Title: Lactic acid bacteria vs. pathogens in the gastrointestinal tract of fish: a review
Abstract: Aquaculture ResearchVolume 41, Issue 4 p. 451-467 Lactic acid bacteria vs. pathogens in the gastrointestinal tract of fish: a review Einar Ringø, Einar Ringø Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, Norway Institute of Marine Research, Bergen, NorwaySearch for more papers by this authorLisbeth Løvmo, Lisbeth Løvmo Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, Norway *Present address: Lisbeth Løvmo, Granåsveien 34, 7048 Trondheim, Norway.Search for more papers by this authorMads Kristiansen, Mads Kristiansen Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, NorwaySearch for more papers by this authorYvonne Bakken, Yvonne Bakken Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, Norway †Present address: Yvonne Bakken, Skretting, 8450 Storkmarknes, Norway.Search for more papers by this authorIrene Salinas, Irene Salinas Fish Innate Immune System, Department of Cell Biology, University of Murcia, Murcia, SpainSearch for more papers by this authorReidar Myklebust, Reidar Myklebust Institute of Anatomy and Cell Biology, University of Bergen, Bergen, NorwaySearch for more papers by this authorRolf Erik Olsen, Rolf Erik Olsen Institute of Marine Research, Bergen, NorwaySearch for more papers by this authorTerry M Mayhew, Terry M Mayhew School of Biomedical Sciences, Queen's Medical Centre, University of Nottingham, Nottingham, UKSearch for more papers by this author Einar Ringø, Einar Ringø Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, Norway Institute of Marine Research, Bergen, NorwaySearch for more papers by this authorLisbeth Løvmo, Lisbeth Løvmo Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, Norway *Present address: Lisbeth Løvmo, Granåsveien 34, 7048 Trondheim, Norway.Search for more papers by this authorMads Kristiansen, Mads Kristiansen Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, NorwaySearch for more papers by this authorYvonne Bakken, Yvonne Bakken Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, Tromsø, Norway †Present address: Yvonne Bakken, Skretting, 8450 Storkmarknes, Norway.Search for more papers by this authorIrene Salinas, Irene Salinas Fish Innate Immune System, Department of Cell Biology, University of Murcia, Murcia, SpainSearch for more papers by this authorReidar Myklebust, Reidar Myklebust Institute of Anatomy and Cell Biology, University of Bergen, Bergen, NorwaySearch for more papers by this authorRolf Erik Olsen, Rolf Erik Olsen Institute of Marine Research, Bergen, NorwaySearch for more papers by this authorTerry M Mayhew, Terry M Mayhew School of Biomedical Sciences, Queen's Medical Centre, University of Nottingham, Nottingham, UKSearch for more papers by this author First published: 16 March 2010 https://doi.org/10.1111/j.1365-2109.2009.02339.xCitations: 191 Correspondence: E Ringø, Department of Marine Biotechnology, Norwegian College of Fishery Science, University of Tromsø, N-9037 Tromsø, Norway. E-mail: [email protected] Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract Intensive fish production worldwide has increased the risk of infectious diseases. However, before any infection can be established, pathogens must penetrate the primary barrier. In fish, the three major routes of infection are the skin, gills and gastrointestinal (GI) tract. The GI tract is essentially a muscular tube lined by a mucous membrane of columnar epithelial cells that exhibit a regional variation in