Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-08T09:33:57.777Z Has data issue: false hasContentIssue false

Adaptation of faecal microbiota in sows after diet changes and consequences for in vitro fermentation capacity

Published online by Cambridge University Press:  22 May 2015

M. A. Sappok
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands
O. Peréz Gutiérrez
Affiliation:
Laboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, the Netherlands
H. Smidt
Affiliation:
Laboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, the Netherlands
W. F. Pellikaan*
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands
M. W. A. Verstegen
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands
G. Bosch
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands
W. H. Hendriks
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands Faculty of Veterinarian Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, the Netherlands
*
Get access

Abstract

In vitro gas production studies are routinely used to assess the metabolic capacity of intestinal microbiota to ferment dietary fibre sources. The faecal inocula used during the in vitro gas production procedure are most often obtained from animals adapted to a certain diet. The present study was designed to assess whether 19 days of adaptation to a diet are sufficient for faecal inocula of pigs to reach a stable microbial composition and activity as determined by in vitro gas production. Eighteen multiparous sows were allotted to one of two treatments for three weeks: a diet high in fibre (H) or a diet low in fibre (L). After this 3-week period, the H group was transferred to the low fibre diet (HL-treatment) while the L group was transferred to the diet high in fibre (LH-treatment). Faecal samples were collected from each sow at 1, 4, 7, 10, 13, 16 and 19 days after the diet change and prepared as inoculum used for incubation with three contrasting fermentable substrates: oligofructose, soya pectin and cellulose. In addition, inocula were characterised using a phylogenetic microarray targeting the pig gastrointestinal tract microbiota. Time after diet change had an effect (P<0.05) on total gas production for the medium–fast fermentable substrates; soya pectin and oligofructose. For the more slowly fermentable cellulose, all measured fermentation parameters were consistently higher (P<0.05) for animals in the HL-treatment. Diet changes led to significant changes in relative abundance of specific bacteria, especially for members of the Bacteroidetes and Bacilli, which, respectively, increased or decreased for the LH-treatment, while changes were opposite for the HL-treatment. Changing the diet of sows led to changes in fermentation activity of the faecal microbiota and in composition of the microbiota over time. Adaptation of the microbiota as assessed by gas production occurred faster for LH-animals for fast fermentable substrates compared with HL-animals. Overall, adaptation of the large intestinal microbiota of sows as a result of ingestion of low and high fibre diets seems to take longer than 19 days, especially for the ability to ferment slowly fermentable substrates.

