Effect of progressive inoculation of fauna-free sheep with holotrich protozoa and total-fauna on rumen fermentation, microbial diversity and methane emissions

FEMS Microbiology Ecology

Volumn 91, Issue 3, 2015, Pages

  Belanche, Alejandro ^a   De La Fuente, Gabriel ^a   Newbold, Charles J ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

Entodiniomorphids; Fermentation; Holotrichs; Methanogenesis; Methanogens; Rumen protozoa

Indexed keywords

ACETATE; AMMONIA; CILIATE; CONCENTRATION (COMPOSITION); DIGESTIBILITY; DIGESTIVE SYSTEM; FERMENTATION; FUNGUS; INOCULATION; METHANE; METHANOGENESIS; METHANOGENIC BACTERIUM; MICROBIAL COMMUNITY; ORGANIC ACID; SHEEP; SPECIES DIVERSITY;

BACTERIA (MICROORGANISMS); ENTODINIOMORPHIDA; FUNGI; OVIS ARIES; PROTOZOA;

AMMONIA; LACTIC ACID; METHANE; PROPIONIC ACID; PROPIONIC ACID DERIVATIVE;

ANIMAL; BIOSYNTHESIS; CILIATE; DIETARY FIBER; EURYARCHAEOTA; FERMENTATION; FUNGUS; HOST PARASITE INTERACTION; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RUMEN; SHEEP;

AMMONIA; ANIMALS; CILIOPHORA; DIETARY FIBER; EURYARCHAEOTA; FERMENTATION; FUNGI; HOST-PARASITE INTERACTIONS; LACTIC ACID; METHANE; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PROPIONATES; RUMEN; SHEEP;

EID: 84942325908     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiu026     Document Type: Article

References (57)

