The Role of Protozoa in Feed Digestion

Asian-Australasian Journal of Animal Sciences

Volumn 12, Issue 1, 1999, Pages 113-128

  Jouany, J P ^a   Ushida, K ^a  

^a CEMAGREF   (France)

Author keywords

Carbohydrate Digestion; Ecosystem; Fermentation; Protein Digestion; Review; Rumen Protozoa

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); BOVIDAE; MICROBIOTA; PROTOZOA;

EID: 0033476618     PISSN: 10112367     EISSN: None     Source Type: Journal    
DOI: 10.5713/ajas.1999.113     Document Type: Review

References (84)

1. 14C-L-Leucine by rumen protozoa. Zentrl Veter. Med. Reike A, 26, 551-557.
2. Argyle, J. L. and R. J. Forster. 1989. Effects of ciliate protozoa on rumen bacterial populations. In «The Roles of Protozoa and Fungi in Ruminant Digestion», J. V. Nolan, R. A. Leng and D. I. Demeyer Eds, Penambul Books, Armidale, Australia, pp. 317-319.
3. Bailey, R. W. and B. D. E. Gaillard. 1965. Carbohydrases of the rumen ciliate Epidinium ecaudatum. Hydrolysis of plant hemicellulose fractions and -linked glucose polymers. Biochem. J., 95, 758-766.
4. Bohatier, J., J. Senaud and M. Benyahya. 1990. In situ degradation of cellulose fibres by the entodiniomorph rumen ciliate Polyplastron multivesiculatum. Protoplasma, 154, 122-131.
5. Coleman, G. S. 1969. The metabolism of starch, maltose, glucose and some other sugars by the rumen ciliate Entodinium caudatum. J. Gen. Microbiol., 57, 303-332.
6. Coleman, G. S. 1975. The inter-relationship between rumen ciliate protozoa and bacteria. In «Digestion and Metabolism in the Ruminant», I. W. Mc Donald and A. C. Warner Eds, University of New England Publishing Unit, Armidale, Australia, pp. 149-164.
7. Coleman, G. S. 1985. The cellulase content of 15 species of entodiniomorphid protozoa, mixed bacteria and plant debris isolated from the ovine rumen. J. Agric. Sci., 104, 349-360.
8. Coleman, G. S., J. I. Laurie, J. E. Bailey and S. A. Holdgate. 1976. The cultivation of cellulolytic protozoa isolated from the rumen. J. Gen. Microbiol. 95, 144-150.
9. Collombier, J. 1981. Contribution à l'étude du rôle des protozoaires ciliés du rumen dans l'apport d'azote microbien entrant dans le duodénum de ruminant. Thése de Docteur-Ingénieur. Université Clermont II, no d'ordre 105. 85 pages, Clermont-Ferrand, France.
10. Denholm, A. M. and J. R. Ling. 1984. In vitro metabolism of bacterial cell walls by rumen ciliate protozoa. Can. J. Anim. Sci. 64 (suppl.), 18-19.
11. De Puytorac, P., A. Batisse, J. Bohatier, J. O. Corliss, G. Deroux, P. Didier, J. Dragesco, G. Fryd-Versavel, J. Grain, C. A. Grolière, R. Hovasse, F. Iftode, M. Laval, M. Roque, A. Savoie and M. Tuffrau. 1974. Proposition dune classification du phylum ciliophora Doflein, 1901. CR Acad. Sci., Paris, 278, 2799-2802.
12. Demeyer, D. I. 1989. Effect of defaunation on rumen fibre digestion and digesta kinetics. In «The Role of Protozoa and Fungi in Ruminant Digestion», J. V. Nolan, R. A. Leng and D. I. Demeyer Eds, Penambul Books, Armidale, Australia, pp. 171-179.
13. Eadie, J. M. and P. N. Hobson. 1962. Effect of the presence or absence of rumen ciliate protozoa on the total rumen bacterial count in lambs. Nature, London, 193, 503-505.
14. Faichney, G. and D. A. Griffiths. 1978. Behaviour of solute and particulate markers in the stomach of sheep given a concentrate diet. Br. J. Nutr., 40, 71-82.
15. Faichney, G., C. Poncet. B. Lassalas, J. P. Jouany, L. Millet, J. Dore and A. G. Brownlee. 1997. Effect of concentrate in a hay diet on the contribution of anaerobic fungi, protozoa and bacteria to nitrogen into rumen and duodenal digesta in sheep. Anim. Feed Sci. Technol., 64, 193-213.
