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Influence of ionophores and energy inhibitors on peptide metabolism by rumen bacteria

Published online by Cambridge University Press:  27 March 2009

R. J. Wallace
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB, UK
C. J. Newbold
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB, UK
N. McKain
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB, UK

Summary

Ionophores and inhibitors of bacterial energy metabolism were added to mixed rumen bacteria prepared from sheep receiving grass hay plus concentrate diets, and their influence on the rate of metabolism of alanine (Ala) peptides was determined. Dicyclohexylcarbodiimide (DCCD) had no influence on the rate of breakdown of Ala2, Ala3, Ala4 or Ala5, indicating that the metabolism of these peptides did not require ATP. The protonophores tetrachlorosalicylanilide (TCS) and carbonyl cyanide m-chlorophenyl-hydrazone (CCCP) inhibited peptide breakdown to a minor extent (< 15%), whereas the ionophores monensin and tetronasin had greater, but still small (12–31%), inhibitory effects. Toluene stimulated peptide breakdown, consistent with a permeability barrier having been removed. Thus, at least some peptide metabolism depends on transport into bacteria; transport appears not to be ATP-linked, and may well be coupled to the uptake of mineral cations rather than protons. Rumen fluid from sheep receiving a similar diet with added monensin (33 mg/kg) or tetronasin (10 mg/kg) hydrolysed Ala3 and Ala4 at rates that did not differ significantly from controls. Nevertheless, the peak concentration of free peptides in rumen fluid after feeding was more than doubled in ionophore-fed sheep, and peptides persisted for longer than in control animals.

