Journal of Applied & Environmental Microbiology
ISSN (Print): 2373-6747 ISSN (Online): 2373-6712 Website: Editor-in-chief: Sankar Narayan Sinha
Open Access
Journal Browser
Journal of Applied & Environmental Microbiology. 2014, 2(6), 287-293
DOI: 10.12691/jaem-2-6-4
Open AccessArticle

The Impact of Diet on the Gut Microbiota of Tasmanian Atlantic Salmon (Salmo Salar L.) Using a Semi-Continuous Fermenter Model

Neuman C1, Hatje E1, Stevenson H1, Smullen R2, Bowman JP3 and Katouli M1,

1Genecology Research Centre, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Maroochydore DC, Queensland

2Ridley AquaFeed Pty, Narangba, Queensland

3Tasmanian Institute of Agriculture, University of Tasmania, Hobart, Tasmania, Australia

Pub. Date: November 19, 2014

Cite this paper:
Neuman C, Hatje E, Stevenson H, Smullen R, Bowman JP and Katouli M. The Impact of Diet on the Gut Microbiota of Tasmanian Atlantic Salmon (Salmo Salar L.) Using a Semi-Continuous Fermenter Model. Journal of Applied & Environmental Microbiology. 2014; 2(6):287-293. doi: 10.12691/jaem-2-6-4


Farmed Tasmanian Atlantic salmon in Australia may experience water temperatures as high as 20°C during summer, which may impact on health and mariculture productivity. In this study we investigated the impact of two commercial feed on the major bacterial population in the gut of Atlantic salmon using an anaerobic semi-continuous fermenter model set at 20°C. Fermentation was conducted in a 5L culture vessel with 100 rpm agitation under CO2. For each diet the hindgut contents of three farmed Tasmanian Atlantic salmon were collected, mixed and used as fermenter inocula. Samples were collected at day 0, 1, 6 and 12 and used for bacterial enumeration and measurement of the functional status of the gut microbiota as well as their metabolic capacity (MC) values. With diet A, Vibrio spp. and lactic acid bacteria (LAB) increased over the course of fermentation. In contrast, diet B did not support the growth of LAB and instead promoted the growth of Plesiomonasshigelloides. MC values of gut microbiota receiving either diet also increased over the course of fermentation, reaching the highest level on day 12. This was independent of the type of diet used as the functional status of the microbiota for both diets was highly similar at each sampling round. Our results indicate that at the temperature experienced by Tasmanian Atlantic salmon during warm season i.e. 20°C, the type of diet may select for the growth of specific species of bacteria.

