) Microbiota of Atlantic cod (Gadus morhua L.) rearing systems at pre- and posthatch stages and the effect of different treatments. Journal of Applied Microbiology 109, 1775-1789.
27. LeaMaster B.R., Walsh W.A., Brock J.A. & Fujioka R.S. (1997) Cold stress-induced changes in the aerobic heterotrophic gastrointestinal tract bacterial flora of red hybrid tilapia. Journal of Fish Biology 50, 770-780.
28. Ley R.E., Hamady M., Lozupone C., Turnbaugh P.J., Ramey R.R., Bircher J.S., Schlegel M.L., Tucker T.A., Schrenzel M.D., Knight R. & Gordon J.I. (2008) Evolution of mammals and their gut microbes. Science 320, 1647-1651.
29. Lindsay G.J.H. (1987) Seasonal activities of chitinase and chitobiase in the digestive tract and serum of cod, Gadus morhua (L.). Journal of Fish Biology 30, 495-500.
30. Lindsay G.J.H. & Gooday G.W. (1985) Chitinolytic enzymes and the bacterial microflora in the digestive tract of cod, Gadus morhua. Journal of Fish Biology 26, 255-265.
31. Liu Y., Zhou Z., Yao B., Shi P., He S., Hølvold L.B. & Ringø E. (2008) The effect of intraperitoneal injection of immunostimulatory substances on allochthonous gut microbiota of Atlantic salmon (Salmo salar L.) determined using Denaturing Gradient Gel Electrophoresis (DGGE). Aquaculture Research 39, 635-646.
32. Løvmo Martinsen L., Salma W., Myklebust R., Mayhew T.M. & Ringø E. (2011) Carnobacterium maltaromaticum vs. Vibrio (Listonella) anguillarum in the midgut of Atlantic cod (Gadus morhua L.): an ex vivo study. Aquaculture Research 42, 1830-1839.
33. Michaud L., Giudice A.L., Troussellier M., Smedile F., Bruni V. & Blancheton J.P. (2009) Phylogenetic characterization of the heterotrophic bacterial communities inhabiting a marine recirculating aquaculture system. Journal of Applied Microbiology 107, 1935-1946.
34. Michel C., Pelletier C., Boussaha M., Douet D.G., Lautraite A. & Tailliez P. (2007) Diversity of lactic acid bacteria associated with fish and the fish farm environment, established by amplified rRNA gene restriction analysis. Applied and Environmental Microbiology 73, 2947-2955.
35. Miller D.N., Bryant J.E., Madsen E.L. & Ghirose W.C. (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Applied and Environmental Microbiology 65, 4715-4724.
36. Navarrete P., Espejo R.T. & Romero J. (2009) Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.). Microbial Ecology 57, 550-561.
37. Olsen R.E., Sundell K., Ringø E., Myklebust R., Hemre G.-I., Hansen T. & Karlsen Ø. (2008) The acute stress response in fed and food deprivated Atlantic cod, Gadus morhua L. Aquaculture 280, 232-241.
38. Onarheim A.M., Wiik R., Burghardt J. & Stackebrandt E. (1994) characterization and identification of 2 Vibrio species indigenous to the intestine of fish in cold seawater. Description of Vibrio iliopiscarius. Systematic and Applied Microbiology 17, 370-379.
39. Ray A.K., Ghosh K. & Ringø E. (2012) Enzyme-producing bacteria isolated from fish gut: a review. Aquaculture Nutrition, 1-28. doi: 10.1111/j.1365-2095.2012.00943.x.
40. Ringø E. & Gatesoupe F.-J. (1998) Lactic acid bacteria in fish: a review. Aquaculture 160, 177-203.
41. Ringø E., Sperstad S., Myklebust R., Refstie S. & Krogdahl Å. (2006) Characterisation of the microbiota associated with the intestine of Atlantic cod (Gadus morhua L.). The effect of fish meal, soybean meal and a bioprocessed soybean meal. Aquaculture 261, 829-841.
42. Ringø E., Zhou Z., Olsen R.E. & Song S.K. (2012) Use of chitin and krill in aquaculture - the effect on gut microbiota and the immune system: a review. Aquaculture Nutrition 18, 117-131.