16. Forsberg, L. W., L. K. A. Lovelock., L. Krumholz and J. G. Buchanan-Smith. 1984. Protease activities of rumen protozoa. Appl. Environ. Microbiol., 47, 101-110.
17. Grain, J. and J. Senaud. 1985. Degradation de fragments de luzerne fraîche par le cilié du rumen Epidinium caudatum; attachement, ingestion et digestion. Protistologica, 21, 447-466.
18. Hino, T. and J. B. Russell. 1987. Relative contributions of ruminal bacteria and protozoa to the degradation of protein in vitro. J. Anim. Sci., 64, 261-270.
19. Hsu, J. T., G. C. Fahey, N. R. Merchen and R. I. Mackie. 1991. Effect of defaunation and various nitrogen supplementation regimens on microbial numbers and activity in the rumen of sheep. J. Anim. Sci., 69, 1279-1289.
20. Itabashi, H. and M. Kandatsu. 1975. Influence of rumen ciliate protozoa on the concentration of free amino acids in the rumen fluids. Jpn. J. Zootech. Sci., 46, 600-606.
21. Itabashi, H. and T. Matsukawa. 1979. Studies on nutritional significance of rumen ciliate protozoa in cattle. 3-Influence of protozoa on growth rate, food intake, rumen fermentation and various plasma components in calves under different planes of nutrition. Bull. Tohoku Natl. Agric. Exp. Sta., Morioka, 59, 111-128.
22. th World Conf. Anim. Prod., Tokyo, 3, 34.
23. Itabashi, H., T. Kobayashi, M. Matsumoto and H. Takenaka, 1989. Effect of unfaunation on plasma free amino acids, gastrin and insulin, and duodenal nitrogen flow in ruminants. Asian-Australasian J. Anim. Sci. 2, 489-490.
24. Itabashi, H., T. Kobayashi, A. Takenaka and M. Matsumoto. 1990. Effect of protozoa on nutritional characteristics of ruminants. In «The Rumen Ecosystem; The Microbial Metabolism and Its Regulation», S. Hoskino, R. Onodera, H. Minato and H. Itabashi Eds, Japan Scientific Society Press, Springer-Verlag, Tokyo, Japan, pp. 169-176.
25. Ivan, M., M. Hidiroglou and H. V. Petit. 1991. Duodenal flow of nitrogen following protozoal inoculation of fauna-free sheep fed a diet supplemented with casein of soybean meal. Can. J. Anim. Sci., 71, 793-801.
26. Ivan, M., D. M. Veira and C. A. Kellecher. 1986. The allievation of chronic copper toxicity in sheep by ciliate protozoa. Br. J. Nutr., 55, 361-367.
27. Joblin, K. N. 1981. Isolation, enumeration and maintenance of rumen anaerobic fungi in roll tubes. Appl. Environ. Microbiol., 42, 1119-1122.
28. Jouany, J. P. 1994. Manipulation of microbial activity in the rumen. Arch. Anim. Nutr., 46, 133-153.
29. Jouany, J. P. 1996. Effect of rumen protozoa on nitrogen utilization by ruminants. J. Nutr., 126, 1335S-1346S.
30. Jouany, J. P. and C. Martin. 1997. Effect of protozoa in plant cell wall and starch digestion in the rumen. In «Rumen Microbes and Digestive Physiology in Ruminants», R. Onodera, H. Itabashi, K. Ushida, H. Yano and Y. Sasaki Eds, Japan Sci. Soc. Press, S. Karger, Basel, Tokyo, Japan, pp. 11-24.
31. Jouany, J. P. and J. Senaud. 1979. Role of rumen protozoa in the digestion of food cellulolytic materials. Ann. Rech. Vet., 10, 261-263.
32. Jouany, J. P. and P. Thivend. 1972. Evolution post prandiale de la composition glucidique des corps microbiens du rumen en fonction de la nature des glucides du rumen. I-Les protozoaires. Ann. Biol. Anim. Bioch. Biophys., 12, 673-677.
33. Jouany, J. P., D. I. Demeyer and J. Grain. 1988. Effect of defaunating the rumen. Anim. Feed Sci. Technol., 21, 229-265.