structure and function. In the last two decades, our understanding of the endocytosis and translocation of bacteria across this mucosa, and the sorts of cell damage caused by pathogenic bacteria, has increased. Electron microscopy has made a valuable contribution to this knowledge. In the fish-farming industry, severe economic losses are caused by furunculosis (agent, Aeromonas salmonicida spp. salmonicida) and vibriosis [agent, Vibrio (Listonella) anguillarum]. This article provides an overview of the GI tract of fish from an electron microscopical perspective focusing on cellular damage (specific attack on tight junctions and desmosomes) caused by pathogenic bacteria, and interactions between the ‘good’ intestinal bacteria [e.g. lactic acid bacteria (LAB)] and pathogens. Using different in vitro methods, several studies have demonstrated that co-incubation of Atlantic salmon (Salmo salar L.) foregut (proximal intestine) with LAB and pathogens can have beneficial effects, the cell damage caused by the pathogens being prevented, to some extent, by the LAB. However, there is uncertainty over whether or not similar effects are observed in other species such as Atlantic cod (Gadus morhua L.). When discussing cellular damage in the GI tract of fish caused by pathogenic bacteria, several important questions arise including: (1) Do different pathogenic bacteria use different mechanisms to infect the gut? (2) Does the gradual development of the GI tract from larva to adult affect infection? (3) Are there different infection patterns between different fish species? The present article addresses these and other questions. References Andlid T., Vázquez-Juárez R.V. & Gustafsson L. (1995) Yeast colonizing the intestine of rainbow trout (Salmo gairdneri) and turbot (Scophthalmus maximus). Microbial Ecology 30, 321– 334. Austin B. & Austin D.A. (1999) Bacterial Fish Pathogens: Diseases of Farmed and Wild Fish, 3rd edn. Springer – praxis, London, 457pp. Baccazar J.L., Vendrell D., De Blas I., Ruiz-Zarzuela I., Girones O. & Muzquiz J.L. (2007) In vitro competitive adhesion and production of antagonistic compounds by lactic acid bacteria against fish pathogens. Veterinary Microbiology 122, 373– 380. Bakken Y. (2002) Histological studies of pyloric caeca of Atlantic salmon (Salmo salar L.) fed diets containing linseed, soybean, and marine oils. Effects of challenge with Aeromonas salmonicida ssp. salmonicida. MSc thesis, Norwegian College of Fishery Science, University of Tromsø, Norway. Balcazar J.L. (2003) Evaluation of probiotics bacterial strains in Litopenaeus vannamei. Final report, National Center for Marine and Aquaculture Research, Guayaquil, Ecuador. Balcázar J.L., De Blas I., Ruiz-Zarzuela I., Vendrell D. & Muzquiz J.L. (2004) Probiotics: a tool for the future of fish and shellfish health management. Journal of Aquaculture in the Tropics 19, 239– 242. Balcazar J.L., De Blas I., Ruiz-Zarzuela I., Cunningham D., Vendrell D. & Muzquiz J.L. (2006) The role of probiotics in aquaculture. Veterinary Microbiology 114, 173– 186. Balcazar J.L., Decamp O., Vendrell D., De Blas I. & Ruiz-Zarzuela I. (2006) Health and nutritional properties of probiotics in fish and shellfish. Microbial Ecology in Health and Diseases 18, 65– 70. Balcazar J.L., De Blas I., Ruiz-Zarzuela I., Vendrell D., Calvo A.C., Marquez I., Girones O. & Muzquiz J.L. (2007) Changes in intestinal microbiota and humoral immune response following probiotics administration in brown trout (Salmo trutta). British Journal