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The role of dynamic modelling in understanding the microbial contribution to rumen function

Published online by Cambridge University Press:  14 December 2007

Jan Dijkstra ,
Jonathan A. N. Mills  and
James France
Jan Dijkstra*
Affiliation:
Animal Nutrition Group, Wageningen Institute of Animal Sciences, Wageningen University, Marijkeweg 40, 6709 PG Wageningen, The Netherlands
Jonathan A. N. Mills
Affiliation:
The University of Reading, Department of Agriculture, Earley Gate, Reading RG6 6AT, UK
James France
Affiliation:
The University of Reading, Department of Agriculture, Earley Gate, Reading RG6 6AT, UK
*
*Corresponding author: Dr Jan Dijkstra, fax +31 317 484260, email [email protected]
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Abstract

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Mechanistic models of microbial metabolism in the rumen aim at an improved understanding and integration for research purposes or at an improved prediction for practical purposes. The standard way of representing such models is the rate : state formalism. The system is defined by a number of state variables and a set of differential equations describe the change of the state variables with time. Three different types of solution to these dynamic models are distinguished, and examples of these solutions are described to illustrate the applications and contributions of dynamic modelling in the study of the rumen microbial ecosystem. Type I solutions are obtained when the system is in steady state and the differential equations are solved by setting the differentials to zero. An application of the type I solution is the indirect approach to quantifying the fibrolytic anaerobic fungi in the rumen. The solutions of the model describing the alternate life cycle of rumen fungi, with its free-swimming dispersal and particle-attached stages, appear to be consistent with ruminal and faecal observations. Type II solutions are obtained when the system is not in steady state but the differential equations can be integrated analytically. An application of this type of solution is the quantification of the growth and growth yield in batch cultures. Such models help to quantify the degradation of substrates in the rumen and to elucidate the interactions between groups of rumen micro-organisms. Type III solutions are obtained when the system is not in steady state and when the differential equations have to be solved numerically. Applications of the type III solutions are the rumen simulation models that describe substrate degradation, endproduct formation and microbial metabolism in an integrated manner. To illustrate this type III solution, a model of lactic acid metabolism in the rumen is defined, and its contribution to understanding of the paths and rates of lactic acid disappearance described. It is essential that the models are based on sound mathematical and biological principles. However, the various applications described in the paper show that models need not necessarily be complex and very detailed to contribute to better understanding.

Keywords

Modelling
Type
Research Article
Information
Nutrition Research Reviews , Volume 15 , Issue 1 , June 2002 , pp. 67 - 90
Copyright
Copyright © CABI Publishing 2002

References

AFRC, (1998) Responses in the yield of milk constituents to the intake of nutrients by dairy cows. AFRC Technical Committee on Responses to Nutrients. Report no. 11. Nutrition Abstracts and Reviews 68, 937–989.Google Scholar
Alderman, G, France, J & Kebreab, E (2001) A critique of the Cornell Net Carbohydrate and Protein System with emphasis on dairy cattle. 1. The rumen model. Journal of Animal and Feed Sciences 10, 1–24.CrossRefGoogle Scholar
Allen, MS (1997) Relationship between fermentative acid production in the rumen and the requirement for physically effective fiber. Journal of Dairy Science 80, 1447–1462.CrossRefGoogle ScholarPubMed
Argyle, JL & Baldwin, RL (1988) Modeling of rumen water kinetics and effects of rumen pH changes. Journal of Dairy Science 71, 1178–1188.CrossRefGoogle ScholarPubMed