34. Jouany, J. P., A. Cornu, F. Mathieu and J. Senaud. 1997. Effect of rumen protozoa on the degradation of neutral sugars from plant cell walls. In «Evolution of the Rumen Microbial Ecosystem», A. Chesson, C. S. Stewart, H. J. Flint Eds, Reprod. Nutr. Develop., suppl., Elsevier, France, pp. 43 -44.
35. Jouany, J. P., M. Ivan, Y. Papon and B. Lassalas. 1992. Effects of Isotricha, Eudiplodinium, Epidinium + Entodinium, and a mixed population of rumen protozoa on the in vitro degradation of fishmeal, soybeanmeal and casein. Can. J. Anim. Sci., 72, 871-880.
36. Jouany, J. P., B. Zainab, J. Senaud, C. A. Groliere, J. Grain and P. Thivend. 1981. Role of the rumen ciliate protozoa Polyplastron multivesiculatum, Entodinium sp. and Isotricha prostoma in the digestion of a mixed diet in sheep. Reprod. Nutr. Develop., 21, 871-884.
37. Kiessling, K. H., H. Petterson, K. Sandholm and M. Olsen. 1984. Metabolism of aflatoxin, ochratoxin, zealarenone and three trichotecenes by intact fluid, rumen protozoa and rumen bacteria. Appl. Environ. Microbiol., 47, 1070-1073.
38. Kurihara, Y., T. Takechi and F. Shibata. 1978. Relationship between bacteria and ciliate protozoa in the rumen of sheep fed on a purified diet. J. Agric. Sci., 90, 373-381.
39. Martin, C., B. Michalet-Doreau, G. Fonty and A. G. Williams. 1993. Post prandial variations in the activitiy of polysaccharide degrading enzymes of fluid-and particle-associated rumen microbial populations. Curr. Microbiol., 27, 223-228.
40. Mathieu, F., J. P. Jouany, J. Senaud, J. Bohatier, G. Bertin and M. Mercier. 1996. The effect of Saccharomyces cerevisiae and Aspergillus oryzae on fermentation in the rumen of defaunated and refaunated sheep; protozoal and probiotic interactions. Reprod. Nutr. Develop., 36, 271-287.
41. Mathieu, F., J. Senaud, J. P. Jouany, J. Bohatier, B. Berlin and M. Mercier, 1997. Effect of Saccharomyces cerevisiae and Aspergillus oryzae on the digestion of nitrogen in the rumen of defaunated and refaunated sheep. Anim. Feed Sci. Technol. 75, 1-13.
42. Mathieu F., J. Senaud, J. P. Jouany, J. Bohatier, G. Bertin and M. Mercier. 1998. The effect of Saccharomyces cerevisiae and Aspergillus oryzae on the digestion of cell wall fraction of a mixed diet in defaunated and refaunated sheep rumen. Reprod. Nutr. Develop. 38, 401-416.
43. Matsumoto, M., A. Takenaka, T. Kobayashi and H. Itabashi. 1989. The effects of Epidinium caudatum or Dasytricha ruminatium on the rumen fermentation and nitrogen metabolism in goat. Asian-Australasian J. Anim. Sci. 2:483-484.
44. McNaught, M. L., E. C. Owen, K. M. Henry and S. K. Kon. 1954. The utilization of non protein nitrogen in the bovine rumen. 8-The nutritive value of the proteins of preparation of dried rumen bacteria, rumen protozoa and brewers yeasts for rats. Biochem. J., 56, 151-156.
45. Mendoza, G. D., R. A. Britton and R. A. Stock. 1993. Influence of ruminai protozoa on site and extent of starch digestion and ruminai fermentation. J. Anim. Sci., 71, 1572-1578.
46. Mendoza, G. D., R. A. Britton and R. A. Stock. 1995. Effect of protozoa and urea level on in vitro starch disappearance and amylolytic activity of ruminal microorganisms. Anim. Feed Sci. Technol., 54, 315-325.
47. Meyer, J. H. F., S. I. Van Der Walt and H. M. Schwartz. 1986. The influence of diet and protozoal numbers on the break-down and synthesis of protein in the rumen of sheep. J. Anim. Sci., 62, 509-520.
48. Michalowski, T. 1989. The importance of protein solubility and nature of dietary nitrogen for the growth of rumen ciliates in vitro. In «The Role of Protozoa and Fungi in Ruminant Digestion», J. V. Nolan, R. A. Leng and D. I. Demeyer eds, Penambul Books, Armidale, Australia, pp. 223-232.