Type
Research Article
Copyright
© The Animal Consortium 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anguita, M, Canibe, N, Pérez, JF and Jensen, BB 2006. Influence of dietary fiber on the available energy from hindgut fermentation in growing pigs: use of cannulated pigs and in vitro fermentation. Journal of Animal Science 84, 27662778.Google Scholar
Awati, A, Williams, BA, Bosch, MW, Li, YC and Verstegen, MWA 2006. Use of in vitro cumulative gas production technique for pigs: an examination of alterations in fermentation products and substrate losses at various time points. Journal of Animal Science 84, 11101118.CrossRefGoogle ScholarPubMed
Bach Knudsen, KE, Hedeman, MS and Lærke, HN 2012. The role of carbohydrates in intestinal health of pigs. Animal Feed Science and Technology 173, 4153.Google Scholar
Bauer, E, Williams, BA, Voigt, C, Mosenthin, R and Verstegen, MWA 2001. Microbial activities of faeces from unweaned and adult pigs in relation to selected fermentable carbohydrates. Animal Science 73, 313322.Google Scholar
Bauer, E, Williams, BA, Bosch, MW, Voigt, C, Mosenthin, R and Verstegen, MWA 2004. Differences in microbial activity of digesta from three sections of the porcine large intestine according to in vitro fermentation of carbohydrate-rich substrates. Journal of the Science of Food and Agriculture 84, 20972104.Google Scholar
Beuvink, JMW and Spoelstra, SF 1992. Interactions between substrate, fermentation end-products, buffering systems and gas production upon fermentation of different carbohydrates by mixed rumen microorganisms in vitro . Applied Microbiology and Biotechnology 37, 505509.Google Scholar
Bindelle, J, Leterme, P and Buldgen, A 2008. Nutritional and environmental consequences of dietary fibre in pig nutrition: a review. Biotechnology, Agronomy, Society and Environment 12, 6980.Google Scholar
Bindelle, J, Buldgen, A, Michaux, D, Wavreille, J, Destain, JP and Leterme, P 2007. Influence of purified dietary fibre on bacterial protein synthesis in the large intestine of pigs, as measured by the gas production technique. Livestock Science 109, 232235.Google Scholar
Bindelle, J, Buldgen, A, Delacolette, M, Wavreille, J, Agneessens, R, Destain, JP and Leterme, P 2009. Influence of source and concentrations of dietary fiber on in vivo nitrogen excretion pathways in pigs as reflected by in vitro fermentation and nitrogen incorporation by fecal bacteria. Journal of Animal Science 87, 583593.Google Scholar
Bosch, G, Pellikaan, WF, Rutten, PGP, van der Poel, AFB, Verstegen, MWA and Hendriks, WH 2008. Comparative in vitro fermentation activity in the canine distal gastrointestinal tract and fermentation kinetics of fiber sources. Journal of Animal Science 86, 29792989.Google Scholar
Chabeauti, E, Noblet, J and Carré, B 1991. Digestion of plant cell walls from four different sources in growing pigs. Animal Feed Science and Technology 32, 207213. 7.CrossRefGoogle Scholar
Cone, JW, van Gelder, AH, Visscher, GJW and Oudshoorn, L 1996. Influence of rumen fluid and substrate concentration on fermentation kinetics measured with a fully automated time related gas production apparatus. Animal Feed Science and Technology 61, 113128.CrossRefGoogle Scholar
Centraal Veevoederbureau (CVB) 2010. Veevoedertabel [Feedstuff Table, Nutritional Value of Feed Ingredients]. CVB, Lelystad, the Netherlands.Google Scholar
De Leeuw, JA, Bolhuis, JE, Bosch, G and Gerrits, WJJ 2008. Effects of dietary fibre on behaviour and satiety in pigs. Proceedings of the Nutrition Society 67, 334342.Google Scholar
Goering, HK and van Soest, PJ 1972. Forage fiber analyses (apparatus, reagents, procedures and some applications). Agriculture handbook No 379. US Department of Agriculture, US Government Printing Office, Washington, DC, USA.Google Scholar
Groot, JCJ, Cone, JW, Williams, BA, Debersaques, FMA and Lantinga, EA 1996. Multiphasic analysis of gas production kinetics for in vitro fermentation of ruminant feeds. Animal Feed Science and Technology 64, 7789.Google Scholar
Haenen, D, Zhang, J, da Silva, CS, Bosch, G, van der Meer, IM, van Arkel, J, van den Borne, JJ, Perez Gutierrez, O, Smidt, H, Kemp, B, Muller, M and Hooiveld, GJ 2013. A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine. Journal of Nutrition 143, 274283.Google Scholar
Kolmeder, CA, de Been, M, Nikkila, J, Ritamo, I, Matto, J, Valmu, L, Salojarvi, J, Palva, A, Salonen, A and de Vos, WM 2012. Comparative metaproteomics and diversity analysis of human intestinal microbiota testifies for its temporal stability and expression of core functions. PLoS One 7, e29913.CrossRefGoogle ScholarPubMed