of Nutrition 97, 522– 527. Birkbeck T.H. & Ringø E. (2005) Pathogenesis and the gastrointestinal tract of growing fish. In: Microbial Ecology in Growing Animals (ed. by W. Holzapfel & P. Naughton), pp. 208– 234. Elsevier, Edinburgh, UK. Bowden T.J., Adamson K. & Bricknell I.R. (2003) Diseases of relevance to haddock. In: Early Rearing of Haddock. State of the Art (Special Publication), Vol. 7 (ed. by D.E. Aitkin), pp. 113– 114. Aquaculture Association of Canada, Halifax, Canada. Bricknell I.R., Bron J.E. & Bowden T.J. (2006) Diseases of gadoid fish in cultivation: a review. ICES Journal of Marine Science 63, 253– 266. Bruhn J.B., Dalsgaard I., Nielsen K.F., Buchholtz C., Larsen J.L. & Gram L. (2005) Quorum sensing signal molecules (acylated homoserine lactones) in Gram-negative fish pathogenic bacteria. Diseases of Aquatic Organisms 65, 43– 52. Buchholtz C., Nielsen K.F., Milton D., Larsen J.L. & Gram L. (2006) Profiling of acylated homoserine lactones of Vibrio anguillarum in vitro and in vivo: influence of growth conditions and serotype. Systematic and Applied Microbiology 29, 433– 445. 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. Journal of World Aquaculture Society 36, 425– 436. Cahill M.M. (1990) Bacterial flora of fishes: a review. Microbial Ecology 19, 21– 41. Chabrillon M., Ouwehand A.C., Diaz-Rosales P., Arijo S., Martinez-Manzanares E., Balebona M.C. & Morinigo M.A. (2006) Adhesion of lactic acid bacteria to mucus of farmed gilthead seabream, and interactions with fish pathogenic microorganisms. Bulletin of European Association of Fish Pathology 26, 202– 210. Chabrillon M., Arijo S., Diaz-Rosales P. & Balebona M.C. (2006) Interference of Listonella anguillarum with potential probiotics microorganisms isolated from farmed gilthead seabream (Sparus aurata, L.). Aquaculture Research 37, 78– 86. Chalfie M., Tu Y., Euskirchen G., Ward W.W. & Prasher D.C. (1994) Green fluorescent protein as a marker for gene expression. Science 263, 802– 805. Chopra A.K., Xu X.J., Ribardo D., Gonzalez M., Kuhl K., Peterson J.W. & Houston C.W. (2000) The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infection and Immunology 68, 2808– 2818. Defoirdt T., Boon N., Bossier P. & Verstraete W. (2004) Disruption of bacterial quorum sensing: an unexplored strategy to fight infection in aquaculture. Aquaculture 240, 69– 88. Defoirdt T., Boon N., Sorgeloos P., Verstraete W. & Bossier P. (2008) Quorum sensing and quorum quenching in Vibrio harveyi: lessons learned from in vivo work. Mini review. The ISME Journal 2, 19– 26. Direkbusarakom S., Yoshimizu M., Ezura Y., Ruangpan L. & Danayadol Y. (1998) Vibrio spp. the dominant flora in shrimp hatchery against some fish pathogenic viruses. Journal of Marine Biotechnology 6, 266– 267. Egidius E. (1987) Vibriosis: pathogenicity and pathology. A review. Aquaculture 67, 15– 28. Farzanfar A. (2006) The use of probiotics in shrimp aquaculture. FEMS Immunology and Medical Microbiology 48, 149– 158. Fasano A. (2002) Toxins and the gut: role in human disease. Gut 50, 9– 14. Fivaz M. & Van Der Goot F.G. (1999) The tip of a molecular syringe. Trends in Microbiology 7, 341– 343. Fuller R. (1973) Ecological studies of lactobacillus flora associated with the crop epithelium of the fowl. Journal of Applied Bacteriology 36, 131– 139. Fung W.Y., Woo Y.P, Wan-Abdullah W.N., Ahmad R., Easa A.M. & Liong M.T. (2009) Benefits of probiotics: beyond gastrointestinal health. Milchwissenschaft Milk Science International 64, 17– 21. Gatesoupe F.J. (1999) The