49. Musynski, P., T. Michalowski and P. Szczemkowski. 1985. The influence of protein on the number of rumen ciliates Entodinium caudatum and Diplodinium affine in vitro. Act. Protozool., 24, 307-317.
50. Newbold, C. J., P. W. Griffin and R. J. Wallace. 1989. Interactions between rumen bacteria and ciliate protozoa in the attachment to barley straws. Lett. Appl. Microbiol., 8, 63 -66.
51. Nilsson, J. R. 1979. Phagotrophy in Tetrahymena. In «Biochemistry and Physiology of Protozoa», vol. 2, N. Levandowsky and S. H. Hutner Eds, Academic Press, New York, pp. 339-379.
52. Ohta, M., H. Matsumoto, K. Ishii and Y. Ueno. 1978. Metabolism of thrichotecene mycotoxins. J. Biochem. (Tokyo), 84, 697-706.
53. Onodera, R. and M. Kandatsu. 1970. Amino acids and protein metabolism of rumen ciliate protozoa. 4. Metabolism of casein. Jpn. J. Zootech. Sci., 41, 307-313.
54. Onodera, R. and K. Koga. 1987. Effect of inhabitation by rumen protozoa on the nutritive value of protein in rumen contents. Agric. Biol. Chem., 51, 1417-1424.
55. Orpin, C. G. and F. J. Hall. 1983. Surface structures of the rumen holotrich protozoa Isotricha intestinalis with particular reference to the attachment Zone. Curr. Microbiol., 8, 321-325.
56. Orpin, C. G. and A. J. Letcher. 1983-84. Effect of absence of ciliate protozoa on rumen fluid volume, flow rate and bacterial populations in sheep. Anim. Feed Sci. Technol., 10, 145-153.
57. Prins, R. A. and W. Van Hoven. 1977. Carbohydrate fermentation by the rumen ciliate Isotricha prostoma Protistologica, 13, 549-556.
58. Punia, B. S., J. Leibholz and G. Faichney. 1987. The role of rumen protozoa in the utilization of paspalum hay by cattle. Br. J. Nutr., 57, 395-406.
59. Romulo, B., S. H. Bird and R. A. Leng. 1989. Combined effect of defaunation and protein supplementation on intake, digestibility, N retention and fungi counts in sheep fed straw-based diets. In «The Role of Protozoa and Fungi in Ruminant Digestion», J. V. Nolan, R. A. Leng and D. I. Demeyer Eds, Penambul Books, Armidale, Australia, pp. 285-288.
60. Rowe, J. B., A. Davies and A. W. J. Broome. 1985. Quantitative effects of defaunation on rumen fermentation and digestion in sheep. Br. J. Nutr., 54, 105-119.
61. Salter, D. M. and R. H. Smith. 1977. Digestibilities of nitrogen compounds in rumen bacteria and in other components of digesta in the small intestine of the young steer. Br. J. Nutr., 38, 207-216.
62. Senaud, J., J. Bohatier and J. Grain. 1986. Comparaisons du comportement alimentaire de 2 protozoaires ciliès du rumen, Epidinium ecaudatum and Polyplastron multivesiculatum: mècanismes dingestion et de digestion. Reprod. Nutr. Develop., 26, 287-289.
63. Siddons, R. C., J. V. Nolan, D. E. Beever and J. C. Mc Rae. 1985. Nitrogen digestion and metabolism in sheep consuming diets contrasting in forms and levels of nitrogen. Br. J. Nutr., 54, 175-187.
64. Storm, E., E. R. Ørskov and R. Smart. 1983. The nutritive value of rumen microorganisms in ruminants. 2-The apparent digestibility and net utilization of microbial N for growing lambs. Br. J. Nutr., 50, 471-478.
65. Takenaka, H. and Itabashi. 1994. The properties of cellulases derived from rumen protozoa and cellulase gene cloning from cDNA library of rumen protozoa. Proc. Jpn. Soc. Rum. Metab. Physiol., 5 (2), 63-65.
66. Teather, R. M., S. Mahadevan, J. D. Erfle and F. D. Sauer. 1984. Negative correlation between protozoal and bacterial levels in rumen samples and its relation to the determination of dietary effects on the rumen microbial population. Appl. Environ. Microbiol., 47, 566-570.
