Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T04:59:10.017Z Has data issue: false hasContentIssue false
  • English
  • Français

Response of rumen microbiota, and metabolic profiles of rumen fluid, liver and serum of goats to high-grain diets

Published online by Cambridge University Press:  07 January 2019

R. Y. Zhang ,
Y. J. Liu ,
Y. Y. Yin ,
W. Jin ,
S. Y. Mao  and
J. H. Liu
R. Y. Zhang
Affiliation:
Key Laboratory of Zoonosis of Liaoning Province, College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang 110866, China
Y. J. Liu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Y. Y. Yin
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
W. Jin
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
S. Y. Mao
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
J. H. Liu*
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
*
†E-mail: [email protected]
Get access

Abstract

Feeding ruminants a high-grain (HG) diet is a widely used strategy to improve milk yield and cost efficiency. However, it may cause certain metabolic disorders. At present, information about the effects of HG diets on the systemic metabolic profile of goats and the correlation of such diets with rumen bacteria is limited. In the present study, goats were randomly divided into two groups: one was fed the hay diet (hay; n = 5), while the other was fed HG diets (HG; n = 5). On day 50, samples of rumen contents, peripheral blood serum and liver tissues were collected to determine the metabolic profiles in the rumen fluid, liver and serum and the microbial composition in rumen. The results revealed that HG diets reduced (P < 0.05) the community richness and diversity of rumen microbiota, with an increase in the Chao 1 and Shannon index and a decrease in the Simpson index. HG diets also altered the composition of rumen microbiota, with 30 genera affected (P < 0.05). Data on the metabolome showed that the metabolites in the rumen fluid, liver and serum were affected (variable importance projection > 1, P <0.05) by dietary treatment, with 47, 10 and 27 metabolites identified as differentially metabolites. Pathway analysis showed that the common metabolites in the shared key pathway (aminoacyl-transfer RNA biosynthesis) in the rumen fluid, liver and serum were glycine, lysine and valine. These findings suggested that HG diets changed the composition of the rumen microbiota and metabolites in the rumen fluid, liver and serum, mainly involved in amino acid metabolism. Our findings provide new insights into the understanding of diet-related systemic metabolism and the effects of HG diets on the overall health of goats.

Keywords

rumenpyrosequencingmetabolomicsamino acidsgoat
Type
Research Article
Information
animal , Volume 13 , Issue 9 , September 2019 , pp. 1855 - 1864
Copyright
© The Animal Consortium 2019 

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.)

Footnotes

a

These two authors contributed equally to this work.