Type
Animals
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Bladen, H. A., Bryant, M. P. & Doetsch, R. N. (1961). A study of bacterial species from the rumen which produce ammonia from protein hydrolyzate. Applied Microbiology 9, 175180.CrossRefGoogle ScholarPubMed
Booth, I. R. (1988). Bacterial transport: energetics and mechanisms. In Bacterial Energy Transduction (Ed. Anthony, C.), pp. 377428. London: Academic Press.Google Scholar
Broderick, G. A. & Wallace, R. J. (1988). Effects of dietary nitrogen source on concentrations of ammonia, free amino acids and fluorescamine-reactive peptides in the sheep rumen. Journal of Animal Science 66, 22332238.CrossRefGoogle Scholar
Broderick, G. A., Wallace, R. J. & McKain, N. (1988). Uptake of small neutral peptides by mixed rumen microorganisms in vitro. Journal of the Science of Food and Agriculture 42, 109118.CrossRefGoogle Scholar
Chen, G. & Russell, J. B. (1989). More monensin-sensitive, ammonia-producing bacteria from the rumen. Applied and Environmental Microbiology 55, 10521057.CrossRefGoogle ScholarPubMed
Chen, G., Russell, J. B. & Sniffen, C. J. (1987 a). A procedure for measuring peptides in rumen fluid and evidence that peptide uptake can be a rate-limiting step in ruminal protein degradation. Journal of Dairy Science 70, 12111219.CrossRefGoogle ScholarPubMed
Chen, G., Sniffen, C. J. & Russell, J. B. (1987 b). Concentration and estimated flow of peptides from the rumen of dairy cattle: effects of protein quantity, protein solubility, and feeding frequency. Journal of Dairy Science 70, 983992.CrossRefGoogle ScholarPubMed
Chen, M. & Wolin, M. J. (1979). Effect of monensin and lasalocid-sodium on the growth of methanogenic and rumen saccharolytic bacteria. Applied and Environmental Microbiology 38, 7277.CrossRefGoogle ScholarPubMed
Dinius, D.A., Simpson, M. S. & Marsh, P. B. (1976). Effect of monensin fed with forage on digestion and the ruminal ecosystem of steers. Journal of Animal Science 42, 229234.CrossRefGoogle Scholar
Hanson, T. L. & Klopfenstein, T. (1979). Monensin, protein source and protein levels for growing steers. Journal of Animal Science 48, 474479.CrossRefGoogle Scholar
Henderson, C., Stewart, C. S. & Nekrep, F. V. (1981). The effect of monensin on pure and mixed cultures of rumen bacteria. Journal of Applied Bacteriology 51, 159169.CrossRefGoogle Scholar
Jones, C. W. (1988). Membrane-associated energy conservation in bacteria: a general introduction. In Bacterial Energy Transduction (Ed. Anthony, C.), pp. 182. London: Academic Press.Google Scholar
Jouany, J. P. & Senaud, J. (1979). Defaunation du rumen de mouton. Annales de Biologie Animate, Biochimie el Biophysique 19, 619624.CrossRefGoogle Scholar
Newbold, C. J. & Wallace, R. J. (1989). Changes in the rumen bacterium, Bacteroides ruminicola, grown in the presence of the ionophore, tetronasin. Asian-Australasian Journal of Animal Science 2, 452453.CrossRefGoogle Scholar
Newbold, C. J., Wallace, R. J., Watt, N. D. & Richardson, A. J. (1988). Effect of the novel ionophore tetronasin (ICI 139603) on ruminal micro-organisms. Applied and Environmental Microbiology 54, 544547.CrossRefGoogle Scholar
Newbold, C. J., McKain, N. & Wallace, R. J. (1989). The role of protozoa in ruminal peptide metabolism. In Biochemistry and Physiology of Anaerobic Protozoa (Eds Lloyd, D., Coombs, G. H. & Paget, T. A. P.), pp. 4255. London: Harwood Academic Publishers.Google Scholar
Newbold, C. J., Wallace, R. J. & McKain, N. (1990). Effect of the ionophore tetronasin on nitrogen metabolism of rumen microorganisms in vitro. Journal of Animal Sciences, 11031109.CrossRefGoogle ScholarPubMed
Owens, F. N., Shockey, R. W., Fent, R. W. & Rust, S. R. (1978). Monensin and abomasal passage of steers. Journal of Animal Science 47 (Suppl. I), 114.Google Scholar
Payne, J. W. (1980). Transport and utilisation of peptides by bacteria. In Microorganisms and Nitrogen Sources (Ed. Payne, J. W.), pp. 211256. Chichester: Wiley.Google Scholar
Payne, J. W. (1983). Peptide transport in bacteria: methods, mutants and energy coupling. Biochemical Society Transactions 11, 794798.CrossRefGoogle ScholarPubMed
Poos, M. I., Hanson, T. L. & Klopfenstein, T. J. (1979). Monensin effects on diet digestibility, ruminal protein bypass and microbial protein synthesis. Journal of Animal Science 48, 15161524.CrossRefGoogle ScholarPubMed
Rowe, J. B., Davies, A. & Broome, A. W. J. (1983). Effect of the novel ionophore ICI 139603 on nitrogen digestion in sheep. In Proceedings of the IVth International Symposium. Protein Metabolism and Nutrition, pp. 259262. No. 16. Paris: Institut National de la Recherche Agronomique.Google Scholar
Russell, J. B. & Martin, S. A. (1984). Effects of various methane inhibitors on the fermentation of amino acids by mixed rumen microorganisms in vitro. Journal of Animal Science 59, 13291338.CrossRefGoogle Scholar
Russell, J. B., Strobel, H. J. & Chen, G. (1988). Enrichment and isolation of a ruminal bacterium with a very high specific activity of ammonia production. Applied and Environmental Microbiology 54, 872877.CrossRefGoogle ScholarPubMed
Sauer, F. D. & Teather, R. M. (1987). Changes in oxidation reduction potentials and volatile fatty acid production by rumen bacteria when methane synthesis is inhibited. Journal of Dairy Science 70, 18351840.CrossRefGoogle ScholarPubMed
Van Boven, A. & Konings, W. N. (1986). The uptake of peptides by microorganisms. Netherlands Milk and Dairy Journal 40, 117127.Google Scholar
Van Nevel, C. J. & Demeyer, D. I. (1977). Effect of monensin on rumen metabolism in vitro. Applied and Environmental Microbiology 34, 251257.CrossRefGoogle ScholarPubMed
Wallace, R. J. & McKain, N. (1989 a). Analysis of peptide metabolism by ruminal microorganisms. Applied and Environmental Microbiology 55, 23722376.CrossRefGoogle ScholarPubMed
Wallace, R. J. & McKain, N. (1989 b). Some observations on the susceptibility of peptides to degradation by rumen microorganisms. Asian-Australasian Journal of Animal Sciences 2, 333335.CrossRefGoogle Scholar
Wallace, R. J. & McKain, N. (1990). A comparison of methods for determining the concentration of extracellular peptides in rumen fluid of sheep. Journal of Agricultural Science, Cambridge 114, 101105.CrossRefGoogle Scholar
Wallace, R. J., Czerkawski, J. W. & Breckenridge, G. (1981). Effect of monensin on the fermentation of basal rations in the rumen simulation technique (Rusitec). British Journal of Nutrition 46, 131148.CrossRefGoogle ScholarPubMed
Wallace, R. J., McKain, N.Newbold, C. J. (1990). Metabolism of small peptides in rumen fluid. Accumulation of intermediates during hydrolysis of alanine oligomers, and comparison of peptidolytic activities of bacteria and protozoa. Journal of the Science of Food and Agriculture 50, 191199.CrossRefGoogle Scholar
Whetstone, H. D., Davis, C. L. & Bryant, M. P. (1981). Effect of monensin on breakdown of protein by ruminal microorganisms in vitro. Journal of Animal Science 53, 803809.CrossRefGoogle ScholarPubMed