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Reducing protein content in the diet of growing goats: implications for nitrogen balance, intestinal nutrient digestion and absorption, and rumen microbiota

Published online by Cambridge University Press:  08 May 2020

X. X. Zhang ,
Y. X. Li ,
Z. R. Tang ,
W. Z. Sun ,
L. T. Wu ,
R. An ,
H. Y. Chen ,
K. Wan  and
Z. H. Sun Open the ORCID record for Z. H. Sun [Opens in a new window]
X. X. Zhang
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
Y. X. Li
Affiliation:
Institute of Animal Nutrition, Sichuan Agricultural University, Chengdu611130, P. R. China
Z. R. Tang
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
W. Z. Sun
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
L. T. Wu
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
R. An
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
H. Y. Chen
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
K. Wan
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
Z. H. Sun*
Affiliation:
Laboratory of Bio-feed and Molecular Nutrition, Southwest University, Chongqing400715, P. R. China
*
†E-mail: sunzh2002cn@aliyun.com
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Abstract

Reducing dietary CP content is an effective approach to reduce animal nitrogen excretion and save protein feed resources. However, it is not clear how reducing dietary CP content affects the nutrient digestion and absorption in the gut of ruminants, therefore it is difficult to accurately determine how much reduction in dietary CP content is appropriate. This study was conducted to investigate the effects of reduced dietary CP content on N balance, intestinal nutrient digestion and absorption, and rumen microbiota in growing goats. To determine N balance, 18 growing wether goats (25.0 ± 0.5 kg) were randomly assigned to one of three diets: 13.0% (control), 11.5% and 10.0% CP. Another 18 growing wether goats (25.0 ± 0.5 kg) were surgically fitted with ruminal, proximate duodenal, and terminal ileal fistulae and were randomly assigned to one of the three diets to investigate intestinal amino acid (AA) absorption and rumen microbiota. The results showed that fecal and urinary N excretion of goats fed diets containing 11.5% and 10.0% CP were lower than those of goats fed the control diet (P < 0.05). When compared with goats fed the control diet, N retention was decreased and apparent N digestibility in the entire gastrointestinal tract was increased in goats fed the 10% CP diet (P < 0.05). When compared with goats fed the control diet, the duodenal flow of lysine, tryptophan and phenylalanine was decreased in goats fed the 11.5% CP diet (P < 0.05) and that of lysine, methionine, tryptophan, phenylalanine, leucine, glutamic acid, tyrosine, essential AAs (EAAs) and total AAs (TAAs) was decreased in goats fed the 10.0% CP diet (P < 0.05). When compared with goats fed the control diet, the apparent absorption of TAAs in the small intestine was increased in goats fed the 11.5% CP diet (P < 0.05) and that of isoleucine, serine, cysteine, EAAs, non-essential AAs, and TAAs in the small intestine was increased in goats fed the 10.0% CP diet (P < 0.05). When compared with goats fed the control diet, the relative richness of Bacteroidetes and Fibrobacteres was increased and that of Proteobacteria and Synergistetes was decreased in the rumen of goats fed a diet with 10.0% CP. In conclusion, reducing dietary CP content reduced N excretion and increased nutrient utilization by improving rumen fermentation, enhancing nutrient digestion and absorption, and altering rumen microbiota in growing goats.

Keywords

low-protein dietnitrogen excretionamino acidssmall intestinesruminants
Type
Research Article
Information
animal , Volume 14 , Issue 10 , October 2020 , pp. 2063 - 2073
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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Footnotes

*

These two authors contributed equally to this work.