use of probiotics in aquaculture. Aquaculture 180, 147– 165. Gatesoupe F.J. (2007) Live yeast in the gut: natural occurrence, dietary introduction, and their effects on fish health and development. Aquaculture 267, 20– 30. Gatesoupe F.J. (2008) Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotics treatments. Journal of Molecular Microbiology and Biotechnology 14, 107– 114. Gildberg A. & Mikkelsen H. (1998) Effects of supplementing the feed to Atlantic cod (Gadus morhua) fry with lactic acid bacteria and immuno-stimulating peptides during a challenge trial with Vibrio anguillarum. Aquaculture 167, 103– 113. Girones R., Jofre J.T. & Bosch A. (1989) Isolation of marine bacteria with antiviral properties. Canadian Journal of Microbiology 35, 1015– 1021. Gomez G.D. & Balcazar J.L. (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology 52, 145– 154. Gomez-Gil B., Roque A. & Turnbull J.F. (2000) The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture 191, 259– 270. Gram L. & Ringø E. (2005) Prospects of fish probiotics. In: Microbial Ecology in Growing Animals (ed. by W. Holzapfel & P. Naughton), pp. 379– 417. Elsevier, Edinburgh, UK. Griffith S., Melville K., Cook M., Vincent S., St Pierre M. & Lanteigne C. (2001) Profiling of bacterial species associated with haddock larviculture by PCR amplification of 16S rDNA and denaturing gradient gel electrophoresis. Journal of Aquatic Animal Health 13, 355– 363. Groff J. & LaPatra S. (2000) Infectious diseases impacting the commercial culture of salmonids. Journal of Applied Aquaculture 10, 17– 90. Gullian M. & Rodríguez J. (2002) Immunostimulant qualities of probiotic bacteria. Global Aquaculture Advocate 5, 52– 54. 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. Harikrishnan R. & Balasundaram C. (2005) Modern trends in Aeromonas hydrophila disease management with fish. Reviews in Fisheries Science 13, 281– 320. Holben W.E., Särkilahti L.K., Williams P., Saarinen M. & Apajalahti J.H.A. (2002) Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microbial Ecology 44, 175– 185. Hong H.A., Duc L.H. & Cutting S.M. (2005) The use of bacterial spore formers as probiotics. FEMS Microbiology Reviews 29, 813– 835. 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. Irianto A. & Austin B. (2002a) Probiotics in aquaculture. Journal of Fish Diseases 25, 633– 642. Irianto A. & Austin B. (2002b) Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 25, 333– 342. Irianto A., Roberwen P.A.W., Austin B. & Pandalai S.G. (2000) The use of probiotics in aquaculture. Recent Research Developments in Microbiology 4, 557– 567. Jacobsen C.N., Rosenfelt Nielsen V., Hayford A.E., Møller P.L., Michaelsen K.F., Paerregaard A., Sandström B., Tvede M. & Jakobsen M. (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Applied and Environmental Microbiology 65, 4949– 4956. Jensen S., Øvreås L., Bergh Ø. & Torsvik V. (2004) Phylogenetic analysis of bacterial communities associated with larvae of the Atlantic halibut propose succession from a uniform normal flora. Systematic and Applied Microbiology 27, 728– 736. Jutfelt F., Olsen R.E., Glette J., Ringø E. & Sundell K. (2006) Translocation of viable Aeromonas salmonicida across the intestine of rainbow trout. Journal of Fish Diseases 29, 255– 262. Kamei Y., Yoshimizu M., Ezura Y. & Kimura T. (1988) Screening of bacteria with antiviral activity from fresh water salmonid hatcheries. Microbiology and Immunology 32, 67– 73. Karunasagar I. & Karunasagar I. (1999) Diagnosis, treatment and prevention of microbial diseases of fish and shellfish. Current Science 76, 387– 399. Kesarcodi-Watson A., Kaspar H., Lategan M.J. & Gibson L. (2008) Probiotics in aquaculture. The need, principles and mechanisms of action and screening processes. Aquaculture 274, 1– 14. 