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Comparative metabolome analysis of ruminal changes in Holstein dairy cows fed low- or high-concentrate diets

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Abstract

Introduction

Currently, information on the comprehensive changes in the ruminal metabolites of dairy cows fed high-concentrate diet is limited.

Objectives

This study aimed to compare the composition of whole-ruminal metabolites in dairy cows that were fed a low concentrate diet or a high concentrate diet using modern metabolome analysis.

Methods

Cows were fed a low-concentrate diet (LC; 40% concentrate feeds, dry matter (DM) basis) or a high-concentrate diet (HC; 70% concentrate feeds, DM basis). GC/MS was used to analyze rumen fluid samples.

Results

As compared with the LC group, HC diet significantly increased the concentration of bacterial degradation products (included xanthine, hypoxanthine, uracil, etc.), some toxic compounds (included lipopolysaccharide, biogenic amines, ethanolamine, etc.) and 15 amino acids (included alanine, leucine, glycine, etc.). The enrichment analysis of differentially expressed metabolites indicated that three pathways, including aminoacyl-tRNA biosynthesis; phenylalanine, tyrosine, and tryptophan biosynthesis; and valine, leucine and isoleucine biosynthesis, were significantly enriched after the diet treatments. Correlation network analysis revealed that HC diets altered the ruminal metabolic pattern, and the metabolites in the HC group were more complicated than those in the LC group. The correlations between ruminal metabolites and blood parameters were mainly centralized in the ruminal metabolites and albumin (40 metabolites), followed by globulin (18 metabolites) and total protein (6 metabolites).

Conclusions

These findings revealed that HC feeding altered the concentrations of ruminal metabolites as well as the metabolic pattern, and the rumen metabolism could be reflected by blood metabolism to a certain degree.

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References

  • Aschenbach, J. R., & Gäbel, G. (2000). Effect and absorption of histamine in sheep rumen: significance of acidotic epithelial damage. Journal of Animal Science, 78, 464–470.

    Article  CAS  PubMed  Google Scholar 

  • Atasoglu, C., Valdés, C., Walker, N. D., Newbold, C. J., & Wallace, R. J. (1998). De novo synthesis of amino acids by the ruminal bacteria Prevotella bryantii B14, Selenomonas ruminantium HD4, and Streptococcus bovis ES1. Applied Environmental Microbiology, 64, 2836–2843.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey, S. R., Marr, C. M., & Elliott, J. (2003). Identification and quantification of amines in the equine caecum. Research in Veterinary Science, 74, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Bastian, M., Heymann, S., & Jacomy, M. (2009). Gephi: an open source software for exploring and manipulating networks. Proceedings of the Third International ICWSM Conference, 8, 361–362.

    Google Scholar 

  • Beauchemin, K. A., Yang, W. Z., & Rode, L. M. (2003). Effects of particle size of alfalfa-based dairy cow diets on chewing activity, ruminal fermentation, and milk production. Journal of Dairy Science, 86, 630–643.

    Article  CAS  PubMed  Google Scholar 

  • Bergsten, C. (2003). Causes, risk factors, and prevention of laminitis and related claw lesions. Acta Veterinaria Scand Inavica, Suppl, 98, 157–166.

    Article  CAS  Google Scholar 

  • Bertram, H. C., Kristensen, N. B., Malmendal, A., Nielsen, N. C., Bro, R., & Andersen, H. J. (2005). A metabolomic investigation of splanchnic metabolism using 1 H NMR spectroscopy of bovine blood plasma. Analytica Chimica Acta, 536, 1–6.

    Article  CAS  Google Scholar 

  • Dain, J. A., Neal, A. L., & Dougherty, R. W. (1955). The occurrence of histamine and tyramine in rumen ingesta of experimentally over-fed sheep. Journal of Animal Science, 14, 930–935.

    Article  CAS  Google Scholar 

  • Doweiko, J. P., & Nompleggi, D. J. (1991). Reviews: Role of albumin in human physiology and pathophysiology. Journal of Parenteral and Enteral Nutrition, 15, 207–211.