References

Agricultural Research Council (ARC) 1984. The nutrient requirements of ruminants. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, UK.Google Scholar
Association of Official Analytical Chemists (AOAC) 1990. Official methods of analysis, 15th edition. AOAC, Arlington, VA, USA.Google Scholar
Atti, N, Rouissi, H and Mahouachi, M 2004. The effect of dietary crude protein level on growth, carcass and meat composition of male goat kids in Tunisia. Small Ruminant Research 54, 89–97.CrossRefGoogle Scholar
Broderick, GA, Stevenson, MJ, Patton, RA, Lobos, NE and Olmos Colmenero, JJ 2008. Effect of supplementing rumen-protected methionine on production and nitrogen excretion in lactating dairy cows. Journal of Dairy Science 91, 1092–1102.CrossRefGoogle ScholarPubMed
Bush, RS, Toullec, R, Caugant, I and Guilloteau, P 1992. Effects of raw pea flour on nutrient digestibility and immune responses in the preruminant calf. Journal of Dairy Science 75, 3539–3552.CrossRefGoogle ScholarPubMed
Chen, JC, Xu, QQ, Li, YX, Tan, ZR, Sun, WZ, Zhang, XX, Sun, JJ and Sun, ZH 2019. Comparative effects of supplementing diets with sodium butyrate, medium-chain fatty acids, and n-3 polyunsaturated fatty acids during late pregnancy and lactation on the reproductive performance of sows and growth performance of suckling piglets. Journal of Animal Science 97, 4256–4267.CrossRefGoogle Scholar
Cowieson, AJ and Bedford, MR 2009. The effect of phytase and carbohydrase on ileal amino acid digestibility in monogastric diets: complimentary mode of action? World Poultry Science Journal 2009, 609–624.CrossRefGoogle Scholar
Dewhurst, RJ, Davies, DR and Merry, RJ 2000. Microbial protein supply from the rumen. Animal Feed Science and Technology 85, 1–21.CrossRefGoogle Scholar
Dutta, TK, Agnihotri, MK, Sahoo, PK, Rajkumar, V and Das, AK 2009. Effect of different protein-energy ratio in pulse by-product and residue based pelleted feeds on growth, rumen fermentation, carcass and sausage quality in Barbari kids. Small Ruminant Research 85, 34–41.CrossRefGoogle Scholar
Edgar, RC 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle ScholarPubMed
Galassi, G, Colombini, S, Malagutti, L, Crovetto, GM and Rapetti, L 2010. Effects of high fibre and low protein diets on performance, digestibility, nitrogen excretion and ammonia emission in the heavy pig. Animal Feed Science and Technology 16, 1140–1148.Google Scholar
Gallo, L, Montà, GD, Carraro, L, Cecchinato, A, Carnier, P and Schiavon, S 2014. Growth performance of heavy pigs fed restrictively diets with decreasing crude protein and indispensable amino acids content. Livestock Science 61, 130–138.CrossRefGoogle Scholar
Henke, A, Dickhoefer, U, Westreicher-Kristen, E, Knappstein, K, Molkentin, J, Hasler, M and Susenbeth, A 2017. Effects of quebra chotannin extract on feed intake, digestibility, excretion of urinary purine derivatives and milk production in lactating dairy cows. Archives of Animal Nutrition 71, 37–53.CrossRefGoogle Scholar
Hu, WL, Liu, JX, Ye, JA, Wu, YM and Guo, YQ 2005. Effect of tea saponin on rumen fermentation in vitro. Animal Feed Science and Technology 120, 333–339.CrossRefGoogle Scholar
Hwangbo, S, Choi, SH, Kim, SW, Son, DS, Park, HS, Lee, SH and Jo, IH 2009. Effects of crude protein levels in total mixed rations on growth performance and meat quality in growing Korean Black goats. Asian-Australasian Journal of Animal Sciences 22, 1133–1139.CrossRefGoogle Scholar
Knapp, JR, Laur, GL, Vadas, PA, Weiss, WP and Tricarico, JM 2014. Invited review: enteric methane in dairy cattle production: quantifying the opportunities and impact of reducing emissions. Journal of Dairy Science 97, 3231–3261.CrossRefGoogle ScholarPubMed
Larsbrink, J, Rogers, TE, Hemsworth, GR, McKee, LS, Tauzin, AS, Spadiut, O, Klinter, S, Pudlo, NA, Urs, K, Koropatkin, NM, Creagh, AL, Haynes, CA, Kelly, AG, Cederholm, SN, Davies, GJ, Martens, EC and Brumer, H 2014. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506, 498–502.CrossRefGoogle ScholarPubMed