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. Knudsen G., Sørum H., McLPress C. & Olafsen J.A. (1999) In situ adherence of Vibrio spp. to cryosections of Atlantic salmon, Salmo salar L., tissue. Journal of Fish Diseases 22, 409– 418. Krogdahl Å., Bakke-Mckellep A.M., Rød K.H. & Bæverfjord G. (2000) Feeding Atlantic salmon, Salmo salar L., soybean products: effect on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquaculture Nutrition 6, 77– 84. Lødemel J.B., Mayhew T.M., Myklebust R., Olsen R.E., Espelid S. & Ringø E. (2001) Effect of three dietary oils on disease susceptibility in Arctic charr (Salvelinus alpinus L.) during cohabitant challenge with Aeromonas salmonicida ssp. salmonicida. Aquaculture Research 32, 935– 945. Løvmo L. (2007a) In vitro eksponering av torsketarm. Histologiske forandringer som følge av Carnobacterium divergens og Vibrio anguilllarum. Project thesis (in Norwegian), University of Tromsø, Norway, p. 55. Løvmo L. (2007b) In vitro eksponering av torsketarm. Histologiske og bakteriologiske forandringer som følge av Carnobacterium maltaromaticum og Vibrio anguilllarum. Master thesis (in Norwegian), p. 56. Ling S.H.M., Xie L., Lim T.M. & Leung K.Y. (2000) Use of green fluorescent protein (GFP) to track the invasion pathways of Edwardsiella tarda in in vivo and in vitro fish models. Microbiology 146, 7– 19. Liu Y., Zhou Z., Yao B., Shi P., He S., Benjamisen Hølvold L. & 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. Lun S. & Willson P.J. (2004) Expression of green fluorescent protein and its application in pathogenesis studies of serotype 2 Streptococcus suis. Journal of Microbiological Methods 56, 401– 412. Mackie T.J., Arkwright J.A., Pyrce-Tannatt T.E., Mottram J.C., Johnston W.D. & Menzies W.J. (1930) Interim Report of the Furunculosis Committee. HMSO, Edinburgh, UK. Madigan M.T., Martinko J.M. & Parker J. (2000) Brock. Biology of Microorganisms, 9th edn. Prentice Hall International, Upper Saddle River, NJ, USA. Mayhew T.M., Myklebust R., Whybrow A. & Jenkins R. (1999) Epithelial integrity, cell death and cell loss in mammalian small intestine. Histology and Histopathology 14, 257– 267. Mäyrä-Mäkinen A., Manninen M. & Gyllenberg H. (1983) The adherence of lactic acid bacteria to columnar epithelial cells of pigs and calves. Journal of Applied Bacteriology 55, 241– 245. Medellina-Pena M.J., Wang H., Johnson R., Anand S. & Griffiths M.W. (2007) Probiotics affect virulence-related gene expression in Escherichia coli O157:H7. Applied and Environmental Microbiology 73, 4259– 4267. 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. Moriarty D. (1997) The role of microorganisms in aquaculture ponds. Aquaculture 151, 333– 349. Namba A., Mano N. & Hirose H. (2007) Phylogenetic analysis of intestinal bacteria and their adhesive capability in relation to the intestinal mucus of carp. Journal of Applied Microbiology 102, 1307– 1317. Nikoskelainen S., Salminen S., Bylund G. & Ouwehand A. (2001) Characterization of the properties of human and dairy-derived probiotics for prevention of infectious diseases in fish. Applied and Environmental Microbiology 67, 2430– 2435. Norwegian Scientific Committee for Food Safety (2009) Criteria for Safe Use of Plant Ingredients in Diets for Aquacultured Fish. ISBN 978-82-8082-299-4. Norwegian Scientific Committee for Food Safety, Oslo, Norway. Olafsen J.A. (2001) Interactions between fish larvae and bacteria in marine aquaculture. Aquaculture 200, 223– 247. Olivier G. (1997) Getting to know your enemy. In: Furunculosis. Multidisciplinary Fish Disease Research (ed. by E.