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Analysis of bacterial community shifts in the gastrointestinal tract of pigs fed diets supplemented with β-glucan from Laminaria digitata, Laminaria hyperborea and Saccharomyces cerevisiae

Published online by Cambridge University Press:  28 February 2013

P. Murphy ,
F. Dal Bello ,
J. O'Doherty ,
E. K. Arendt ,
T. Sweeney  and
A. Coffey
P. Murphy
Affiliation:
Department of Biological Sciences, Cork Institute of Technology, Bishopstown, Cork, Ireland
F. Dal Bello
Affiliation:
Department of Food and Nutritional Sciences, University College Cork, Cork, Ireland
J. O'Doherty
Affiliation:
School of Agriculture and Food Science, University College Dublin, Lyons Research farm, Newcastle, Co Dublin, Ireland
E. K. Arendt
Affiliation:
Department of Food and Nutritional Sciences, University College Cork, Cork, Ireland
T. Sweeney
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
A. Coffey*
Affiliation:
Department of Biological Sciences, Cork Institute of Technology, Bishopstown, Cork, Ireland
*
†E-mail: [email protected]
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Abstract

This study was designed to evaluate the effects of algal and yeast β-glucans on the porcine gastrointestinal microbiota, specifically the community of Lactobacillus, Bifidobacterium and coliforms. A total of 48 pigs were fed four diets over a 28-day period to determine the effect that each had on these communities. The control diet consisted of wheat and soya bean meal. The remaining three diets contained wheat and soya bean meal supplemented with β-glucan at 250 g/tonne from Laminaria digitata, Laminaria hyperborea or Saccharomyces cerevisiae. Faecal samples were collected from animals before feeding each diet and after the feeding period. The animals were slaughtered the following day and samples were collected from the stomach, ileum, caecum, proximal colon and distal colon. Alterations in Lactobacillus in the gastrointestinal tract (GIT) were analysed using denaturing gradient gel electrophoresis (DGGE) profiles generated by group-specific 16S rRNA gene PCR amplicons. Plate count analysis was also performed to quantify total coliforms. DGGE profiles indicated that all β-glucan diets provoked the emergence of a richer community of Lactobacillus. The richest community of lactobacilli emerged after feeding L. digitata (LD β-glucan). Plate count analysis revealed that the L. hyperborea (LH β-glucan) diet had a statistically significant effect on the coliform counts in the proximal colon in comparison with the control diet. β-glucan from L. digitata and S. cerevisiae also generally reduced coliforms but to a lesser extent. Nevertheless, the β-glucan diets did not significantly reduce levels of Lactobacillus or Bifidobacterium. DGGE analysis of GIT samples indicated that the three β-glucan diets generally promoted the establishment of a more varied range of Lactobacillus species in the caecum, proximal and distal colon. The LH β-glucan had the most profound reducing effect on coliform counts when compared with the control diet and diets supplemented with L. digitata and S. cerevisiae β-glucans.

Keywords

β-glucanspigsalgaeyeastdenaturing gradient gel electrophoresis
Type
Nutrition
Information
animal , Volume 7 , Issue 7 , July 2013 , pp. 1079 - 1087
Copyright
Copyright © The Animal Consortium 2013 

