Effects of replacing starch with three sugars in a concentrate and forage diet on in vitro rumen fermentation, fatty acid composition and related bacteria
X. Q. Sun A , Y. P. Wang A , R. Y. Wei A , B. Chen A and X. Zhao A B CA College of Animal Science and Technology, Northwest A&F University, No. 22, Xinong Road, Yangling, Shaanxi, 712100, People’s Republic of China.
B Department of Animal Science, McGill University, 21111 Lakeshore, Sainte-Anne-de-Bellevue, Quebec, H9X 3V9, Canada.
C Corresponding author. Email: xin.zhao@mcgill.ca
Animal Production Science 60(9) 1173-1182 https://doi.org/10.1071/AN18287
Submitted: 7 May 2018 Accepted: 22 November 2019 Published: 10 March 2020
Abstract
Context: Replacing starch with sugar could maintain dietary energy density with reduced risks of rumen acidosis and milk fat depression, but the underlying mechanism is not well understood, and the effects of sugar feeding might vary among sugars.
Aims: Objectives of the present study were to evaluate the effects of replacing corn starch in a diet containing 40 : 60 forage-to-concentrate ratio (control) with 3%, 6% and 9% of sucrose, fructose and lactose on in vitro rumen fermentation, fatty acid (FA) composition and populations of bacteria involved in the production of trans-11 and trans-10 FA.
Methods: A 3 × 3 + 1 (control) factorial experimental design was used, and the pH, concentrations of volatile fatty acids (VFA) and ammonia-N, profiles of FA and the relative abundance of four trans-11-producing bacteria and two trans-10 FA-producing bacteria were measured after a 6-h incubation.
Key results: Replacing dietary corn starch with sucrose, fructose and lactose neither altered the concentration of total VFA after 6-h fermentation, nor decreased the pH, except for substitution with 9% sucrose. Increased butyrate proportions and decreased branched-chain VFA proportions were the common effects in sugar treatments, but the proportions of acetate and propionate varied among sugars. Lactose inclusion in the diet led to a higher pH, greater acetate and butyrate concentrations, and lower propionate concentrations than did sucrose inclusion. Sugar substitution decreased the concentrations of C18:1 trans-4 and most C18:2 isomers, but did not influence the major isomers related to trans-11 and trans-10 biohydrogenation pathways. Abundance of the four measured trans-11 FA-producing bacteria was increased by sugars, with sucrose showing a greater influence than did fructose and lactose. As to trans-10 FA-producing bacteria, only Megasphaera elsdenii populations were decreased by 3% and 6% fructose inclusion compared with the control. Dose-effect varied among sugars and the parameters measured, with sucrose having the most obvious dose effect among the three sugars; however, fructose affected mainly fermentation parameters, while lactose affected mainly C18 FA profiles.
Conclusions: Replacing corn starch in a high-concentrate diet with up to 9% of sucrose, fructose and lactose differentially affected rumen fermentation and rumen FA metabolism, by influencing the abundance of rumen bacteria involved in rumen FA biohydrogenation.
Implications: Lactose may be more efficient in increasing milk fat than are sucrose and fructose, and dose effect should be considered in the utilisation of sucrose.
Additional keywords: bacterial populations, corn starch, fatty acid biohydrogenation, sugars, volatile fatty acids.
References
AOAC (1998) ‘Official methods of analysis.’ (Association of Analytical Chemists: Arlington, VA)Aschenbach JR, Penner GB, Stumpff F, Gabel G (2011) Ruminant nutrition symposium: role of fermentation acid absorption in the regulation of ruminal pH. Journal of Animal Science 89, 1092–1107.
Broderick GA, Luchini ND, Reynal SM, Varga GA, Ishler VA (2008) Effect on production of replacing dietary starch with sucrose in lactating dairy cows. Journal of Dairy Science 91, 4801–4810.
| Effect on production of replacing dietary starch with sucrose in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 19038955PubMed |
Chamberlain DG, Robertson S, Choung J-J (1993) Sugars versus starch as supplements to grass silage: effects on ruminal fermentation and the supply of microbial protein to the small intestine, estimated from the urinary excretion of purine derivatives, in sheep. Journal of the Science of Food and Agriculture 63, 189–194.
| Sugars versus starch as supplements to grass silage: effects on ruminal fermentation and the supply of microbial protein to the small intestine, estimated from the urinary excretion of purine derivatives, in sheep.Crossref | GoogleScholarGoogle Scholar |
Chibisa GE, Gorka P, Penner GB, Berthiaume R, Mutsvangwa T (2015) Effects of partial replacement of dietary starch from barley or corn with lactose on ruminal function, short-chain fatty acid absorption, nitrogen utilization, and production performance of dairy cows. Journal of Dairy Science 98, 2627–2640.