-M. Bernoth, A.E. Ellis, P.J. Midtlyng, G. Olivier & P. Smith), pp. 233– 234. Academic, San Diego, CA, USA. Olsen R.E., Myklebust R., Ringø E. & Mayhew T.M. (2000) The influence of dietary linseed oil and saturated fatty acids on caecal enterocytes in Arctic charr (Salvelinus alpinus L.): a quantitative ultrastructural study. Fish Physiology and Biochemistry 22, 207– 216. O'Toole R., Hofsten J.V., Rosqvist R., Olsson P.E. & Wolf-Watz H. (2004) Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum. Microbial Pathogenesis 37, 41– 46. Pedersen A. & Dalsgaard A. (2003) Antimicrobial resistance of intestinal Aeromonas spp. and Enterococcus spp. in fish cultured in integrated broiler-fish farms in Thailand. Aquaculture 219, 71– 82. Picchietti S., Mazzini M., Taddei A.R., Renna R., Fausto A.M., Mulero V., Carnevali O., Cresci A. & Abelli L. (2007) Effects of administration of probiotic strains on GALT of larval gilthead seabream: immunohistochemical and ultrastructural studies. Fish and Shellfish Immunology 22, 57– 67. Pond M.J., Stone D.M. & Alderman D.J. (2006) Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Aquaculture 261, 193– 203. Press C.M. & Lillehaug A. (1995) Vaccination in European salmonid aquaculture: a review of practices and prospects. British Veterinary Journal 151, 45– 69. Prieur G., Nicolas J.L., Plusquellec A. & Vigneulle M. (1990) Interactions between bivalves molluscs and bacteria in the marine environment. Oceanographic Marine Biology Annual Reviews 28, 227– 352. Rengpipat S., Rukpratanporn S., Piyatiratitivorakul S. & Menasaveta P. (2000) Immunity enhancement in black tiger shrimp (Penaeus monodon) by a probiont bacterium (Bacillus S11). Aquaculture 191, 271– 288. Ringø E. (2002) Probiotics in aquaculture. In: Disease Control in Fish and Shrimp Aquaculture in South Asia – Diagnosis and Husbandry Techniques (ed. by Y. Inui & E.R. Cruz-Lacierda), pp. 107– 135. South Asian Fisheries Development Centre, Iloilo, Philippines. Ringø E. (2004) Lactic acid bacteria in fish and fish farming. In: Lactic Acid Bacteria (ed. by S. Salminen, A. Ouwehand & A. Von Wrigth), pp. 581– 610. Marcel Dekker, New York, NY, USA. Ringø E. (2008) The ability of carnobacteria isolated from fish intestine to inhibit growth of fish pathogenic bacteria: a screening study. Aquaculture Research 39, 171– 180. Ringø E. & Birkbeck T.H. (1999) Intestinal microflora of fish larvae and fry. Aquaculture Research 30, 73– 93. Ringø E. & Gatesoupe F.J. (1998) Lactic acid bacteria in fish: a review. Aquaculture 160, 177– 203. Ringø E. & Olsen R.E. (1999) The effect of diet on aerobic bacterial flora associated with intestine of Arctic charr (Salvelinus alpinus L.). Journal of Applied Microbiology 86, 22– 28. Ringø E., Strøm E. & Tabachek J.