43. Ringø E., Olsen R.E., Gonzalez Vecino J.L., Wadsworth S. & Song S.K. (2012) Use of immunostimulants and nucleotides in aquaculture: a review. Journal of Marine Science Research & Development 2, 104. doi: 10.4172/2155-9910.1000104.
44. Salma W., Zhou Z., Wang W., Askarian F., Kousha A., Ebrahimi M., Myklebust R. & Ringø E. (2011) Histological and bacteriological changes in intestine of beluga (Huso huso) following ex vivo exposure to bacterial strains. Aquaculture 314, 24-33.
45. Sawabe T., Hayashi K., Moriwaki J., Thompson F.L., Swings J., Potin P., Christen R. & Ezura Y. (2004) Vibrio gallicus sp. nov., isolated from the gut of French abalone Haliotis tuberculata. International Journal of Systematic and Evolution Microbiology 54, 843-846.
46. Scharschmidt T.C., List K., Grice E.A., Szabo R., Renaud G., Lee C.C., Wolfsberg T.G., Bugge T.H. & Segre J.A. (2009) Matriptase-deficient mice exhibit ichthyotic skin with a selective shift in skin microbiota. Journal of Investigative Dermatology 129, 2435-2442.
47. Seppola M., Olsen R.E., Sandaker E., Kanapathippillai P., Holzapfel W. & Ringø E. (2006) Random amplification of polymorphic DNA (RAPD) typing of carnobacteria isolated from hindgut chamber and large intestine of Atlantic cod (Gadus morhua L.). Systematic and Applied Microbiology 29, 131-137.
48. Shah H.N. & Collins M.D. (1986) Reclassification of Bacteroides furcosus Veillon and Zuber (hauduroy, Ehringer, Urbain, Guillot and Magrou) in a new genus Anaerorhabdus, as Anaerorhabdus furcosus comb. nov. Systematic and Applied Microbiology 8, 86-88.
49. Shannon C.E. & Weaver W. (1963) The Mathematical Theory of Communication. p. 117. University Illinois press, Urbana.
50. Simpson J.M., McCracken V.J., White B.A., Gaskins H.R. & Mackie R.I. (1999) Application of denaturant gradient gel electrophoresis for the analysis of the porcine gastrointestinal microbiota. Journal of Microbiology Methods 36, 167-179.
51. Smith C.J., Danilowicz B.S. & Meijer W.G. (2007) Characterization of the bacterial community associated with the surface and mucus layer of whiting (Merlangius merlangus). FEMS Microbiology Ecology 62, 90-97.
52. Strøm E. & Olafsen J.A. (1990) The indigenous microflora of wild captured juvenile cod in net pen rearing. In: Microbiology in Poecilotherms (ed. by R. Lesel), pp. 181-185. Elsevier, Amsterdam.
53. Sun H.Y., Deng S.P. & Raun W.R. (2004) Bacterial community structure and diversity in a century - old manure - treated agroecosystem. Applied and Environmental Microbiology 70, 5868-5874.
54. Tharanathan R.N. & Kittur F.S. (2003) Chitin - the undisputed biomolecule of great potential. Critical Reviews in Food Science and Nutrition 43, 61-87.
55. Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R. & Gordon J.I. (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine 1, 6-14.
56. Valerio F., Favilla M., De Bellis P., Sisto A., de Candia S. & Lavermicocca P. (2009) Antifungal activity of strains of lactic acid bacteria isolated from a semolina ecosystem against Penicillium roqueforti, Aspergillus niger and Endomyces fibuliger contaminating bakery products. Systematic and Applied Microbiology 32, 438-448.
57. Ward N.L., Steven B., Penn K., Methe B.A. & Detrich W.H. III (2009) Characterization of the intestinal microbiota of two Antarctic notothenioid fish species. Extremophiles 13, 679-685.
58. Wilson B., Danilowicz B.S. & Meijer W.G. (2008) The diversity of bacterial communities associated with Atlantic cod Gadus morhua. Microbial Ecology 55, 425-434.
59. Zhou Z., Liu Y., Shi P., He S., Yao B. & Ringø E. (2009) Molecular characterization of the autochthonous microbiota in the gastrointestinal tract of adult yellow grouper (Epinephelus awoara) cultured in cages. Aquaculture 286, 184-189.