    Article  CAS  PubMed  Google Scholar 

  • Fernando, S. C., Purvis, H. T., Najar, F. Z., Sukharnikov, L. O., Krehbiel, C. R., Nagaraja, T. G., et al. (2010). Rumen microbial population dynamics during adaptation to a high-grain diet. Applied Environmental Microbiology, 76, 7482–7490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghorbani, G. R., Morgavi, D. P., Beauchemin, K. A., & Leedle, J. A. (2002). Effects of bacterial direct-fed microbials on ruminal fermentation, blood variables, and the microbial populations of feedlot cattle. Journal of Animal Science, 80, 1977–1985.

    Article  CAS  PubMed  Google Scholar 

  • Goad, D. W., Goad, C. L., & Nagaraja, T. G. (1998). Ruminal microbial and fermentative changes associated with experimentally induced subacute acidosis in steers. Journal of Animal Science, 76, 234–241.

    Article  CAS  PubMed  Google Scholar 

  • Gozho, G. N., Krause, D. O., & Plaizier, J. C. (2006). Rumen lipopolysaccharide and inflammation during grain adaptation and subacute ruminal acidosis in steers. Journal of Dairy Science, 89, 4404–4413.

    Article  CAS  PubMed  Google Scholar 

  • Gozho, G. N., Krause, D. O., & Plaizier, J. C. (2007). Ruminal lipopolysaccharide concentration and inflammatory response during grain-induced subacute ruminal acidosis in dairy cows. Journal of Dairy Science, 90, 856–866.

    Article  CAS  PubMed  Google Scholar 

  • Kajikawa, H., Mitsumori, M., & Ohmomo, S. (2002). Stimulatory and inhibitory effects of protein amino acids on growth rate and efficiency of mixed ruminal bacteria. Journal of Dairy Science, 85, 2015–2022.

    Article  CAS  PubMed  Google Scholar 

  • Kawai, K., Fujita, M., & Nakoto, M. (1974). Lipid components of two different regions of an intestinal epithelial cell membrane of mouse. Biochimica et Biophysica Acta (BBA)-Lipids and Lipid Metabolism, 369, 222–233.

    Article  CAS  Google Scholar 

  • Khafipour, E., Li, S., Plaizier, J. C., & Krause, D. O. (2009). Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Applied and Environmental Microbiology, 75, 7115–7124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kind, T., Wohlgemuth, G., Lee, D. Y., Lu, Y., Palazoglu, M., Shahbaz, S., et al. (2009). FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Analytical Chemistry, 81, 10038–10048.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleen, J. L., Hooijer, G. A., Rehage, J., & Noordhuizen, J. P. (2003). Subacute ruminal acidosis (SARA): A review. Journal of Veterinary Medicine Series A-Physiology Pathology Clinical Medicine, 50, 406–414.

    Article  CAS  Google Scholar 

  • Kuwahata, M., & Kido, Y. (2015). Branched chain amino acid supplementation and plasma albumin. In Branched chain amino acids in clinical nutrition. pp. 159–168. Springer: New York

    Google Scholar 

  • Maclean, C. W. (1970). The haematology of bovine laminitis. Veterinary Record, 86, 710–714.

    Article  CAS  PubMed  Google Scholar 

  • Mao, S. Y., Zhang, R. Y., Wang, D. S., & Zhu, W. Y. (2013). Impact of subacute ruminal acidosis (SARA) adaptation on rumen microbiota in dairy cattle using pyrosequencing. Anaerobe, 24, 12–19.

    Article  CAS  PubMed  Google Scholar 

  • McAllan, A. (1982). The fate of nucleic acids in ruminants. Proceedings of the Nutrition Society, 41, 309–316.

    Article  CAS  PubMed  Google Scholar 

  • McAllan, A., & Smith, R. (1973). Degradation of nucleic acids in the rumen. British Journal of Nutrition, 29, 331–345.

    Article  CAS  PubMed  Google Scholar 

  • Minnikin, D. E., Abdolrahimzadeh, H., & Baddiley, J. (1971). The interrelation of phosphatidylethanolamine and glycosyl diglycerides in bacterial membranes. Biochemical Journal, 124, 447–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moco, S., & Ross, A. B. (2015). Can we use metabolomics to understand changes to gut microbiota populations and function? A nutritional perspective. In Metabonomics and gut microbiota in nutrition and disease (pp. 83–108). London: Springer.