References

Abaker, JA, Xu, TL, Jin, D, Chang, GJ, Zhang, K and Shen, XZ 2017. Lipopolysaccharide derived from the digestive tract provokes oxidative stress in the liver of dairy cows fed a high-grain diet. Journal of Dairy Science 100, 666–678.CrossRefGoogle ScholarPubMed
Ametaj, BN, Zebeli, Q, Saleem, F, Psychogios, N, Lewis, MJ, Dunn, SM, Xia, J and Wishart, DS 2010. Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows. Metabolomics 6, 583–594.CrossRefGoogle Scholar
Calder, PC 2006. Branched-chain amino acids and immunity. Journal of Nutrition 136, 288S–293S.CrossRefGoogle ScholarPubMed
Dong, H, Wang, S, Jia, Y, Ni, Y, Zhang, Y, Zhuang, S, Shen, X and Zhao, R 2013. Long-term effects of subacute ruminal acidosis (SARA) on milk quality and hepatic gene expression in lactating goats fed a high-concentrate diet. PLoS One 8, e82850.CrossRefGoogle ScholarPubMed
Dröge, W and Breitkreutz, R 2000. Glutathione and immune function. Proceedings of the Nutrition Society 59, 595–600.CrossRefGoogle ScholarPubMed
Enemark, JM 2009. The monitoring, prevention and treatment of sub-acute ruminal acidosis (SARA): a review. The Veterinary Journal 176, 32–43.CrossRefGoogle Scholar
Faure, M, Choné, F, Mettraux, C, Godin, JP, Béchereau, F, Vuichoud, J, Papet, I, Breuillé, D and Obled, C 2007. Threonine utilization for synthesis of acute phase proteins, intestinal proteins, and mucins is increased during sepsis in rats. Journal of Nutrition 137, 1802–1807.CrossRefGoogle ScholarPubMed
Fernando, SC, Purvis, HT, Najar, FZ, Sukharnikov, LO, Krehbiel, CR, Nagaraja, TG, Roe, BA and Desilva, U 2010. Rumen microbial population dynamics during adaptation to a high-grain diet. Applied and Environmental Microbiology 76, 7482–7490.CrossRefGoogle ScholarPubMed
Geenen, S, Yates, JW, Kenna, JG, Bois, FY, Wilson, ID and Westerhoff, HV 2013. Multiscale modelling approach combining a kinetic model of glutathione metabolism with PBPK models of paracetamol and the potential glutathione-depletion biomarkers ophthalmic acid and 5-oxoproline in humans and rats. Integrative Biology 5, 877–888.CrossRefGoogle ScholarPubMed
Guo, Y, Xu, X, Zou, Y, Yang, Z, Li, S and Cao, Z 2013. Changes in feed intake, nutrient digestion, plasma metabolites, and oxidative stress parameters in dairy cows with subacute ruminal acidosis and its regulation with pelleted beet pulp. Journal of Animal Science and Biotechnology 4, 31.CrossRefGoogle ScholarPubMed
Jiang, XY, Ni, YD, Zhang, SK, Zhang, YS and Shen, XZ 2014. Identification of differentially expressed proteins in liver in response to subacute ruminal acidosis (SARA) induced by high-concentrate diet. Asian-Australasian Journal of Animal Science 27, 1181–1188.CrossRefGoogle ScholarPubMed
Hua, C, Tian, J, Tian, P, Cong, R, Luo, Y, Geng, Y, Tao, S, Ni, Y and Zhao, R 2017. Feeding a high concentration diet induces unhealthy alterations in the composition and metabolism of ruminal microbiota and host response in a goat model. Frontiers in Microbiology 8, 138.CrossRefGoogle Scholar
Kim, SW, Mateo, RD, Yin, YL and Wu, G 2007. Functional amino acids and fatty acids for enhancing production performance of sows and piglets. Asian-Australasian Journal of Animal Science 20, 295–306.CrossRefGoogle Scholar
Kleen, JL and Cannizzo, C 2012. Incidence, prevalence and impact of SARA in dairy herds. Animal Feed Science and Technology 172, 4–8.CrossRefGoogle Scholar
Li, SC 2005. Study on the nitrogen metabolism and limiting amino acids of lactating dairy cows fed diets differing in forage to concentrate ratios. PhD thesis, Chinese Academy of Agricultural Sciences, Beijing, China.Google Scholar
Liu, JH, Xu, TT, Liu, YJ, Zhu, WY and Mao, SY 2013. A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 305, R232–R241.CrossRefGoogle ScholarPubMed
Liu, JH, Xu, TT, Zhu, WY and Mao, SY 2014. A high-grain diet alters the omasal epithelial structure and expression of tight junction proteins in a goat model. The Veterinary Journal 201, 95–100.CrossRefGoogle Scholar
Mao, SY, Huo, WJ and Zhu, WY 2016. Microbiome-metabolome analysis reveals unhealthy alterations in the composition and metabolism of ruminal microbiota with increasing dietary grain in a goat model. Environmental Microbiology 18, 525–541.CrossRefGoogle Scholar