67. Trabalza-Marinucci, M., B. A. Dehority and S. C. Loech. 1992. In vitro and in vivo studies of factors affecting digestion of feeds in synthetic fiber bags. 3. Anim. Sci., 70, 296-307.
68. Ueda, Y., R. Onodera and M. Kandatsu. 1975. Metabolism of peptides by rumen ciliate protozoa. Jpn J. Zootech. Sci., 46, 34.
69. Ushida, K. and J. P. Jouany. 1985. Effects of protozoa on rumen protein degradation in sheep. Reprod Nutr. Develop., 25, 1075-1081.
70. Ushida, K. and J. P. Jouany. 1990. Effects of defaunation on fibre digestion in sheep given two isonitrogenous diets. Anim. Feed Sci. Technol., 29, 153-158.
71. Ushida, K. and J. P. Jouany. 1994. Fibre digesting capacities of 5 genera of rumen ciliates. Proc. Soc. Nutr. Physiol., 3, 168.
72. Ushida, K. and J. P. Jouany. 1996. Methane production associated with rumen ciliated protozoa and its effect on protozoa activity. Lett. Appl. Microbial., 23, 129-132.
73. Ushida, K., J. P. Jouany and D. I. Demeyer. 1991. Effects of presence or absence of rumen protozoa on the efficiency of utilisation of concentrate and fibrous feeds. In «Physiological Aspects of Digestion and Metabolism in Ruminants», T. Tsuda, Y. Sasaki and R. Kawashima eds, Academic Press, Tokyo, pp. 625-654.
74. Ushida, K., J. P. Jouany and P. Thivend. 1986. Role of protozoa in nitrogen digestion in sheep given two isonitrogenous diets. Br. J. Nutr., 56, 407-419.
75. Ushida, K., T. Kaneko and Y. Kojina. 1987. Effect of presence of large entodiniomorphid protozoa on the rumen bacterial flora, fauna composition of small entodinia and in vitro cellulolysis and xylanolysis. Jpn. J. Zootech. Sci., 58, 893-902.
76. Ushida, K., H. Takenaka and Y. Kojima. 1989. A simple in situ method for estimating fungal population sizes in the rumen. Lett. Appl. Microbiol., 9, 109-111.
77. Ushida, K., J. P. Jouany, C. Kayouli, and D. I. Demeyer. 1989. Effect of defaunation on fibre digestion in sheep fed ammonia-treated straw based diets. In «The Role of Protozoa and Fungi in Ruminant Digestion». J. V. Nolan, R. A. Leng and D. I. Demeyer Eds, Penambul Books, Armidale, Australia, pp. 307-308.
78. Ushida, K., C. Kayouli, S. De Smet and J. P. Jouany. 1990. Effect of defaunation on protein and fibre digestion in sheep fed on ammonia-treated straw-based diets with or without maize. Br. J. Nutr., 64, 765-775.
79. Veira, D. M., M. Ivan and P. Y. Jui. 1983. Rumen dilate protozoa: effects on digestion in the stomach of sheep. J. Dairy Sci., 66, 1015-1022.
80. Wichterman, R. 1986. The biology of Paramecium. Plenum Press, New York, 327 pages.
81. Williams, A. G. and G. S. Coleman. 1992. The Rumen Protozoa, A. G. Williams and G. S. Coleman Eds, Springer-Verlag, London, 441 pages.
82. Williams, A. G. and S. E. Withers. 1990. Effect of ciliate protozoa on the activity of polysaccharide-degrading enzymes and fibre breakdown in the rumen ecosystem. J. Appl. Bacteriol., 70, 144-155.
83. Williams, A. G., N. H. Strachan and A. B. Ellis. 1988. Factors affecting the xylanolytic enzyme activity of microbial populations recovered from the liquid and solid phases of the rumen ecosystem. In «Perspectives in Microbial Ecology», F. Megusar and M. Gantar Eds, Slovene Society for Microbiology, Lubljana, pp. 597-602.
84. Yarlett, N., A. C. Hann, D. Llyod and A. G. Williams. 1983. Hydrogenosomes in a mixed isolate of Isotricha prostoma and Isotricha intestinalis from ovine rumen contents. Comp. Bioch. Physiol., 74 B, 357-364.