    Google Scholar 

  • Motoi, Y., Obara, Y., & Shimbayashi, K. (1984). Changes in histamine concentration of ruminal contents and plasma in cattle fed on a formula feed and rolled barley. The Japanese Journal of Veterinary Science, 46, 309–314.

    Article  CAS  PubMed  Google Scholar 

  • Nocek, J. E., & Tamminga, S. (1991). Site of digestion of starch in the gastrointestinal tract of dairy cows and its effect on milk yield and composition. Journal of Dairy Science, 74, 3598–3629.

    Article  CAS  PubMed  Google Scholar 

  • Phuntsok, T., Froetschel, M. A., Amos, H. E., Zheng, M., & Huang, Y. W. (1998). Biogenic amines in silage, apparent postruminal passage, and the relationship between biogenic amines and digestive function and intake by steers. Journal of Dairy Science, 81, 2193–2203.

    Article  CAS  PubMed  Google Scholar 

  • Razzaque, M. A., & Topps, J. H. (1972). Utilization of dietary nucleic-acids by sheep. Proceedings of the Nutrition Society, 31, A105–A106.

    Google Scholar 

  • Rodríguez, C. A., González, J., Alvir, M. R., Repetto, J. L., Centeno, C., & Lamrani, F. (2000). Composition of bacteria harvested from the liquid and solid fractions of the rumen of sheep as influenced by feed intake. British Journal of Nutrition, 84, 369–376.

    PubMed  Google Scholar 

  • Rothschild, M. A., Oratz, M., & Schreiber, S. S. (1972). Albumin synthesis. New England Journal of Medicine, 286, 816–821.

    Article  CAS  PubMed  Google Scholar 

  • Rothschild, M. A., Oratz, M., & Schreiber, S. S. (1973). Albumin metabolism. Gastroenterology, 64, 324–337.

    CAS  PubMed  Google Scholar 

  • Russell, J. B., & Rychlik, J. L. (2001). Factors that alter rumen microbial ecology. Science, 292, 1119–1122.

    Article  CAS  PubMed  Google Scholar 

  • Saleem, F., Ametaj, B. N., Bouatra, S., Mandal, R., Zebeli, Q., Dunn, S. M., et al. (2012). A metabolomics approach to uncover the effects of grain diets on rumen health in dairy cows. Journal of Dairy Science, 95, 6606–6623.

    Article  CAS  PubMed  Google Scholar 

  • Saleem, F., Bouatra, S., Guo, A. C., Psychogios, N., Mandal, R., Dunn, S. M., et al. (2013). The bovine ruminal fluid metabolome. Metabolomics, 9, 360–378.

    Article  CAS  Google Scholar 

  • Sauer, F. D., Erfle, J. D., & Mahadevan, S. (1975). Amino acid biosynthesis in mixed rumen cultures. Biochemical Journal, 150, 357–372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia, J., Psychogios, N., Young, N., & Wishart, D. S. (2009). MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Research., 37, W652–W660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, R., Zhu, W., & Mao, S. (2016). High-concentrate feeding upregulates the expression of inflammation-related genes in the ruminal epithelium of dairy cattle. Journal of Animal Science and Biotechnology, 7, 42.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, S., Zhao, J., Bu, D., Sun, P., Wang, J., & Dong, Z. (2014). Metabolomics analysis reveals large effect of roughage types on rumen microbial metabolic profile in dairy cows. Letters in Applied Microbiology, 59, 79–85.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by the Open Project of Beijing Key Laboratory of Dairy Cow Nutrition, Beijing University of Agriculture, China.

Author contributions

The authors’ contributions are as follows: RZ carried out the majority of the animal studies including animal care, sample collection and the measurements of ruminal parameters. RZ and SM carried out data interpretation and manuscript preparation. SM, LJ. and WZ were responsible for the conception of the project and the oversight of the experiment.

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Correspondence to Shengyong Mao.

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Zhang, R., Zhu, W., Jiang, L. et al. Comparative metabolome analysis of ruminal changes in Holstein dairy cows fed low- or high-concentrate diets. Metabolomics 13, 74 (2017). https://doi.org/10.1007/s11306-017-1204-0

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