Baldwin, RL (1995) Modeling Ruminant Digestion and Metabolism.. New York: Chapman and Hall.Google Scholar
Baldwin, RL, Thornley, JHM & Beever, DE (1987) Metabolism of the lactating cow. II. Digestive elements of a mechanistic model. Journal of Dairy Research 54, 107–131.CrossRefGoogle ScholarPubMed
Bazin, MJ (1981) Mixed culture kinetics. In Mixed Culture Fermentations. pp. 25–51 [Bushell, ME and Slater, JH editors]. London: Academic Press.Google Scholar
Bazin, MJ, Saunders, PT & Prosser, JI (1976) Models of microbial interactions in the soil. Critical Reviews in Microbiology 4, 463–498.CrossRefGoogle ScholarPubMed
Chamberlain, DG, Thomas, PC & Anderson, FJ (1983) Volatile fatty acid proportions and lactic acid metabolism in the rumen in sheep and cattle receiving silage diets. Journal of Agricultural Science 101, 47–58.CrossRefGoogle Scholar
Chen, G, Sniffen, CJ & Russell, JB (1987) 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, 983–992.CrossRefGoogle ScholarPubMed
Chesson, A & Forsberg, CW (1997) Polysaccharide degradation by rumen micro-organisms. In The Rumen Microbial Eco-system. 2nd ed., pp. 329–381 [Hobson, PN and Stewart, CS editors]. London: Blackie Academic and Professional.CrossRefGoogle Scholar
Clapperton, JL & Czerkawski, JW (1969) Methane production and soluble carbohydrates in the rumen of sheep in relation to the time of feeding and the effects of short-term intraruminal infusions of unsaturated fatty acids. British Journal of Nutrition 23, 813–826.CrossRefGoogle Scholar
Clark, JH, Klusmeyer, TH & Cameron, MR (1992) Microbial protein synthesis and flows of nitrogen fractions to the duodenum of dairy cows. Journal of Dairy Science 75, 2304–2323.CrossRefGoogle Scholar
Counotte, GHM, Lankhorst, A & Prins, RA (1983) Role of DL-lactic acid as an intermediate in rumen metabolism of dairy cows. Journal of Animal Science 56, 1222–1235.CrossRefGoogle ScholarPubMed
Counotte, GHM, Prins, RA, Janssen, RHAM & DeBie, MJA (1981) Role of Megasphaera elsdenii in the fermentation of DL-[2-13C]lactate in the rumen of dairy cattle. Applied and Environmental Microbiology 42, 649–655.CrossRefGoogle ScholarPubMed
Danfær, A (1990) A Dynamic Model of Nutrient Digestion and Metabolism in Lactating Dairy Cows. PhD Dissertation. National Institute of Animal Science, Foulum: Denmark.Google Scholar
Dehority, BA & Tirabasso, PA (2000) Antibiosis between ruminal bacteria and ruminal fungi. Applied and Environmental Microbiology 66, 2921–2927.CrossRefGoogle ScholarPubMed
Dhanoa, MS, France, J & Siddons, RC (1989) On using a double-exponential model for describing faecal marker concentration curves. Journal of Theoretical Biology 141, 247–257.CrossRefGoogle ScholarPubMed
Dijkstra, J (1994) Simulation of the dynamics of protozoa in the rumen. British Journal of Nutrition 72, 679–699.CrossRefGoogle ScholarPubMed
Dijkstra, J & Bannink, A (2000) Analyses of modelling whole rumen function. In Feeding Systems and Feed Evaluation Models, chapter 13: pp. 299–322 [Theodorou, MK and France, J editors. Wallingford: CAB International.Google Scholar
Dijkstra, J & France, J (1995) Modelling and methodology in animal science.In Proceedings Fourth International Workshop on Modelling Nutrient Utilisation in Farm Animals, pp. 9–18 [Danfaer, A and Lescoat, P editors]. Foulum: Denmark: National Institute Animal Science.Google Scholar
Dijkstra, J & France, J (1997) Modelling interactions among micro-organisms in the reticulo-rumen. In Progress in Microbial Ecology, 7th International Symposium on Microbial Ecology, pp. 297–309 [Martins, MT, Sato, MIZ, Tiedje, JM, Hagler, LCNDobereiner, J and Sanchez, PS editors]. Sao Paulo: International Committee on Microbial Ecology/Brazilian Society for Microbiology.Google Scholar
Dijkstra, J, France, J & Davies, DR (1998) Different mathematical approaches to estimating microbial protein supply in ruminants. Journal of Dairy Science 81, 3370–3384.CrossRefGoogle ScholarPubMed
Dijkstra, J, France, J, Dhanoa, MS & Lopez, S (2000) Simulation of substrate degradation, microbial synthesis and gas production in the gas production technique and in vivo. In Gas Production: Fermentation Kinetics for Feed Evaluation and to Assess Microbial Activity. pp. 42–43. Edinburgh: British Society of Animal Science.Google Scholar