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References

Allen, VG, Pond, KR, Saker, KE 2001. Tasco: influence of a brown seaweed on antioxidants in forages and livestock – a review. Journal of Animal Science 79, E21–E31.Google Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ 1990. Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Annan, WD, Hirst, E, Manners, DJ 1965. The constitution of laminarin. Part V. The location of 1,6-glucosidic linkages. Journal of the Chemical Society 162, 885–891.Google Scholar
Bauer, E, Williams, BA, Smidt, H, Mosenthin, R, Verstegen, MWA 2006. Influence of dietary components on development of the microbiota in single-stomached species. Nutrition Research Reviews 19, 63–78.Google Scholar
ben Omar, N, Ampe, F 2000. Microbial community dynamics during production of the Mexican Fermented Maize Dough Pozol. Applied and Environmental Microbiology 66, 3664–3673.CrossRefGoogle ScholarPubMed
Brown, GD, Gordon, S 2005. Immune recognition of fungal β-glucans. Cellular Microbiology 7, 471–479.CrossRefGoogle ScholarPubMed
Corsetti, A, Settanni, L 2007. Lactobacilli in sourdough fermentation. Food Research International 40, 539–558.Google Scholar
Crowther, JS 1971. Transport and storage of faeces for bacteriological examination. The Journal of Applied Bacteriology 34, 477–483.CrossRefGoogle ScholarPubMed
de Lange, CFM, Pluske, J, Gong, J, Nyachoti, CM 2010. Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livestock Science 134, 124–134.Google Scholar
Devillé, C, Gharbi, M, Dandrifosse, G, Peulen, O 2007. Study on the effects of laminarin, a polysaccharide from seaweed, on gut characteristics. Journal of the Science of Food and Agriculture 87, 1717–1725.Google Scholar
Devillé, C, Damas, J, Forget, P, Dandrifosse, G, Peulen, O 2004. Laminarin in the dietary fibre concept. Journal of the Science of Food and Agriculture 84, 1030–1038.CrossRefGoogle Scholar
Fuller, R, Brooker, BE 1974. Lactobacilli which attach to the crop epithelium of the fowl. The American Journal of Clinical Nutrition 27, 1305–1312.Google Scholar
Friedlaender, MHG, Cook, WH, Martin, WG 1954. Molecular weight and hydrodynamic properties of laminarin. Biochimica et Biophysica Acta 14, 136–144.CrossRefGoogle ScholarPubMed
Gahan, DA, Lynch, MB, Callan, JJ, O'Sullivan, JT, O'Doherty, JV 2009. Performance of weanling piglets offered low-, medium- or high-lactose diets supplemented with a seaweed extract from Laminaria spp. Animal 3, 24–31.Google Scholar
Gardiner, GE, Campbell, AJ, O'Doherty, JV 2008. Effect of Ascophyllum nodosum extract on growth performance, digestibility, carcass characteristics and selected intestinal microflora populations of grower-finisher pigs. Animal Feed Science and Technology 141, 259–273.CrossRefGoogle Scholar
Giraffa, G, Chanishvili, N, Widyastuti, Y 2010. Importance of lactobacilli in food and feed biotechnology. Research in Microbiology 161, 480–487.CrossRefGoogle ScholarPubMed
Goñi, I, Gudiel-Urbano, M, Bravo, L, Saura-Calixto, F 2001. Dietary modulation of bacterial fermentative capacity by edible seaweeds in rats. Journal of Agricultural and Food Chemistry 49, 2663–2668.Google Scholar
Hammes, WP, Hertel, C 2006. The genera Lactobacillus and Carnobacterium. In The Prokaryotes (ed. M Dworkin, S Falkow, E Rosenberg, K-H Schleifer and E Stackebrandt). vol. 4, 3rd edition, pp. 320–403. Springer, New York.CrossRefGoogle Scholar
Hopwood, DE, Hampson, DJ 2003. Interactions between the intestinal microflora, diet and diarrhoea, and their influences on piglet health in the immediate post-weaning period. In Weaning The Pig: Concepts and Consequences (ed. JR Pluske, J Le Dividich and MWA Verstegen), pp. 199–218.Google Scholar
Janczyk, P, Pieper, R, Smidt, H, Souffrant, WB 2010. Effect of alginate and inulin on intestinal microbial ecology of weanling pigs reared under different husbandry conditions. FEMS Microbiology Ecology 72, 132–142.Google Scholar
Jaskari, J, Kontula, P, Siitonen, A, Jousimies-Somer, H, Mattila-Sandholm, T, Poutanen, K 1998. Oat beta-glucan and xylan hydrolysates as selective substrates for Bifidobacterium and Lactobacillus strains. Appl Microbiol Biotechnol, 49, 175–181.Google Scholar
Jassim, RAM 2003. Lactobacillus ruminis is a predominant lactic acid producing bacterium in the caecum and rectum of the pig. Letters in Applied Microbiology 37, 213–217.Google Scholar
Johansen, HN, Bach Knudsen, KE, Wood, PJ, Fulcher, RG 1997. Physico-chemical properties and the degradation of oat bran polysaccharides in the gut of pigs. Journal of the Science of Food and Agriculture 73, 81–92.Google Scholar
Kogan, G, Kocher, A 2007. Role of yeast cell wall polysaccharides in pig nutrition and health protection. Livestock Science 109, 161–165.Google Scholar
Kogan, G, Masler, L, Šandula, J, Navarová, J, Trnovec, T 1989. Recent results on the structure and immunomodulating activities of yeast glucan. Gordon and Breach Science Publishers, New York.Google Scholar
Konstantinov, SR, Awati, A, Smidt, H, Williams, BA, Akkermans, ADL, de Vos, WM 2004. Specific response of a novel and abundant lactobacillus amylovorus-like phylotype to dietary prebiotics in the guts of weaning piglets. Applied and Environmental Microbiology 70, 3821–3830.CrossRefGoogle ScholarPubMed