gut microbiota fermenter semi-continuous diet Atlantic salmon

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit


[1]  Apajalahti, J., Kettunen, A. and Graham, H., “Characteristics of the gastrointestinal microbial communities with special reference to the chicken” World’s Poultry Science Journal, 60. 223-232. Jun. 2004.
[2]  Olafsen, J.A., “Interactions between fish larvae and bacteria in marine aquaculture” Aquaculture, 200. 223-247. Aug. 2001.
[3]  Ringø, E., Stone, D.M. and Alderman, D.J., “Intestinal microflora of salmonids, a review”, Aquaculture Research, 26. 773-789. Oct. 1995.
[4]  Ringø, E., Myklebust, R., Mayhew, T.M. and Olsen, R.E., “The effect of dietary inulin on aerobic bacteria associated with hindgut of Arctic charr (Salvelinusalpinus L.)”, Aquaculture Research, 37. 891-897. Jun. 2006.
[5]  Trust, T.J., Bull, L.M., Currie, B.R. and Buckley, J.T., “Obligate anaerobic bacteria in the gastrointestinal microflora of the Grass carp (Ctenopharyngodon idella), Goldfish (Carassius auratus), and Rainbow trout (Salmo gairdneri)”, Journal of Fish Research Board Canada, 36. 1174-1179. 1979.
[6]  Holben, W.E., Williams, P., Gilbert, M.A., Saarinen, M., Sarkilahti, L.K. and Apajalahti, J.H., “Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon”, Microbial Ecology, 44. 175-185. Jun. 2002.
[7]  Hovda, M.B., Fontanillas, R., McGurk, C., Obach, A. and Rosnes, J.T., “Seasonal variations in the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.)”, Aquaculture Research, 43. 154-159. Feb. 2012.
[8]  Huber, I., Spanggaard, B., Appel, K.F., Rossen, L., Nielsen, T. and Gram, L., “Phylogenetic analysis and in situ identification of the intestinal microbial community of rainbow trout (Oncorhynchus mykiss, Walbaum)”, Journal of Applied Microbiology, 96. 117-132. Jan. 2004.
[9]  Pond, M.J., Stone, D.M. and Alderman, D.J., “Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout (Oncorhynchus mykiss)”, Aquaculture, 261. 194-203. Nov. 2006.
[10]  Spanggaard, B., Huber, I., Nielsen, J., Nielsen, T., Appel, K.F. and Gram, L., “The microflora of rainbow trout intestine: a comparison of traditional and molecular identification”, Aquaculture, 182. 1-15. Feb. 2000.
[11]  Hartviksen, M., Vecino, J.L.G., Ringø, E., Bakke, A.-M., Wadsworth, S., Krogdahl, Å., Ruohonen, K. and Kettunen, A., “Alternative dietary protein sources for Atlantic salmon (Salmo salar L.) effect on intestinal microbiota, intestinal and liver histology and growth”, Aquaculture Nutrition, 20 (1). Jan. 2014.
[12]  Heikkinen, J., Vielma, J., Kemiläinen, O., Tiirola, M., Eskelinen, P., Kiuru, T., Navia-Paldanius, D. and von Wright, A., “Effects of soybean meal based diet on growth performance, gut histopathology and intestinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss)”, Aquaculture, 261. 259-268. Jul. 2006.
[13]  Ingerslev, H.-C., von Gersdorff, J.L., Strube, M., Larsen, L.N., Dalsgaard, I., Boye, M. and Madsen, L. 2014. The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type, Aquaculture. 424. 24-34. Jan. 2014.
[14]  14. Desai, A.R., Links, M.G., Collins, S.A., Mansfield, G.S., Drew, M.D., Van Kessel, A.G. and Hill, J.E. 2012. Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture. 350. 134-142. 2012.
[15]  Neuman, C., Hatje, E., Zarkasi, K. Z., Smullen, R., Bowman, J.P., and Katouli, M., “The effect of diet and environmental temperature on the faecal microbiota of farmed Tasmanian Atlantic Salmon (Salmo salar L.)”, Jul. 2014. [early view]
[16]  Gibson, G.R. and Fuller, R., “Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use”, Journal of Nutrition, 130. 391S-395S. Feb. 2000.
[17]  Clarke, R.J. and Bauchop, T. (Eds.), Microbial ecology of the gut, Academic Press, London, 1997, 1-333.
[18]  Mäkivuokko, H., Forssten, S., Saarinen, M., Ouwehand, A. and Rautonen, N., “Symbiotic effects of lactitol and Lactobacillus acidophilus NCFM™ in a semi-continuous colon fermentation model”, Beneficial Microbes, 1 (2). 131-137. Jun. 2010.
[19]  Zhou, Z., Cao, X. and Zhou, J.Y., “Effect of resistant starch structure on short‐chain fatty acids production by human gut microbiota fermentation in vitro”, StarchStärke, 65. 509-516. Jan.2013.
[20]  De Preter, V., Hamer, H.M., Windey, K. and Verbeke, K., “The impact of pre‐and/or probiotics on human colonic metabolism: Does it affect human health?” Molecular Nutrition and Food Research, 55 (1). 46-57. Jan. 2011.
[21]  Miśta, D., Króliczewska, B., Zawadzki, W., Pecka, E., Steininger, M., Hull, S., Zuk, M. and Szopa, J., “The effect of Linola and W92/72 transgenic flax seeds on the rabbit caecal fermentation-in vitro study”, Polish Journal of Veterinary Science, 14 (4). 557-564. Dec. 2011.