Dijkstra, J, France, J, Neal, HDStC, Assis, AG, Aroeira, LJM & Campos, OF (1996) Simulation of digestion in cattle fed sugar cane: model development. Journal of Agricultural Science, Cambridge 127, 231–246.CrossRefGoogle Scholar
Dijkstra, J, France, J & Tamminga, S (1998) Quantification of the recycling of microbial nitrogen in the rumen using a mechanistic model of rumen fermentation processes. Journal of Agricultural Science, Cambridge 130, 81–94.CrossRefGoogle Scholar
Dijkstra, J, Neal, HDStC, Beever, DE & France, J (1992) Simulation of nutrient digestion, absorption and outflow in the rumen: model description. Journal of Nutrition 122, 2239–2256.CrossRefGoogle ScholarPubMed
Dijkstra, J & Tamminga, S (1995) Simulation of the effects of diet on the contribution of rumen protozoa to degradation of fibre in the rumen. British Journal of Nutrition 74, 617–634.CrossRefGoogle ScholarPubMed
Firkins, JL (1996) Maximizing microbial protein synthesis in the rumen. Journal of Nutrition 126, 1347S–1354S.CrossRefGoogle ScholarPubMed
Fonty, G, Chavarot, M, Lepetit, J, Canistro, J & Favier, R (1999) Mechanical resistance of wheat straw after incubation in cultures of rumen cellulolytic micro-organisms. Animal Feed Science and Technology 80, 297–307.CrossRefGoogle Scholar
France, J, Dijkstra, J, Dhanoa, MS & Baldwin, RL (1998) Biomathematical applications in animal nutrition. Journal of the Franklin Institute 335, 241–258.CrossRefGoogle Scholar
France, J, Theodorou, MK & Davies, D (1990) Use of zoospore concentrations and life cycle parameters in determining the population of anaerobic fungi in the rumen eco-system. Journal of Theoretical Biology 147, 413–422.CrossRefGoogle Scholar
France, J & Thornley, JHM (1984) Mathematical Models in Agriculture. London: Butterworths.Google Scholar
France, J, Thornle, JHM & Beever, DE (1982) A mathematical model of the rumen. Journal of Agricultural Science, Cambridge 99, 343–353.CrossRefGoogle Scholar
Fredrickson, AG (1977) Behavior of mixed cultures of micro-organisms. Annual Review of Microbiology 31, 63–87.CrossRefGoogle Scholar
Gill, M, Siddons, RC & Beever, DE (1986) Metabolism of lactic acid isomers in the rumen of silage-fed sheep. British Journal of Nutrition 55, 399–407.CrossRefGoogle ScholarPubMed
Gordon, GLR & Phillips, MW (1998) The role of anaerobic gut fungi in ruminants. Nutrition Research Reviews 11, 133–168.CrossRefGoogle ScholarPubMed
Hanigan, MD, Dijkstra, J, Gerrits, WJJ & France, J (1997) Modelling post-absorptive protein and amino acid metabolism in the ruminant. Proceedings of the Nutrition Society 56, 631–643.CrossRefGoogle ScholarPubMed
Hespell, RB & Bryant, MP (1979) Efficiency of rumen microbial growth: influence of some theoretical and experimental factors on YATP. Journal of Animal Science 49, 1640–1659.CrossRefGoogle ScholarPubMed
Hobson, PN & Stewart, CS (1997) The Rumen Microbial Eco-system. 2nd ed. London: Blackie Acedemic and Professional.CrossRefGoogle Scholar
Isaacson, HR, Hinds, FC, Bryant, MP & Owens, FN (1975) Efficiency of energy utilization by mixed rumen bacteria in continuous culture. Journal of Dairy Science 58, 1645–1659.CrossRefGoogle ScholarPubMed
Kashket, ER (1987) Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiology Reviews 46, 233–244.CrossRefGoogle Scholar
Kaske, M, Hatiboglu, S & Von Engelhardt, W (1992) The influence of density and size of particles on rumination and passage from the reticulo-rumen of sheep. British Journal of Nutrition 67, 235–244.CrossRefGoogle ScholarPubMed
Koch, AL (1994) Growth measurement. In Methods for General and Molecular Bacteriology. pp. 248–277 [Gerhardt, P, Murray, RGEWood, WA and Kreig, NR editors]. Washington: American Society for Microbiology Press.Google Scholar
Krause, DO, Smith, WJM, Ryan, FME, Mackie, RI & McSweeney, CS (1999) Use of 16S-rRNA based techniques to investigate the ecological succession of microbial populations in the immature lamb rumen: Tracking of a specific strain of inoculated Ruminococcus and interactions with other microbial populations in vivo. Microbial Ecology 38, 365–376.CrossRefGoogle ScholarPubMed