| Effects of partial replacement of dietary starch from barley or corn with lactose on ruminal function, short-chain fatty acid absorption, nitrogen utilization, and production performance of dairy cows.Crossref | GoogleScholarGoogle Scholar | 25704977PubMed |
de Menezes AB, Lewis E, O’Donovan M, O’Neill BF, Clipson N, Doyle EM (2011) Microbiome analysis of dairy cows fed pasture or total mixed ration diets. FEMS Microbiology Ecology 78, 256–265.
| Microbiome analysis of dairy cows fed pasture or total mixed ration diets.Crossref | GoogleScholarGoogle Scholar | 21671962PubMed |
DeFrain JM, Hippen AR, Kalscheur KF, Schingoethe DJ (2004) Feeding lactose increases ruminal butyrate and plasma β-hydroxybutyrate in lactating dairy cows. Journal of Dairy Science 87, 2486–2494.
| Feeding lactose increases ruminal butyrate and plasma β-hydroxybutyrate in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 15328272PubMed |
Fawcett J, Scott J (1960) A rapid and precise method for the determination of urea. Journal of Clinical Pathology 13, 156–159.
| A rapid and precise method for the determination of urea.Crossref | GoogleScholarGoogle Scholar | 13821779PubMed |
Fernando SC, Purvis HT, Najar FZ, Sukharnikov LO, Krehbiel CR, Nagaraja TG, Roe BA, Desilva U (2010) Rumen microbial population dynamics during adaptation to a high-grain diet. Applied and Environmental Microbiology 76, 7482–7490.
| Rumen microbial population dynamics during adaptation to a high-grain diet.Crossref | GoogleScholarGoogle Scholar | 20851965PubMed |
Gao X, Oba M (2016) Effect of increasing dietary nonfiber carbohydrate with starch, sucrose, or lactose on rumen fermentation and productivity of lactating dairy cows. Journal of Dairy Science 99, 291–300.
| Effect of increasing dietary nonfiber carbohydrate with starch, sucrose, or lactose on rumen fermentation and productivity of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 26585468PubMed |
Hall MB, Hoover WH, Jennings JP, Webster TKM (1999) A method for partitioning neutral detergent-soluble carbohydrates. Journal of the Science of Food and Agriculture 79, 2079–2086.
| A method for partitioning neutral detergent-soluble carbohydrates.Crossref | GoogleScholarGoogle Scholar |
Heldt JS, Cochran RC, Stokka GL, Farmer CG, Mathis CP, Titgemeyer EC, Nagaraja TG (1999) Effects of different supplemental sugars and starch fed in combination with degradable intake protein on low-quality forage use by beef steers. Journal of Animal Science 77, 2793–2802.
| Effects of different supplemental sugars and starch fed in combination with degradable intake protein on low-quality forage use by beef steers.Crossref | GoogleScholarGoogle Scholar | 10521042PubMed |
Jenkins TC, Wallace RJ, Moate PJ, Mosley EE (2008) Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. Journal of Animal Science 86, 397–412.
| Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem.Crossref | GoogleScholarGoogle Scholar | 18042812PubMed |
Kepler CR, Hirons KP, McNeill JJ, Tove SB (1966) Intermediates and products of the biohydrogenation of linoleic acid by Butyrivibrio fibrisolvens. The Journal of Biological Chemistry 241, 1350–1354.
Khorasani GR, Okine EK, Kennelly JJ (1996) Forage source alters nutrient supply to the intestine without influencing milk yield. Journal of Dairy Science 79, 862–872.
| Forage source alters nutrient supply to the intestine without influencing milk yield.Crossref | GoogleScholarGoogle Scholar | 8792286PubMed |
Kim YJ, Liu RH, Bond DR, Russell JB (2000) Effect of linoleic acid concentration on conjugated linoleic acid production by Butyrivibrio fibrisolvens A38. Applied and Environmental Microbiology 66, 5226–5230.
| Effect of linoleic acid concentration on conjugated linoleic acid production by Butyrivibrio fibrisolvens A38.Crossref | GoogleScholarGoogle Scholar | 11097894PubMed |
Kim YJ, Liu RH, Rychlik JL, Russell JB (2002) The enrichment of a ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid. Journal of Applied Microbiology 92, 976–982.
| The enrichment of a ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid.Crossref | GoogleScholarGoogle Scholar | 11972704PubMed |
Kittelmann S, Seedorf H, Walters WA, Clemente JC, Knight R, Gordon JI, Janssen PH (2013) Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS One 8, e47879
| Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities.Crossref | GoogleScholarGoogle Scholar | 24312255PubMed |
Knudsen KEB (1997) Carbohydrate and lignin contents of plant materials used in animal feeding. Animal Feed Science and Technology 67, 319–338.
