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An in vivo study of ruminal micro-organisms influencing lactate turnover and its contribution to volatile fatty acid production

Published online by Cambridge University Press:  27 March 2009

R. I. Mackie
Affiliation:
Animal and Dairy Science Research Institute, P/Bag X2, Irene, 1675 Republic of South Africa
Frances M. C. Gilchrist
Affiliation:
Animal and Dairy Science Research Institute, P/Bag X2, Irene, 1675 Republic of South Africa
Suzette Heath
Affiliation:
Animal and Dairy Science Research Institute, P/Bag X2, Irene, 1675 Republic of South Africa

Summary

The ruminal metabolism of lactic acid was investigated in vivo under normal feeding conditions in four sheep each adapted to one of the following diets: high-concentrate, intermediate, high-roughage containing 65, 43 or 10% maize meal and molasses respectively, or lucerne hay. A continuous basal turnover of ruminal lactate (0·01–0·02 mmol/1/min) was found which increased 10- to 40-fold immediately after feeding when production exceeded utilization and lactate accumulated in the rumen. This was followed by an increase in utilization rate which removed the accumulated lactate. Both lactate and glucose turnover were related to the amount of readily fermentable carbohydrate in the diet. Approximately 8, 6·5, 5 and 2·5% of the total VFA was formed through lactate on the high-concentrate, intermediate, high-roughage and lucerne hay diets respectively.

Rumen microbial counts of total culturable, glucolytic, amylolytic and lactateutilizing bacteria, and of ciliate protozoa were also performed on the four sheep. Numbers of micro-organisms in all groups were highest on the high-concentrate diet and lowest on the two roughage diets. The proportions of the predominant genera from the different metabolic groups of bacteria differed, although in most cases the same organisms were present in the rumen on all diets. The succinate pathway was found to be quantitatively more important in the conversion of lactate to propionate in the rumen. Although the numbers of lactate-utilizing bacteria increased as the amount of RFC in the diet increased, their metabolic activity was actually lower. Reasons for this finding are discussed, together with factors influencing the regulation of lactate production and utilization in the rumen.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