-A. (1995) Intestinal microflora of salmonids: a review. Aquaculture Research 26, 773– 789. Ringø E., Olsen R.E., Øverli Ø. & Løvik F. (1997) Effect of dominance hierarchy formation on aerobic microbiota associated with epithelial mucosa of subordinate and dominant individuals of Arctic charr, Salvelinus alpinus (L.). Aquaculture Research 28, 901– 904. Ringø E., Sepploa M., Berg A., Olsen R.E., Schillinger U. & Holzapfel W. (2002) Characterization of Carnobacterium divergens strain 6251 isolated from intestine of Arctic charr (Salvelinus alpinus L.). Systematic and Applied Microbiology 25, 120– 129. Ringø E., Olsen R.E., Mayhew T.M. & Myklebust R. (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture 227, 395– 415. Ringø E., Jutfelt F., Kanapathippillai P., Bakken Y., Sundell K., Glette J., Mayhew T.M., Myklebust R. & Olsen R.E. (2004) Damaging effect of the fish pathogen Aeromonas salmonicida ssp. salmonicida on intestinal enterocytes of Atlantic salmon (Salmo salar L.). Cell and Tissue Research 318, 305– 311. Ringø E., Schillinger U. & Holzapfel W. (2005) Antibacterial abilities of lactic acid bacteria isolated from aquatic animals and the use of lactic acid bacteria in aquaculture. In: Microbial Ecology in Growing Animals (ed. by W. Holzapfel & P. Naughton), pp. 418– 453. Elsevier, Edinburgh, UK. Ringø E., Mikkelsen H., Kaino T., Olsen R.E., Mayhew T.M. & Myklebust R. (2006) Endocytosis of indegenous bacteria and cell damage caused by Vibrio anguillarum in the foregut and hindgut of spotted wolffish (Anarhichas minor Olafsen) fry. An electron microscopical study. Aquaculture Research 37, 647– 651. Ringø E., Salinas I., Olsen R.E., Nyhaug A., Myklebust R. & Mayhew T.M. (2007) Histological changes in Atlantic salmon (Salmo salar L.) intestine following in vitro exposure to pathogenic and probiotic bacterial strains. Cell and Tissue Research 328, 109– 116. 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. Rinkinen M.E., Westermarck S., Salminen A.C. & Ouwehand A.C. (2003) Absence of host specificity for in vitro adhesion of probiotic lactic acid bacteria to intestinal mucus. Veterinary Microbiology 9, 55– 61. Robertson P.A.W., O'Dowd C., Burrels C., Williams P. & Austin B. (2000) Use of Carnobacterium sp. as a probiont for Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss, Walbaum). Aquaculture 185, 235– 243. Sakata T. (1990) Microflora in the digestive tract of fish and shell-fish. In: Microbiology in Poecilotherms (ed. by R. Lesel), pp. 171– 176. Elsevier, Amsterdam, the Netherlands. Salinas I., Cuesta A., Esteban M.A. & Meseguer J. (2005) Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish and Shellfish Immunology 19, 67– 77. Salinas I., Myklebust R., Esteban M.A., Olsen R.E., Meseguer J. & Ringø E. (2008) In vitro studies of Lactobacillus delbrueckii subsp. lactis in Atlantic salmon (Salmo salar L.) foregut: tissue responses and evidence of protection against Aeromonas salmonicida subsp. salmonicida epithelial damage. Veterinary Microbiology 128, 167– 177. Salminen S., Deighton M.A., Benno Y. & Gorbach S.L. (1998) Lactic acid bacteria in health and disease. In: Lactic Acid Bacteria. Microbiology and Functional Aspects (ed. by S. Salmonen & A. Von Wright), pp. 221– 253. Marcel Dekker, New York, NY, USA. Samuelsen O.B., Nerland A.H., Jørgensen T., Schrøder M.B., Svåsand T. & Bergh Ø. (2006) Viral and bacterial diseases of Atlantic cod Gadus morhua, their prophylaxis and treatment: a review. Diseases of Aquatic Organisms 71, 239– 254. Santos Y., Pazos F., Bandin I. & Toranzo A.E. (1995) Analysis of antigens present in the extracellular products and cell-surface of Vibrio anguillarum serotypes O1, O2, and O3. Applied and Environmental Microbiology 61, 2493– 2498. Scholz U., Garcia-Diaz G., Ricque D., Cruz-Suarez L.E., Vargas-Albores F. & Latchford J. (1999) Enhancement of vibriosis resistance in juvenile Penaeus vannamei by supplementation of