Lee, C, Hristov, AN, Dell, CJ, Feyereisen, GW, Kaye, J and Beegle, D 2012. Effect of dietary protein concentration on ammonia and greenhouse gas emitting potential of dairy manure. Journal of Dairy Science 95, 1930–1941.CrossRefGoogle ScholarPubMed
Li, Y, Li, F, Duan, Y, Guo, Q, Wang, W, Wen, C, Wen, C, Huang, X and Yin, Y 2017. The protein and energy metabolic response of skeletal muscle to the low-protein diets in growing pigs. Journal of Agricultural and Food Chemistry 65, 8544–8551.CrossRefGoogle ScholarPubMed
Li, YX, Tang, ZR, Li, TJ, Chen, C, Huang, FR, Yang, J, Xu, QQ, Zhen, JF, Wu, ZL, Li, M, Sun, JJ, Chen, JC, Zhang, XX, An, R, Zhao, SJ, Jiang, QY, Zhu, WY, Yin, YL and Sun, ZH 2018. Pyruvate is an effective substitute for glutamate in regulating porcine nitrogen excretion. Journal of Animal Science 96, 3804–3814.CrossRefGoogle ScholarPubMed
Mcdonald, P 2002. Animal nutrition. Pearson Education, Prentice Hall, Harlow, UK.Google Scholar
Magoc, T and Salzberg, SL 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 1978. Nutrient requirements of dairy cattle, 5th edition. National Academy Press, Washington, DC, USA.Google Scholar
National Research Council (NRC) 2001. Nutrient requirements of dairy cattle, 7th edition. National Academy Press, Washington, DC, USA.Google Scholar
National Research Council (NRC) 2007. Nutrient requirements of small ruminants, sheep, goats, cervids, and new world camelids. National Academy Press, Washington, DC, USA.Google Scholar
Negesse, T, Rodehutscord, M and Pfeffer, E 2001. The effect of dietary crude protein level on intake, growth, protein retention and utilization of growing male Saanen kids. Small Ruminant Research 39, 243–251.CrossRefGoogle ScholarPubMed
Pan, L, Ma, XK, Wang, HL, Xu, X, Zeng, ZK, Tian, QY, Zhao, PF, Zhang, S, Yang, ZY and Piao, XS 2015. Enzymatic feather meal as an alternative animal protein source in diets for nursery pigs. Animal Feed Science and Technology 212, 112–121.CrossRefGoogle Scholar
Ravachol, J, de Philip, P, Borne, R, Mansuelle, P, Maté, MJ, Perret, S and Fierobe, HP 2016. Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum. Scientific Reports 6, 22770.CrossRefGoogle ScholarPubMed
Reynal, SM and Broderick, GA 2005. Effect of dietary level of rumen-degraded protein on production and nitrogen metabolism in lactating dairy cows. Journal of Dairy Science 88, 4045–4064.CrossRefGoogle ScholarPubMed
Reynolds, CK and Kristensen, NB 2007. Nitrogen recycling through the gut and the nitrogen economy of ruminants: an asynchronous symbiosis. Journal of Animal Science 86, E293–E305.CrossRefGoogle ScholarPubMed
Rhine, ED, Sims, GK, Mulvaney, RL and Pratt, EJ 1998. Improving the Berthelot reaction for determining ammonium in soil extracts and water. Soil Science Society of America Journal 62, 473–480.CrossRefGoogle Scholar
Savari, M, Khorvash, M, Amanlou, H, Ghorbani, GR, Ghasemi, E, Mirzaei, M. 2018. Effects of rumen-degradable protein: rumen -undegradable protein ratio and corn processing on production performance, nitrogen efficiency, and feeding behavior of Holstein dairy cows. Journal of Dairy Science 101, 1–12.CrossRefGoogle ScholarPubMed
Schloss, PD, Westcott, SL, Ryabin, T, Hall, JR, Hartmann, M, Hollister, EB, Lesniewski, RA, Oakley, BB, Parks, DH, Robinson, CJ, Sahl, JW, Stres, B, Thallinger, GG, Van Horn, DJ and Weber, CF 2009. Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.CrossRefGoogle Scholar
Schulz, F, Westreicher-Kristen, E, Knappstein, K, Molkentin, J and Susenbeth, A 2018. Replacing maize silage plus soybean meal with red clover silage plus wheat in diets for lactating dairy cows. Journal of Dairy Science 101, 1216–1226.CrossRefGoogle ScholarPubMed