Mao, SY, Zhang, RY, Wang, DS and Zhu, WY 2013. Impact of subacute ruminal acidosis (SARA) adaptation on rumen microbiota in dairy cattle using pyrosequencing. Anaerobe 24, 12–19.CrossRefGoogle ScholarPubMed
Pacheco, D, Tavendale, MH, Reynolds, GW, Barry, TN, Lee, J and McNabb, WC 2003. Whole-body fluxes and partitioning of amino acids to the mammary gland of cows fed fresh pasture at two levels of intake during early lactation. British Journal of Nutrition 90, 271–281.CrossRefGoogle ScholarPubMed
Petri, RM, Forster, RJ, Yang, W, McKinnon, JJ and McAllister, TA 2012. Characterization of rumen bacterial diversity and fermentation parameters in concentrate fed cattle with and without forage. Journal of Applied Microbiology 112, 1152–1162.CrossRefGoogle ScholarPubMed
Plaizier, JC, Krause, DO, Gozho, GN and McBride, BW 2008. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. The Veterinary Journal 176, 21–31.CrossRefGoogle ScholarPubMed
Plaizier, JC, Li, S, Tun, HM and Khafipour, E 2017. Nutritional models of experimentally-induced subacute ruminal acidosis (SARA) differ in their impact on rumen and hindgut bacterial communities in dairy cows. Frontiers in Microbiology 7, 2128.CrossRefGoogle ScholarPubMed
Psychogios, N, Hau, DD, Peng, J, Guo, AC, Mandal, R, Bouatra, S, Sinelnikov, I, Krishnamurthy, R, Eisner, R, Gautam, B, Young, N, Xia, JG, Knox, C, Dong, E, Huang, P, Hollander, Z, Pedersen, L, Smith, TL, Bamforth, SR, Greiner, F, McManus, R, Newman, B, Goodfriend, JW, , T and Wishart, DS 2011. The human serum metabolome. PLoS One 6, e16957.CrossRefGoogle ScholarPubMed
Remond, D, Bernard, L and Poncet, C 2000. Free and peptide amino acid net flux across the rumen and the mesenteric- and portal-drained viscera of sheep. Journal of Animal Science 78, 1960–1972.CrossRefGoogle ScholarPubMed
Ronchi, B, Bernabucci, U, Lacetera, N and Nardone, A 2000. Oxidative and metabolic status of high yielding dairy cows in different nutritional conditions during the transition period. In Proceedings of the 51st Annual Meeting. EAAP, Vienna, Austria, 21–24 August 2000, Wageningen, The Netherlands, 125 pp.Google Scholar
Saleem, F, Ametaj, BN, Bouatra, S, Mandal, R, Zebeli, Q, Dunn, SM and Wishart, DS 2012. A metabolomics approach to uncover the effects of grain diets on rumen health in dairy cows. Journal of Dairy Science 95, 6606–6623.CrossRefGoogle ScholarPubMed
Shen, Z, Seyfert, HM, Löhrke, B, Schneider, F, Zitnan, R, Chudy, A, Kuhla, S, Hammon, HM, Blum, JW, Martens, H, Hagemeister, H and Voigt, J 2004. An energy-rich diet causes rumen papillae proliferation associated with more IGF type 1 receptors and increased plasma IGF-1 concentrations in young goats. Journal of Nutrition 134, 11–17.CrossRefGoogle ScholarPubMed
Shilpa, J, Pretty, MA, Anitha, M and Paulose, CS 2013. Gamma aminobutyric acid B and 5-hydroxy tryptamine 2A receptors functional regulation during enhanced liver cell proliferation by GABA and 5-HT chitosan nanoparticles treatment. European Journal of Pharmacology 715, 154–163.CrossRefGoogle ScholarPubMed
Sugiharto, S, Hedemann, MS and Lauridsen, C 2014. Plasma metabolomic profiles and immune responses of piglets after weaning and challenge with E. coli. Journal of Animal Science and Biotechnology 5, 17.CrossRefGoogle ScholarPubMed
Wang, LF, Jia, SD, Yang, GQ, Liu, RY, Yang, GY, Li, M, Zhu, HS, Wang, YY and Han, LQ 2017. The effects of acute lipopolysaccharide challenge on dairy goat liver metabolism assessed with 1HNMR metabonomics. Journal of Animal Physiology and Animal Nutrition 101, 180–189.CrossRefGoogle Scholar
Wu, G, Bazer, FW, Burghardt, RC, Johnson, GA, Kim, SW, Knabe, DA, Li, P, Li, X, McKnight, JR, Satterfield, MC and Spencer, TE 2011. Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40, 1053–1063.CrossRefGoogle ScholarPubMed
Yamashita, Y, Bowen, WH, Burne, RA and Kuramitsu, HK 1993. Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infection and Immunity 61, 3811–3817.Google ScholarPubMed
Supplementary material: File

Zhang et al. supplementary material

Figures S1-S6 and Tables S1-S4

Download Zhang et al. supplementary material(File)
File 516.7 KB