diets with different yeast products. Aquaculture 176, 271– 283. Seppola M., Olsen R.E., Sandaker E., Kanapathippillai P., Holzapfel W. & Ringø E. (2006) Random amplified polymorphic DNA (RAPD) polymerase chain reaction analysis of carnobacteria isolated from hindgut chamber and large intestine of Atlantic cod (Gadus morhua L.). Systematic and Applied Microbiology 29, 131– 137. Skirpstunas R.T. & Baldwin T.J. (2002) Edwardsiella ictaluri invasion of IEC-6, Henle 407, fathead minnow and channel catfish enteric epithelial cells. Diseases of Aquatic Organism 51, 161– 167. Skjermo J. & Vadstein O. (1999) Techniques for microbial control in the intensive rearing of marine larvae. Aquaculture 177, 333– 343. Tinh N.T.N., Dierckens K., Sorgeloos P. & Bossier P. (2008) A review of the functionality of probiotics in the larviculture food chain. Marine Biotechnology 10, 1– 12. Toranzo A.E., Mamarinos B. & Romalde J.E. (2005) A review of the main bacterial fish diseases in mariculture systems. Aquaculture 246, 37– 61. Valdivia R.H., Hromockyj A.E., Monack D., Ramakrishnan L. & Falkow S. (1996) Applications for green fluorescent protein (GFP) in the study of host–pathogen interactions. Gene 173, 47– 52. Van der Marel M., Schroers V., Neuhaus H. & Steinhagen D. (2008) Chemotaxis towards, adhesion to, and growth in carp gut mucus of two Aeromonas hydrophila strains with different pathogenicity for common carp, Cyprinus carpio L. Journal of Fish Diseases 31, 321– 330. Vanderpool C., Yan F. & Polk D.B. (2008) Mechanisms of probiotics action: implication for therapeutic applications in inflammatory bowel diseases. Inflammatory Bowel Diseases 14, 1585– 1596. Verschuere L., Rombaut G., Sorgeloos P. & Verstraete W. (2000) Probiotic bacteria as biological control against in aquaculture. Microbiology Molecular Biology Reviews 64, 655– 671. Vine N.G., Leukes W.D. & Kaiser H. (2004) In vitro growth characteristics of five candidate aquaculture probiotics and two fish pathogens grown in fish intestinal mucus. FEMS Microbiological Letters 231, 145– 152. Vine N.G., Leukes W.D., Kaiser H., Baya S. & Baxter J. (2004) Competition of attachment of aquaculture probiotic and pathogenic bacteria to fish intestinal mucus. Journal of Fish Diseases 27, 319– 326. Vine N.G., Leukes W.D. & Kaiser H. (2006) Probiotics in marine larviculture. FEMS Microbiology Reviews 30, 404– 427. Weiss N., Schillinger U. & Kansdler O. (1983) Lactobacillus lactis, Lactobacillus leichmannii and Lactobacillus bulgaricus, subjective synonyms of Lactobacillus delbrueckii, and description of Lactobacillus delbrueckii subsp. lactis comb. nov. and Lactobacillus delbrueckii subsp. bulgaricus comb. nov. Systematic and Applied Microbiology 4, 552– 557. Yin J.F., Zhou X.Y., Li J.Q., Li Y.H., Hou H.L. & Zhang W.H. (2007) A study on the survival dynamics of Bacillus subtilis in water using green fluorescent protein labelling. Chinese Journal of Analytical Chemistry 35, 1405– 1409. Ying C., Lei W., Jiazhong L., Zhantao S. & Liguo A. (2007) Identification and purification of a novel adhesion-associated protein in a new strain of Lactobacillus, L 15, from flounder (Paralichthys olivaceus). Veterinary Microbiology 122, 116– 122. Zhou Z., Liu Y., Shi P., He S., Yao B. & Ringø E. (2009) Molecular characterization of the autochthonous microbiota in the gastrointestinal tract of yellow grouper (Epinephelus awoara) cultured in cages. Aquaculture 286, 184– 189. Citing Literature Volume41, Issue4March 2010Pages 451-467 ReferencesRelatedInformation