Shabi, Z, Arieli, A, Bruckental, I, Aharoni, Y, Zamwel, S, Bor, A and and Tagari, H 1998. Effect of synchronization of the degradation of dietary crude protein and organic matter and feeding frequency on ruminal fermentation and flow of digesta in the abomasum of dairy cows. Journal of Dairy Science 81, 1991–2000.CrossRefGoogle ScholarPubMed
Shriver, JA, Carter, SD, Sutton, AL, Richert, BT and Senne, BW 2003. Effects of adding fiber sources to reduced-crude protein, amino acid-supplemented diets on nitrogen excretion, growth performance, and carcass traits of finishing pigs. Journal of Animal Science 81, 492–502.CrossRefGoogle ScholarPubMed
Silva, AL, Detmann, E, Dijkstra, J, Pedroso, AM, Silva, LHP, Machado, AF, Sousa, FC, dos Santos, GB and Marcondes, MI 2018. Effects of rumen-undegradable protein on intake, performance, and mammary gland development in prepubertal and pubertal dairy heifers. Journal of dairy science 101, 5991–6001.CrossRefGoogle ScholarPubMed
Stevens, EJ, Thomson, GG and O’Connor, KF 1985. A modified procedure for esophageal fistulation of sheep. Journal of Range Management 38, 88–90.CrossRefGoogle Scholar
Sun, ZH, Tan, ZL, Yao, JH, Tang, ZR, Shan, JG, Hu, JP, Tang, SX and Jiang, YM 2007a. Effects of intra-duodenal provison of limiting amino acids on serum concentrations of immunoglobulins and tissue concentrations of DNA and RNA in growing goats fed a maize stover-based diet. Small Ruminant Research 69, 159–166.CrossRefGoogle Scholar
Sun, ZH, Tan, ZL, Liu, SM, Tayo, GO, Lin, B, Teng, B, Tang, SX, Wang, WJ, Liao, YP, Pan, YF, Wang, JR, Zhao, XG and Hu, Y 2007b. Effects of dietary methionine and lysine sources on nutrient digestion, nitrogen utilization, and duodenal amino acid flow in growing goats. Journal of Animal Science 85, 3340–3347.CrossRefGoogle ScholarPubMed
Tamminga, S 1996. A review on environmental impacts of nutritional strategies in ruminants. Journal of Animal Science 74, 3112–3124.CrossRefGoogle ScholarPubMed
Van Soest, PJ, Robertson, JB and 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.CrossRefGoogle ScholarPubMed
Walker, AW, Ince, J, Duncan, SH, Webster, LM, Holtrop, G, Ze, X, Brown, D, Stares, MD, Scott, P, Bergerat, A, Louis, P, McIntosh, F, Johnstone, AM, Lobley, GE, Parkhill, J and Flint, HJ 2011. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. Isme Journal 5, 220–230.CrossRefGoogle ScholarPubMed
Wang, C, Liu, Q, Guo, G, Huo, WJ, Liang, Y, Pei, CX, Zhang, SL, Yang, WZ and Wang, H 2017. Effects of different dietary protein levels and rumen-protected folic acid on ruminal fermentation, degradability, bacterial populations and urinary excretion of purine derivatives in beef steers. Journal of Agricultural Science 155, 1477–1486.CrossRefGoogle Scholar
Wang, Q, Garrity, GM, Tiedje, JM and Cole, JR 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267.CrossRefGoogle ScholarPubMed
Williams, CH, David, DJ and Iismaa, O 1962. The determination of chromic oxide in faeces samples by atomic absorption spectrophotometry. Journal of Agricultural Science 59, 381–385.CrossRefGoogle Scholar
Wu, LT, Zhang, XX, Tang, ZR, Li, YX, Li, TJ, Xu, QQ, Zhen, JF, Huang, FR, Yang, J, Chen, C, Wu, ZL, Li, M, Sun, JJ, Chen, JC, An, R, Zhao, SJ, Jiang, QY, Zhu, WY, Yin, YL and Sun, ZH 2018. Low-protein diets decrease porcine nitrogen excretion but with restrictive effects on amino acid utilization. Journal of Agricultural and Food Chemistry 66, 8262–8271.CrossRefGoogle ScholarPubMed
Yang, CT, Si, BW, Diao, QY, Jin, H, Zeng, SQ and Tu, Y 2016. Rumen fermentation and bacterial communities in weaned chahaer lambs on diets with different protein levels. Journal of Integrative Agriculture 15, 1564–1574.CrossRefGoogle Scholar
Zhang, S, Chu, L, Qiao, S, Mao, X and Zeng, X 2016. Effects of dietary leucine supplementation in low crude protein diets on performance, nitrogen balance, whole-body protein turnover, carcass characteristics and meat quality of finishing pigs. Animal Science Journal 87, 911–920.CrossRefGoogle ScholarPubMed