Lee, SS, Ha, JK & Cheng, K-J (2000) Relative contributions of bacteria, protozoa, and fungi to in vitro degradation of orchard grass cell walls and their interactions. Applied and Environmental Microbiology 66, 3807–3813.CrossRefGoogle ScholarPubMed
Lescoat, P & Sauvant, D (1995) Development of a mechanistic model for rumen digestion validated using the duodenal flow of amino acids. Reproduction Nutrition Developpement 35, 45–70.CrossRefGoogle Scholar
Lopez, S, Murison, SD, Travis, AJ & Chesson, A (1993) Degradability of parenchyma and sclerenchyma cell walls isolated at different stages from a newly extended maize internode. Acta Botanica Neerlandica 42, 165–174.CrossRefGoogle Scholar
Mackie, RI & Gilchrist, FMC (1979) Changes in lactate-producing and lactate-utilising bacteria in reaction to pH in the rumen of sheep during stepwise adaptation to a high-concentrate diet. Applied and Environmental Microbiology 38, 422–430.CrossRefGoogle Scholar
Mackie, RI, Gilchrist, FMC & Heath, S (1984) An in vivo study of ruminal micro-organisms influencing lactate turnover and its contribution to volatile fatty acid production. Journal of Agricultural Science, Cambridge 103, 37–51.CrossRefGoogle Scholar
Malestein, A, Van't Klooster, AT, Prins, RA & Counotte, GHM (1984) Concentrate feeding and ruminal fermentation 3. Influence of concentrate ingredients on pH, on DL-lactic acid concentration in rumen fluid of dairy cows and on dry matter intake. Netherlands Journal of Agricultural Science 32, 9–21.CrossRefGoogle Scholar
Mitchell and Gauthier Associates (1995) Advanced Continuous Simulation Language (ACSL). User's guide/Reference manual, version 11. MGA Software.Google Scholar
Møller, PD, Diernaes, L, Sehested, J, Hyldgaard-Jensen, J & Skadhauge, E (1997) Lactate transport across the bovine rumen epithelium in vitro. Journal of Veterinary Medicine A44, 31–38.CrossRefGoogle Scholar
Monod, J (1942) Recherches sur la Crossance des Cultures Bactériennes. 2nd ed. Paris: France: Hermann.Google Scholar
Mountfort, DO & Orpin, CG (1995) Anaerobic Fungi. New York: Marcel Dekker Inc.Google Scholar
Newbold, CJ, Williams, AG & Chamberlain, DG (1987) The in-vitro metabolism of D,L-lactic acid by rumen micro-organisms. Journal of the Science of Food and Agriculture 38, 9–18.CrossRefGoogle Scholar
Oldick, BS, Firkins, JL & Kohn, RA (2000) Compartmental modeling with nitrogen-15 to determine effects of degree of fat saturation on intraruminal N recycling. Journal of Animal Science 78, 2421–2430.CrossRefGoogle ScholarPubMed
Owens, FN, Secrist, DS, Hill, WJ & Gill, DR (1998) Acidosis in cattle: a review. Journal of Animal Science 76, 275–286.CrossRefGoogle ScholarPubMed
Pagie, L & Hogeweg, P (1999) Colicin diversity: a result of eco-evolutionary dynamics. Journal of Theoretical Biology 60, 3688–3696.Google Scholar
Pirt, SJ (1965) The maintenance energy of bacteria in growing cultures. Proceedings of the Royal Society London 163B, 224–231.Google Scholar
Pirt, SJ (1975) Principles of Microbe and Cell Cultivation. Oxford: Blackwell Scientific Publications.Google Scholar
Riley, MA (1998) Molecular mechanisms of bacteriocin evolution. Annual Review of Genetics 32, 255–278.CrossRefGoogle ScholarPubMed
Rodriguez, CA, Gonzalez, J, Alvir, MR, Repetto, JL, 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.CrossRefGoogle ScholarPubMed
Rooke, JA & Armstrong, DG (1989) The importance of the form of nitrogen on microbial protein synthesis in the rumen of cattle receiving grass silage and continuous intrarumen infusions of sucrose. British Journal of Nutrition 61, 113–121.CrossRefGoogle ScholarPubMed
Russell, JB & Baldwin, RL (1978) Substrate preferences in rumen bacteria: evidence of catabolite regulatory mechanism. Applied and Environmental Microbiology 36, 319–329.CrossRefGoogle Scholar
Russell, JB & Baldwin, RL (1979) Comparison of substrate affinities among several rumen bacteria: a possible determinant of rumen bacterial competition. Applied and Environmental Microbiology 37, 531–536.CrossRefGoogle ScholarPubMed
Russell, JB & Dombrowski, DB (1980) Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Applied and Environmental Microbiology 39, 604–610.CrossRefGoogle ScholarPubMed