| Carbohydrate and lignin contents of plant materials used in animal feeding.Crossref | GoogleScholarGoogle Scholar |
Lee MR, Huws SA, Scollan ND, Dewhurst RJ (2007) Effects of fatty acid oxidation products (green odor) on rumen bacterial populations and lipid metabolism in vitro. Journal of Dairy Science 90, 3874–3882.
| Effects of fatty acid oxidation products (green odor) on rumen bacterial populations and lipid metabolism in vitro.Crossref | GoogleScholarGoogle Scholar | 17638998PubMed |
Li F, Li Z, Li S, Ferguson JD, Cao Y, Yao J, Sun F, Wang X, Yang T (2014) Effect of dietary physically effective fiber on ruminal fermentation and the fatty acid profile of milk in dairy goats. Journal of Dairy Science 97, 2281–2290.
| Effect of dietary physically effective fiber on ruminal fermentation and the fatty acid profile of milk in dairy goats.Crossref | GoogleScholarGoogle Scholar | 24508430PubMed |
Loor JJ, Ueda K, Ferlay A, Chilliard Y, Doreau M (2004) Biohydrogenation, duodenal flow, and intestinal digestibility of trans fatty acids and conjugated linoleic acids in response to dietary forage: concentrate ratio and linseed oil in dairy cows. Journal of Dairy Science 87, 2472–2485.
| Biohydrogenation, duodenal flow, and intestinal digestibility of trans fatty acids and conjugated linoleic acids in response to dietary forage: concentrate ratio and linseed oil in dairy cows.Crossref | GoogleScholarGoogle Scholar | 15328271PubMed |
Martel CA, Titgemeyer EC, Mamedova LK, Bradford BJ (2011) Dietary molasses increases ruminal pH and enhances ruminal biohydrogenation during milk fat depression. Journal of Dairy Science 94, 3995–4004.
| Dietary molasses increases ruminal pH and enhances ruminal biohydrogenation during milk fat depression.Crossref | GoogleScholarGoogle Scholar | 21787935PubMed |
McSweeney CS, Denman SE (2007) Effect of sulfur supplements on cellulolytic rumen micro-organisms and microbial protein synthesis in cattle fed a high fibre diet. Journal of Applied Microbiology 103, 1757–1765.
| Effect of sulfur supplements on cellulolytic rumen micro-organisms and microbial protein synthesis in cattle fed a high fibre diet.Crossref | GoogleScholarGoogle Scholar | 17953586PubMed |
Oba M (2011) Review: effects of feeding sugars on productivity of lactating dairy cows. Canadian Journal of Animal Science 91, 37–46.
| Review: effects of feeding sugars on productivity of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |
Oba M, Mewis JL, Zhining Z (2015) Effects of ruminal doses of sucrose, lactose, and corn starch on ruminal fermentation and expression of genes in ruminal epithelial cells. Journal of Dairy Science 98, 586–594.
| Effects of ruminal doses of sucrose, lactose, and corn starch on ruminal fermentation and expression of genes in ruminal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 25468705PubMed |
Or-Rashid MM, Kramer JKG, Wood MA, McBride BW (2008) Supplemental algal meal alters the ruminal trans-18:1 fatty acid and conjugated linoleic acid composition in cattle. Journal of Animal Science 86, 187–196.
| Supplemental algal meal alters the ruminal trans-18:1 fatty acid and conjugated linoleic acid composition in cattle.Crossref | GoogleScholarGoogle Scholar | 17940158PubMed |
Owens FN, Goetsch AL (1988) Ruminal fermentation. In ‘The ruminant animal: digestive physiology and nutrition’. (Ed. DC Church) pp. 145–171. (Waveland Press Inc.: Prospect Heights, IL)
Penner GB, Oba M (2009) Increasing dietary sugar concentration may improve dry matter intake, ruminal fermentation, and productivity of dairy cows in the postpartum phase of the transition period. Journal of Dairy Science 92, 3341–3353.
| Increasing dietary sugar concentration may improve dry matter intake, ruminal fermentation, and productivity of dairy cows in the postpartum phase of the transition period.Crossref | GoogleScholarGoogle Scholar | 19528611PubMed |
Penner GB, Guan LL, Oba M (2009) Effects of feeding Fermenten on ruminal fermentation in lactating Holstein cows fed two dietary sugar concentrations. Journal of Dairy Science 92, 1725–1733.
| Effects of feeding Fermenten on ruminal fermentation in lactating Holstein cows fed two dietary sugar concentrations.Crossref | GoogleScholarGoogle Scholar | 19307654PubMed |
Razzaghi A, Valizadeh R, Naserian AA, Mesgaran MD, Carpenter AJ, Ghaffari MH (2016) Effect of dietary sugar concentration and sunflower seed supplementation on lactation performance, ruminal fermentation, milk fatty acid profile, and blood metabolites of dairy cows. Journal of Dairy Science 99, 3539–3548.