[22]  Soto, E.C., Yáñez-Ruiz, D.R., Cantalapiedra-Hijar, G., Vivas, A. and Molina-Alcaide, E., “Changes in ruminal microbiota due to rumen content processing and incubation in single-flow continuous-culture fermenters”, Animal Production Science, 52 (9). 813-822. July. 2012.
[23]  Zarkasi, K.Z., Abell, G.C.J., Taylor, R.S., Neuman, C., Hatje, E., Tamplin, M.L., Katouli, M. and Bowman, J.P., “Pyrosequencing-based characterization of gastrointestinal bacteria of Atlantic salmon (Salmo salar L.) within a commercial mariculture system”, Journal of Applied Microbiology, 117. 18-27. Jul. 2014.
[24]  Zihler, A., Gagnon, M., Chassard, C., Hegland, A., Stevens, M.J.A., Braegger, C.P. and Lacroix, C., “Unexpected consequences of administering bacteriocinogenic probiotic strains for Salmonella populations, revealed by an in vitro colonic model of the child gut”, Microbiology, 156. 3342-3353. Nov. 2010.
[25]  Zampa, A., Silvia, S., Fabianib, R., Morozzib, G., Orpianesia, C. and Cresci, A., “Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture”, Anaerobe, 10. 19-26. Feb. 2004.
[26]  Usher, M.L., Talbot, C. and Eddy, F.B., “Drinking in Atlantic salmon smolts transferred to seawater and the relationship between drinking and feeding”, Aquaculture 73 (1-4), 237-246. Oct. 1988.
[27]  Mandel, A.D., Wright, K. and McKinnon, J.M., “Selective medium for isolation of Mima and Herellea organisms”, Journal of Bacteriology, 68. 1524-1525. Nov. 1964.
[28]  Katouli, M., Lund, A., Wallgren, P., Kuhn, I., Soderlind, O. and Mollby, R., “Metabolic fingerprinting and fermentative capacity of the intestinal flora of pigs during pre- and post-weaning periods”, Journal of Applied Microbiology, 83. 147-154. Aug. 1997.
[29]  Katouli, M., Foo, E.L., Kühn, I.and Möllby, R., “Evaluation of the PhP generalized microplate for measuring fermentative capacity and for fingerprinting of the intestinal microflora”, Journal of Applied Microbiology, 82.511-518. 1997.
[30]  Sneath, P.H.A. and Sokal, R.R., Numerical taxonomy: the Principles and Practice of Numerical Classification, WH Freeman, San Francisco, 1973.
[31]  Katouli, M., Erhardt-Bennet, A.S., Kuhn, I., Kollberg, B. and Mollby, R., “Metabolic capacity and pathogenic properties of the intestinal coliforms in patients with ulcerative colitis”, Microbial Ecology, Health and Disease, 5. 245-255. Jun. 1992.
[32]  Ringø, E. and Olsen, R.E., “The effect of diet on aerobic bacterial flora associated with intestine of Artic charr (Salvelinus alpinus L.)”, Journal of Applied Microbiology, 86. 22-28. Jan. 1999.
[33]  Navarrete, P., Magne, F., Arcaneda, C., Fuentes, P., Barros, L., Opazo, R., Espejo, R. and Romero, J., “PCR-TTGE analysis of 16S rRNA from Rainbow Trout (Oncorhynchus mykiss) gut microbiota reveals host-specific communities of active bacteria”. Plos one, 7(2), February 2012. [Online]. Available: [Acessed Apr. 15, 2014].
[34]  Navarrete, P., Fuentes, P., De la Fuente, L., Barros, L., Magne, F., Opazo, R., Ibacache, C., Espejo, R. and Romero, J., “Short-term effects of dietary soybean meal and lactic acid bacteria on the intestinal morphology and microbiota of Atlantic salmon (Salmo salar)”, Aquaculture Nutrition, 19. 827-836. Jun. 2013.
[35]  Cinquin, C., Le Blay, G., Fliss, I. and Lacroix, C., “Immobilization of infant fecal microbiota and utilization in an in vitro colonic fermentation model”, Microbial Ecology, 48(1). 128-138. Jul. 2004
[36]  Macfarlane, G.T., Macfarlane, S. and Gibson, G.R., “Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon”, Microbial Ecology, 35 (2). 180-187. Mar. 1998.
[37]  Sghir, A., Chow, J.M. and Mackie, R.I., “Continuous culture selection of Bifidobacteria and Lactobacilli from human faecal samples using fructooligosaccharide as selective substrate”, Journal of Applied Microbiology, 85 (4). 769-777. Oct. 1998.
[38]  De Boever, P., Wouters, R., Vermeirssen, V., Boon, N. and Verstraete, W., “Development of a six-stage culture system for simulating the gastrointestinal microbiota of weaned infants”, Microbial Ecology in Health and Disease, 13 (2). 111-123. 2001.
[39]  Rajilic-Stojanovic, M., Maathuis, A., Heilig, H.G.H.J., Venema, K., De Vos, W.M. and Smidt, H., “Evaluating the microbial diversity of an in vitro model of the human large intestine by phylogenetic microarray analysis”, Microbiology, 156 (11). 3270-3281. Nov. 2010.
[40]  Payne, A.N., Zihler, A., Chassard, C. and Lacroix, C., “Advances and perspectives in in vitro human gut fermentation modelling”, Trends in Biotechnology, 30 (1). 17-25. Jan. 2012.