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References

Baldwin, R. L., Wood, W. A. & Emery, R. S. (1962). Conversion of lactate-C14 to propionate by the rumen microflora. Journal of Bacteriology 83, 907913.CrossRefGoogle ScholarPubMed
Baldwin, R. L., Wood, W. A. & Emery, R. S. (1963). Conversion of glucose-C14 to propionate by the rumen miorobiota. Journal of Bacteriology 85, 13461349.CrossRefGoogle Scholar
Briggs, P. K., Hogan, J. P. & Reid, J. L. (1957). The effect of volatile fatty acids, lactic acid, and ammonia on rumen pH in sheep. Australian Journal of Agricultural Research 8, 674690.CrossRefGoogle Scholar
Brüggemann, J. & Giesecke, D. (1965). Über das Wachstum von Streptococcus bovis in Gegenwart von Ammoniumsulfat als einzige Stickstoffquelle. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 1. Abt. (Originale) 197, 347353.Google Scholar
Bryant, M. P. (1979). Microbial methane production — theoretical aspects. Journal of Animal Science 48, 193202.CrossRefGoogle Scholar
Bryant, M. P., Campbell, L. L., Reddy, C. A. & Crabill, M. R. (1977). Growth of desulfovibrio in lactate or ethanol media low in sulfate and in association with H2-utilizing methanogenic bacteria. Applied and Environmental Microbiology 33, 11621169.CrossRefGoogle ScholarPubMed
Bryant, M. P. & Robinson, I. M. (1962). Some nutritional characteristics of predominant culturable ruminal bacteria. Journal of Bacteriology 84, 605614.CrossRefGoogle ScholarPubMed
Buchanan, R. E. & Gibbons, N. E. (1974). Bergey's Manual of Determinative Bacteriology, 8th edn.Baltimore: Williams & Wilkins.Google Scholar
Counotte, G. H. M. (1981). Regulation of lactate metabolism in the rumen. Ph.D. thesis, University of Utrecht, The Netherlands.CrossRefGoogle Scholar
Counotte, G. H. M., Lankhorst, A. & Prins, R. A. (1983). Role of DL-lactic acid as an intermediate in rumen metabolism of dairy cows. Journal of Animal Science 56, 12221235.CrossRefGoogle ScholarPubMed
Counotte, G. H. M., Prins, R. A., Janssen, R. H. A. M. & de Bie, M. J. A. (1981). Role of Megasphaera elsdenii in the fermentation of DL-[2-13C]-lactate in the rumen of dairy cattle. Applied and Environmental Microbiology 42, 649655.CrossRefGoogle ScholarPubMed
Gawehn, K. & Bergmeyer, H. U. (1974). Methods of Enzymatic Analysis, 2nd English edn. translated from 3rd edn., vol. III (ed. Bergmeyer, H. U.), pp. 14921495. Weinheim: Verlag Chemie.Google Scholar
Gutierrez, J. (1953). Numbers and characteristics of lactate-utilizing organisms in the rumen of cattle. Journal of Bacteriology 66, 123128.CrossRefGoogle ScholarPubMed
Hishinuma, F., Kanegasaki, S. & Takahashi, H. (1968). Ruminal fermentation and sugar concentrations. A model experiment with Selenomonas ruminantium. Agricultural and Biological Chemistry 32, 13251330.Google Scholar
Hobson, P. N. & Mann, S. O. (1961). The isolation of glycerol-fermenting and lipolytic bacteria from the rumen of sheep. Journal of General Microbiology 25, 227240.CrossRefGoogle Scholar
Holdeman, L. V. & Moore, W. E. C. (1975). Anaerobe Laboratory Manual, 3rd edn.Blacksburg: Virginia Polytechnic Institute and State University.Google Scholar
Jayasuriya, G. C. N. & Hungate, R. E. (1959). Lactate conversions in the bovine rumen. Archives of Biochemistry and Biophysics 82, 274287.CrossRefGoogle ScholarPubMed
Mackie, R. I. & Gilchrist, F. M. C. (1979). Changes in lactate-producing and lactate-utilizing bacteria in relation to pH in the rumen of sheep during stepwise adaptation to a high-concentrate diet. Applied and Environmental Microbiology 38, 422430.CrossRefGoogle ScholarPubMed
Mackie, R. I. & Gilchrist, F. M. D. (1981). Stepwise adaptation of sheep fed ad libitum to a high concentrate diet and its effect on ruminal pH and lactic acid concentration. South African Journal of Animal Science 11, 229236.Google Scholar
Mackie, R. I., Gilchrist, F. M. C, Robberts, A. M., Hannah, P. E. & Schwartz, H. M. (1978). Microbiological and chemical changes in the rumen during stepwise adaptation of sheep to high concentrate diets. Journal of Agricultural Science, Cambridge 90, 241254.CrossRefGoogle Scholar
Mackie, R. I. & Heath, S. (1979). Enumeration and isolation of lactate-utilizing bacteria from the rumen of sheep. Applied and Environmental Microbiology 38, 416421.CrossRefGoogle ScholarPubMed
Morant, S. V., Ridley, J. L. & Sutton, J. D. (1978). A model for the estimation of volatile fatty acid production in the rumen in non-steady-state conditions. British Journal of Nutrition 39, 451462.CrossRefGoogle Scholar
Nakamura, K. & Takahashi, H. (1971). Role of lactato as an intermediate of fatty acid fermentation in the sheep rumen. Journal of General and Applied Microbiology 17, 319328.CrossRefGoogle Scholar