Lin, B, Gong, J, Wang, Q, Cui, S, Yu, H and Huang, B 2011. In vitro assessment of the effects of dietary fibres on microbial fermentation and communities from large intestinal digesta of pigs. Food Hydrocolloids 25, 180188.Google Scholar
Littell, RC, Henry, PR and Ammermann, CB 1998. Statistical analysis of repeated measures data using SAS procedures. Journal of Animal Science 76, 12161231.CrossRefGoogle Scholar
Longland, AC, Low, AG, Quelch, DB and Bray, SP 1993. Adaptation to the digestion of non-starch polysaccharide in growing pigs fed on cereal or semi-purified basal diets. British Journal of Nutrition 70, 557566.Google Scholar
Martín-Paláez, S, Manzanilla, EG, Anguita, M, Fondevila, M, Martín, M, Mateu, E and Martín-Orúe, SM 2009. Different fibrous ingredients and coarsely ground maize effect hindgut fermentation in the pig in vitro but not Salmonella typhimurium survival. Animal Feed Science and Technology 153, 141152.Google Scholar
Owusu-Asiedu, A, Patience, JF, Laarveld, B, van Kessel, AG, Simmins, PH and Zijlstra, RT 2006. Effects of guar gum and cellulose on digesta passage rate, ileal microbial populations, energy and protein digestibility, and performance of grower pigs. Journal of Animal Science 84, 843852.Google Scholar
Pérez Gutiérrez, O 2010. Unravelling piglet gut microbiota dynamics in response to feed additives. PhD, Laboratory of Microbiology of the Wageningen University, Wageningen, the Netherlands.Google Scholar
Rajilić-Stojanović, M 2007. Diversity of the human gastrointestinal microbiota: novel perspectives from high throughput analyses. PhD, Laboratory of Microbiology of the Wageningen University, Wageningen, the Netherlands.Google Scholar
Rajilić-Stojanović, M, Heilig, HG, Molenaar, D, Kajander, K, Surakka, A, Smidt, H and de Vos, WM 2009. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environmental Microbiology 11, 17361751.Google Scholar
R Development Core Team 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Salonen, A, Nikkilä, J, Jalanka-Tuovinen, J, Immonen, O, Rajilić-Stojanović, M, Kekkonen, RA, Palva, A and de Vos, WM 2010. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. Journal of Microbial Methods 81, 127134.Google Scholar
Sappok, M, Pellikaan, WF, Verstegen, MWA, Bosch, G, Sundrum, A and Hendriks, WH 2013a. Repeated measurements of in vitro fermentation of fibre-rich substrates using large intestinal microbiota of sows. Journal of the Science of Food and Agriculture 93, 987994.Google Scholar
Sappok, M, Pellikaan, WF, Verstegen, MWA, Bosch, G, Sundrum, A and Hendriks, WH 2013b. Large intestinal capacity of fattening pigs on organic farms as measured in vitro using contrasting substrates. Journal of the Science of Food and Agriculture 93, 24022409.Google Scholar
Tempelman, RJ 2004. Experimental design and statistical methods for classical and bioequivalence hypothesis testing with an application to dairy nutrition studies. Journal of Animal Science 82, E162E172.Google Scholar
Ter Braak, CJF and Šmilauer, P 2002. CANOCO reference manual and CanoDraw for windows user’s guide: software for canonical community ordination, version 4.5. Microcomputer Power, Ithaca, NY, USA.Google Scholar
Van den Brink, PJ and ter Braak, CJFT 1999. Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environmental Toxicology and Chemistry 18, 138148.Google Scholar
Varel, VH, Pond, WG and Yen, JT 1984. Influence of dietary fiber on the performance and cellulase activity of growing-finishing swine. Journal of Animal Science 59, 388393.Google Scholar
Varel, VH, Robinson, IM and Jung, HJ 1987. Influence of dietary fiber on xylanolytic and cellulolytic bacteria of adult pigs. Applied and Environmental Biology 53, 2226.Google Scholar
Varel, VH, Pond, WG, Pekas, JC and Yen, JT 1982. Influence of high fiber diet on microbial populations in gastrointestinal tracts of obese- and lean-genotype pigs. Applied and Environmental Biology 44, 107112.Google Scholar
Williams, BA, Verstegen, MWA and Tamminga, S 2001. Fermentation in the monogastric large intestine: its relation to animal health. Nutrition Research Reviews 14, 207227.Google Scholar
Williams, BA, Bosch, MW, Boer, H, Verstegen, MWA and Tamminga, S 2005. An in vitro batch culture method to assess potential fermentability of feed ingredients for monogastric diets. Animal Feed Science and Technology 123–124, 445462.Google Scholar
Yu, Z and Morrison, M 2004. Comparisons of different hypervariable regions of rrs genes for use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Applied and Environmental Biology 70, 48004806.Google Scholar
Zoetendal, EG, Raes, J, van den Bogert, B, Arumugam, M, Booijink, CC, Troost, FJ, Bork, P, Wels, M, de Vos, WM and Kleerebezem, M 2012. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. International Society for Microbial Ecology Journal 6, 14151426.Google Scholar