Lynch, M, Sweeney, T, Callan, J, O’ Sullivan, J, O’ Doherty, JV 2010. The effect of dietary Laminaria-derived laminarin and fucoidan on nutrient digestibility, nitrogen utilisation, intestinal microflora and volatile fatty acid concentration in pigs. Journal of the Science of Food and Agriculture 90, 430–437.Google Scholar
Mackie, RI, Sghir, A, Gaskins, HR 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. The American Journal of Clinical Nutrition 69, 1035S–1045S.Google Scholar
Majtán, J, Kogan, G, Kováčová, E, Bíliková, K, Šimúth, J 2005. Stimulation of TNF-α release by fungal cell wall polysaccharides. Bioscience (Section C) 60, 921–926.Google Scholar
Marais, MF, Joseleau, JP 2001. A fucoidan fraction from Ascophyllum nodosum. Carbohydrate Research 336, 155–159.Google Scholar
Marti, R, Dabert, P, Ziebal, C, Pourcher, AM 2010. Evaluation of Lactobacillus sobrius/L. amylovorus as a new microbial marker of pig manure. Applied and Environmental Microbiology 76, 1456–1461.Google Scholar
Mathers, JC, Annison, EF 1993. Stoichiometry of polysaccharide fermentation in the large intestine. In Dietary fibre and beyond – Australian perspectives; No. 1 (ed. S Samman and G Annison), pp. 95–114. Nutrition Society of Australia Occasional Publications, Perth, Australia.Google Scholar
Meroth, CB, Walter, J, Hertel, C, Brandt, MJ, Hammes, WP 2003. Monitoring the bacterial population dynamics in sourdough fermentation processes by using PCR-denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 69, 475–482.Google Scholar
Michel, C, Bernard, C, Lahaye, M 1999. Algal oligosaccharides as functional foods: in vitro study of their cellular and fermentative effects. Food science 19, 311–332.Google Scholar
Mirelman, D, Altmann, G, Eshdat, Y 1980. Screening of bacterial isolates for mannose-specific lectin activity by agglutination of yeasts. Journal of Clinical Microbiology 11, 328–331.Google Scholar
Naito, S, Hayashidani, H, Kaneko, K, Ogawa, M, Benno, Y 1995. Development of intestinal lactobacilli in normal piglets. Journal of Applied Microbiology 79, 230–236.Google ScholarPubMed
Percival, EMcDowell, RH 1967. Chemistry and enzymology of marine algae polysaccharides. Mag Westerlo, London, pp. 53–71.Google Scholar
Pieper, R, Janzcyk, P, Zeyner, A, Smidt, H, Guiard, V, Souffrant, WB 2008. Ecophysiology of the developing total bacterial and Lactobacillus communities in the terminal small intestine of weaning piglets. Microbial Ecology 56, 474–483.CrossRefGoogle ScholarPubMed
Read, SM, Currie, G, Bacic, A 1996. Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydrate Research 281, 187–201.CrossRefGoogle ScholarPubMed
Reilly, P, O'Doherty, JV, Pierce, KM, Callan, JJ, O'Sullivan, JT, Sweeney, T 2008. The effects of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient digestibility, volatile fatty acid concentrations and the immune status of the weaned pig. Animal 2I1465–1473.Google Scholar
Roos, S, Karner, F, Axelsson, L, Jonsson, H 2000. Lactobacillus mucosae sp. nov., a new species with in vitro mucus-binding activity isolated from pig intestine. International Journal of Systematic and Evolutionary Microbiology 50, 251–258.Google Scholar
Shibata, H, Iimuro, M, Uchiya, N 2003. Preventive effects of Cladosiphon Fucoidan against Helicobacter pylori infection in Mongolian gerbils. Helicobacter 8, 59–65.Google Scholar
Smith, HW, Jones, JE 1963. Observations on the alimentary tract and its bacterial flora in healthy and diseased pigs. Journal of Pathology and Bacteriology 86, 387–412.Google Scholar
Stewart, CS 1997. Microorganisms in hindgut fermentors. Chapman & Hall, New York.Google Scholar
Tannock, GW, Fuller, R, Pedersen, K 1990. Lactobacillus succession in the piglet digestive tract demonstrated by plasmid profiling. Applied and Environmental Microbiology 56, 1310–1316.Google Scholar
Teitelbaum, JE, Walker, WA 2002. Nutritional impact of pre- and probiotics as protective gastrointestinal organisms. Annual Review of Nutrition 22, 107–138.Google Scholar
Vaughan, EE, de Vries, MC, Zoetendal, EG, Ben-Amor, K, Akkermans, ADL, de Vos, WM 2002. The intestinal LABs. Antonie van Leeuwenhoek 82, 341–352.CrossRefGoogle ScholarPubMed
Walter, J 2008. Ecological role of Lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Applied and Environmental Microbiology 74, 4985–4996.CrossRefGoogle ScholarPubMed
Walter, J, Hertel, C, Tannock, GW, Lis, CM, Munro, K, Hammes, WP 2001. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella Species in Human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 67, 2578–2585.Google Scholar
Wang, Y 2009. Prebiotics: present and future in food science and technology. Food Research International 42, 8–12.Google Scholar
Yun, C-H, Estrada, A, van Kessel, A, Park, BC, Laarveld, B 2003. β-Glucan, extracted from oat, enhances disease resistance against bacterial and parasitic infections. FEMS Immunology & Medical Microbiology 35, 67–75.Google Scholar
Zvyagintseva, TN, Shevchenko, NM, Chizhov, AO, Krupnova, TN, Sundukova, EV, Isakov, VV 2003. Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. Journal of Experimental Marine Biology and Ecology 294, 1–13.CrossRefGoogle Scholar
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