Russell, JB, O'Connor, JD, Fox, DG, Van Soest, PJ & Sniffen, CJ (1992) A net carbohydrate and protein system for evaluating cattle diets: I. Ruminal fermentation. Journal of Animal Science 70, 3551–3561.CrossRefGoogle Scholar
Russell, JB, Sharp, WM & Baldwin, RL (1979) The effect of pH on maximum bacterial growth rate and its possible role as a determinant of bacterial competition in the rumen. Journal of Animal Science 48, 251–255.CrossRefGoogle ScholarPubMed
Shi, Y & Weimer, PJ (1992) Response surface analysis of the effects of pH and dilution rate on Ruminococcus flavefaciens FD-1 in cellulose-fed continuous culture. Applied and Environmental Microbiology 58, 2583–2591.CrossRefGoogle ScholarPubMed
Smith, RH (1979) Synthesis of microbial nitrogen compounds in the rumen and their subsequent digestion. Journal of Animal Science 49, 1604–1612.CrossRefGoogle Scholar
Stewart, CS (1992) Lactic acid bacteria in the rumen. In The Lactic Acid Bacteria in Health and Disease. pp. 49–68 [Wood, BJB editor]. New York: Elsevier.Google Scholar
Tamminga, S (1996) A review on environmental impacts of nutritional strategies in ruminants. Journal of Animal Science 74, 3112–3124.CrossRefGoogle ScholarPubMed
Tamminga, S, Van Straalen, WM, Subnel, APJ, Meijer, RGM, Steg, A, Wever, CJG & Blok, MC (1994) The Dutch protein evaluation system: the DVB/OEB-system. Livestock Production Science 40, 139–155.CrossRefGoogle Scholar
Tamminga, S & Van Vuuren, AM (1988) Formation and utilization of end products of lignocellulose degradation in ruminants. Animal Feed Science and Technology 21, 141–159.CrossRefGoogle Scholar
Tamminga, S, Van Vuuren, AM, Van der Koelen, CJ, Ketelaar, RS & Van der Togt, PL (1990) Ruminal behaviour of structural carbohydrates, non-structural carbohydrates and crude protein from concentrate ingredients in dairy cows. Netherlands Journal of Agricultural Science 38, 513–526.CrossRefGoogle Scholar
Theodorou, MK, Gill, M, King-Spooner, C & Beever, DE (1990) Enumeration of anaerobic chytridiomycetes as thallus forming units: novel method for quantification of fibrolytic fungal populations from the digestive tract eco-system. Applied and Environmental Microbiology 56, 1073–1078.CrossRefGoogle Scholar
Therion, JJ, Kistner, AA & Kornelius, JH (1982) Effect of pH on growth rates of amylolytic and lactilytic bacteria. Applied and Environmental Microbiology 44, 428–434.CrossRefGoogle ScholarPubMed
Ushida, K & Jouany, JP (1990) Effect of defaunation on fibre digestion in sheep given two isonitrogenous diets. Animal Feed Science and Technology 29, 153–158.CrossRefGoogle Scholar
Ushida, K, Kayouli, C, De Smet, S & Jouany, JP (1990) Effect of defaunation on protein and fibre digestion in sheep fed on ammonia-treated straw-based diets with or without maize. British Journal of Nutrition 64, 765–775.CrossRefGoogle ScholarPubMed
Williams, AG & Cockburn, JE (1991) Effect of slowly and rapidly degraded protein sources of the concentrations of amino acids and peptides in the rumen of steers. Journal of the Science of Food and Agriculture 56, 303–314.CrossRefGoogle Scholar
Williams, AG & Coleman, GS (1997) The Rumen Protozoa. In The Rumen Microbial Eco-system, 2nd ed., pp. 73–139 [Hobson, PN and Stewart, CS editors]. London: Blackie Academic and Professional.CrossRefGoogle Scholar
Williams, VJ & Mackenzie, DDS (1964) The absorption of lactic acid from the reticulo-rumen of the sheep. Australian Journal of Biological Sciences 18, 917–934.CrossRefGoogle Scholar
Wimpenny, JWT (1981) Spatial order in microbial eco-systems. Biological Reviews of the Cambridge Philosophical Society 56, 295–342.CrossRefGoogle Scholar
Wolin, MJ (1979) The rumen fermentation: a model for microbial interactions in anaerobic eco-systems. In Advances in Microbial Ecology 3. pp. 49–77 [Alexander, M editor]. New York: 2Plenum Press.CrossRefGoogle Scholar
Wolin, MJ, Miller, TL & Stewart, CS (1997) Microbe-microbe interactions. In The Rumen Microbial Eco-system.2nd ed., pp. 467–491 [Hobson, PN and Stewart, CS editors]. London: Blackie Academic and Professional.Google Scholar