Neish, A. C. (1952). Analytical Methods for Bacterial Fermentations. Saskatoon: National Research Council of Canada.Google Scholar
Ogimoto, K. & Giesecke, D. (1974). Untersuchungen zur Genese und Biochemie der Pansenacidose. 2. Mikroorganismen und Umsetzung von Milchsäureisomeren. Zentralblatt fur Veterinärmedizin, Reihe A 21, 532538.CrossRefGoogle Scholar
Prins, R. A., Lankhorst, A., van der Meer, P. & van Nevel, C. J. (1975). Some characteristics of Anaerovibrio lipolytica, a rumen lipolytic organism. Antonie van Leeuwenhoek Journal of Microbiology and Serology 41, 111.CrossRefGoogle ScholarPubMed
Prins, R. A. & van der Meer, P. (1976). On the contribution of tho acrylate pathway to the formation of propionate from lactate in the rumen of cattle. Antonie van Leeuwenhoek Journal of Microbiology and Serology 42, 2531.CrossRefGoogle Scholar
Robinson, J. A., Strayer, R. F. & Tiedje, J. M. (1981). Method for measuring dissolved hydrogen in anaerobic ecosystems: application to the rumen. Applied and Environmental Microbiology 41, 545548.CrossRefGoogle Scholar
Russell, J. B. & Baldwin, R. L. (1978). Substrate preferences in rumen bacteria: evidence of catabolite regulatory mechanisms. Applied and Environmental Microbiology 36, 319329.CrossRefGoogle ScholarPubMed
Russell, J. B. & Baldwin, R. L. (1979 a). Comparison of substrate affinities among several rumen bacteria: a possible determinant of rumen bacterial competition. Applied and Environmental Microbiology 37, 531536.CrossRefGoogle ScholarPubMed
Russell, J. B. & Baldwin, R. L. (1979 b). Comparison of maintenance energy expenditure among several rumen bacteria grown on continuous culture. Applied and Environmental Microbiology 37, 537543.CrossRefGoogle Scholar
Russell, J. B., Delfino, F. J. & Baldwin, R. L. (1979). Effects of combinations of substrates on maximum growth rates of several rumen bacteria. Applied and Environmental Microbiology 37, 544549.CrossRefGoogle ScholarPubMed
Russell, J. B. & Dombrowski, D. B. (1980). Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Applied and Environmental Microbiology 39, 604610.CrossRefGoogle ScholarPubMed
Sakami, W. (1955). Handbook of Isotope Tracer Methods. Cleveland: Western Reserve University Press.Google Scholar
Satter, L. D. & Esdale, W. J. (1968). In vitro lactate metabolism by ruminal ingesta. Applied Microbiology 16, 680688.CrossRefGoogle ScholarPubMed
Schmidt, S. P., Smith, J. A. & Young, J. W. (1975). Rapid determination of (carbon-14) glucose specific radioactivity for in vivo glucose kinetics. Journal of Dairy Science 58, 952956.CrossRefGoogle ScholarPubMed
Shipley, R. A. & Clark, R. E. (1972). Tracer Methods for in vivo Kinetics. Theory and Applications, pp. 163175. London: Academic Press.Google Scholar
Slyter, L. L. (1976). Influence of acidosis on rumen function. Journal of Animal Science 43, 910929.CrossRefGoogle ScholarPubMed
Sutton, J. D. (1971). Carbohydrate digestion and glucose supply in the gut of the ruminant. Proceedings of the Nutrition Society 30, 243248.CrossRefGoogle ScholarPubMed
Sutton, J. D. (1979). Carbohydrate fermentation in the rumen — variations on a theme. Proceedings of the Nutrition Society 38, 275281.CrossRefGoogle ScholarPubMed
Taljaard, T. L. (1972). Representative rumon sampling. Journal of the South African Veterinary Association 43, 6569.Google Scholar
Therion, J. J., Kistner, A. & Kornelius, J. H. (1982). Effect of pH on growth rates of rumen amylolytic and lactilytic bacteria. Applied and Environmental Microbiology 44, 428434.CrossRefGoogle ScholarPubMed
Van der Walt, J. G. (1977). The separation of some volatile fatty acids on a ‘Sephadex’ partition chromatogram. Onderstepoorl Journal of Veterinary Research 44, 6972.Google ScholarPubMed
Wallnöfer, P., Baldwin, R. L. & Staono, E. (1966). Conversion of C14-labolled substrates to volatile fatty acids by the rumen microbiota. Applied Microbiology 14, 10041010.CrossRefGoogle ScholarPubMed
Williams, V. J. & Mackenzie, D. D. S. (1965). The adsorption of lactic acid from the roticulo-rumen of the sheep. Australian Journal of Biological Science 18, 917934.CrossRefGoogle Scholar
Wolin, M. J. (1976). Interactions between H2-producing and methane producing species. In Microbial Production and Utilization of Gases (ed. Schlegel, H. G., Gottschalk, G. and Pfennig, N.), pp. 141150. Göttingen, West Germany: E. Goltze, K. G.Google Scholar
Wolin, M. J. (1979). The rumen fermentation: a model for microbial interactions in anaorobic ecosystems. Advances in Microbial Ecology 3, 4977.CrossRefGoogle Scholar