| Effect of dietary sugar concentration and sunflower seed supplementation on lactation performance, ruminal fermentation, milk fatty acid profile, and blood metabolites of dairy cows.Crossref | GoogleScholarGoogle Scholar | 26971160PubMed |
Ribeiro CV, Karnati SK, Eastridge ML (2005) Biohydrogenation of fatty acids and digestibility of fresh alfalfa or alfalfa hay plus sucrose in continuous culture. Journal of Dairy Science 88, 4007–4017.
| Biohydrogenation of fatty acids and digestibility of fresh alfalfa or alfalfa hay plus sucrose in continuous culture.Crossref | GoogleScholarGoogle Scholar | 16230707PubMed |
Shingfield KJ, Kairenius P, Arola A, Paillard D, Muetzel S, Ahvenjarvi S, Vanhatalo A, Huhtanen P, Toivonen V, Griinari JM, Wallace RJ (2012) Dietary fish oil supplements modify ruminal biohydrogenation, alter the flow of fatty acids at the omasum, and induce changes in the ruminal butyrivibrio population in lactating cows. Journal of Nutrition 142, 1437–1448.
| Dietary fish oil supplements modify ruminal biohydrogenation, alter the flow of fatty acids at the omasum, and induce changes in the ruminal butyrivibrio population in lactating cows.Crossref | GoogleScholarGoogle Scholar | 22739367PubMed |
Stevenson DM, Weimer PJ (2007) Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Applied Microbiology and Biotechnology 75, 165–174.
| Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR.Crossref | GoogleScholarGoogle Scholar | 17235560PubMed |
Sun X, Wang Y, Chen B, Zhao X (2015) Partially replacing cornstarch in a high-concentrate diet with sucrose inhibited the ruminal trans-10 biohydrogenation pathway in vitro by changing populations of specific bacteria. Journal of Animal Science and Biotechnology 6, 57
| Partially replacing cornstarch in a high-concentrate diet with sucrose inhibited the ruminal trans-10 biohydrogenation pathway in vitro by changing populations of specific bacteria.Crossref | GoogleScholarGoogle Scholar | 26705470PubMed |
Sutton JD (1968) The fermentation of soluble carbohydrates in rumen contents of cows fed diets containing a large proportion of hay. British Journal of Nutrition 22, 689–712.
| The fermentation of soluble carbohydrates in rumen contents of cows fed diets containing a large proportion of hay.Crossref | GoogleScholarGoogle Scholar | 5712037PubMed |
Vallimont JE, Bargo F, Cassidy TW, Luchini ND, Broderick GA, Varga GA (2004) Effects of replacing dietary starch with sucrose on ruminal fermentation and nitrogen metabolism in continuous culture. Journal of Dairy Science 87, 4221–4229.
| Effects of replacing dietary starch with sucrose on ruminal fermentation and nitrogen metabolism in continuous culture.Crossref | GoogleScholarGoogle Scholar | 15545386PubMed |
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
| Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar | 1660498PubMed |
Vlaeminck B, Khattab W, Fievez V (2015) Is ruminal trans-11–18:1 accumulation a prerequisite for trans-10–18:1 production? Animal Production Science 55, 225–230.
| Is ruminal trans-11–18:1 accumulation a prerequisite for trans-10–18:1 production?Crossref | GoogleScholarGoogle Scholar |
Wallace RJ, McKain N, Shingfield KJ, Devillard E (2007) Isomers of conjugated linoleic acids are synthesized via different mechanisms in ruminal digesta and bacteria. Journal of Lipid Research 48, 2247–2254.
| Isomers of conjugated linoleic acids are synthesized via different mechanisms in ruminal digesta and bacteria.Crossref | GoogleScholarGoogle Scholar | 17644775PubMed |
Weisbjerg MR, Hvelplund T, Bibby BM (1998) Hydrolysis and fermentation rate of glucose, sucrose and lactose in the rumen. Acta Agriculturæ Scandinavica. Section A, Animal Science 48, 12–18.
| Hydrolysis and fermentation rate of glucose, sucrose and lactose in the rumen.Crossref | GoogleScholarGoogle Scholar |
Zened A, Troegeler-Meynadier A, Nicot MC, Combes S, Cauquil L, Farizon Y, Enjalbert F (2011) Starch and oil in the donor cow diet and starch in substrate differently affect the in vitro ruminal biohydrogenation of linoleic and linolenic acids. Journal of Dairy Science 94, 5634–5645.
| Starch and oil in the donor cow diet and starch in substrate differently affect the in vitro ruminal biohydrogenation of linoleic and linolenic acids.Crossref | GoogleScholarGoogle Scholar | 22032386PubMed |