1. AFRC (Agricultural and Food Research Council). Energy and Protein Requirements of Ruminant. An Advisory Manual Prepared by the ARC Technical Committee on Response to Nutrients. Wallingford, U.K.: CAB International, 1993.
2. AOAC (Association of Official Analytical Chemists). Official Methods of Analysis of the AOAC, 18th edn. Arlington, VA, USA:AOAC, 2005.
3. Belanche A, Abecia L, Holtrop G, et al. Study of the effect of presence or absence of protozoa on rumen fermentation and microbial protein contribution to the chyme. J Anim Sci 2011;89:4163-74.
4. Belanche A, de la Fuente G, Moorby JM, et al. Bacterial protein degradation by different rumen protozoal groups. J Anim Sci 2012b;90:4495-504.
5. Belanche A, de la Fuente G, Newbold CJ. Study of methanogen communities associated with different rumen protozoal populations. FEMS Microbiol Ecol 2014;90:663-77.
6. Belanche A, de la Fuente G, Pinloche E, et al. Effect of diet and absence of protozoa on the rumen microbial community and on the representativeness of bacterial fractions used in the determination of microbial protein synthesis. J Anim Sci 2012a;90:3924-36.
7. Belanche A, Doreau M, Edwards JE, et al. Shifts in the rumen microbiota due to the type of carbohydrate and level of protein ingested by dairy cattle are associated with changes in rumen fermentation. J Nutr 2012c;142:1684-92.
8. Bird SH, Hegarty RS, Woodgate R. Persistence of defaunation effects on digestion and methane production in ewes. Aust J Exp Agr 2008;48:152-5.
9. Cecava MJ, Merchen NR, Gay LC, et al. Composition of ruminal bacteria harvested from steers as influenced by dietary energy level, feeding frequency, and isolation techniques. J Dairy Sci 1990;73:2480-8.
10. de la Fuente G, Cebrian JA, Fondevila M. A cryopreservation procedure for the rumen protozoon Entodinium caudatum: estimation of its viability by fluorescence microscopy. Lett Appl Microbiol 2004;38:164-8.
11. Dehority BA. Rumen Microbiology. Nottingham, UK: Nottingham University Press, 2003.
12. Dehority BA, Tirabasso PA. Factors affecting the migration and sequestration of rumen protozoa in the family Isotrichidae. J Gen Microbiol 1989;135:539-48.
13. Ellis JE, Williams AG, Lloyd D. Oxygen consumption by ruminal microorganism: protozoal and bacterial contributions. Appl Environ Microb 1989;55:2583-7.
14. Embley TM, van der Giezen M, Horner DS, et al. Hydrogenosomes, mitochondria and early eukaryotic evolution. Iubmb Life 2003;55:387-95.
15. Eugène M, Archimède H, Sauvant D. Quantitative meta-analysis on the effects of defaunation of the rumen on growth, intake and digestion in ruminants. Livest Prod Sci 2004;85:81-97.
16. Firkins JL, Yu Z. Characterisation and quantification of the microbial populations of the rumen. In: Sejrsen K, Hvelplund T, Nielson MO, (eds). Ruminant Physiology: Digestion, Metabolism and Impact of Nutrition on Gene Expression, Immunology and Stress. The Netherlands: Wageningen Academic Publishers, 2006, 19-54.
17. Hegarty RS. Mechanisms for competitively reducing ruminal methanogenesis. Aust J Agr Res 1999a;50:1299-305.
18. Hegarty RS. Reducing rumen methane emissions through elimination of rumen protozoa. Aust J Agr Res 1999b;50:1321-7.
19. Hegarty RS, Bird SH, Vanselow BA, et al. Effects of the absence of protozoa from birth or from weaning on the growth and methane production of lambs. Brit J Nutr 2008;100:1220-7.
20. Hill TCJ, Walsh KA, Harris JA, et al. Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 2003;43:1-11.
21. Hook SE, Wright A-DG, McBride BW. Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010;2010:1-11.
22. Hristov AN, Oh J, Firkins JL, et al. Special Topics-mitigation of methane and nitrous oxide emissions from animal operations:I. A review of enteric methane mitigation options. J Anim Sci 2013;91:5045-69.
23. Ivan M. Comparison of duodenal flow and digestibility in faunafree sheep inoculated with Holotrich protozoa, Entodinium monofauna or total mixed protozoa population. Brit J Nutr 2009;101:34-40.
24. Ivan M, Neill L, Entz T. Ruminal fermentation and duodenal flow following progressive inoculations of fauna-free wethers with major individual species of ciliate protozoa or total fauna. J Anim Sci 2000;78:750-9.
25. Jami E, Israel A, Kotser A, et al. Exploring the bovine rumen bacterial community from birth to adulthood. ISME J 2013;7:1069-79.
26. Johnson KA, Johnson DE. Methane emissions from cattle. J Anim Sci 1995;73:2483-92.
27. Koenig KM, Newbold CJ, McIntosh FM, et al. Effects of protozoa on bacterial nitrogen recycling in the rumen. J Anim Sci 2000;78:2431-45.
28. Krumholz LR, Forsberg CW, Veira DM. Association of methanogenic bacteria with rumen protozoa. Can J Microbiol 1983;29:676-80.
29. Leahy SC, Kelly WJ, Ronimus RS, et al. Genome sequencing of rumen bacteria and archaea and its application to methane mitigation strategies. Animal 2013;2:235-43.
30. Lloyd D, Hillman K, Yarlett N, et al. Hydrogen production by rumen holotrich protozoa: effects of oxygen and implications for metabolic control by in situ conditions. J Protozool 1989;36:205-13.
31. McAllister TA, Newbold CJ. Redirecting rumen fermentation to reduce methanogenesis. Aust J Exp Agr 2008;48:7-13.
32. Morgavi DP, Forano E, Martin C, et al. Microbial ecosystem and methanogenesis in ruminants. Animal 2010;4:1024-36.
33. Morgavi DP, Martin C, Jouany JP, et al. Rumen protozoa and methanogenesis: not a simple cause-effect relationship. Brit J Nutr 2011;107:388-97.
34. Morgavi DP, Popova M, Rathahao-Paris E, et al. Historical colonization events and age shape rumen microbial communities and metabolic phenotypes in lambs. In: Rowett INRA (eds) Proceedings of Gut Microbiology: from Sequence to Function. Aberdeen, UK, 2014, 142.
35. Mosoni P, Martin C, Forano E, et al. Long-term defaunation increases the abundance of cellulolytic ruminococci and methanogens but does not affect the bacterial and methanogen diversity in the rumen of sheep. J Anim Sci 2011;89:783-91.
36. Moss AR, Jouany JP, Newbold CJ. Methane production by ruminants:its contribution to global warming. Ann Zootech 2000;49:231-53.
37. Newbold CJ, Lassalas B, Jouany JP. The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Lett Appl Microbiol 1995;21:230-4.
38. Ohene-Adjei S, Teather RM, Ivanj M, et al. Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Appl Environ Microb 2007;73:4609-18.
39. Orpin CG, Hall FJ. Surface structures of the rumen holotrich protozoon Isotricha intestinalis with particular reference to the attachment zone. Curr Microbiol 1983;8:321-5.
40. Ozutsumi Y, Tajima K, Takenaka A, et al. The effect of protozoa on the composition of rumen bacteria in cattle using 16S rRNA gene clone libraries. Biosci Biotech Bioch 2005;69:499-506.
41. Paul RG, Williams AG, Butler RD. Hydrogenosomes in the rumen Entodiniomorphid ciliate Polyplastron multivesiculatum. J Gen Microbiol 1990;136:1981-9.
42. PfafflMW. A newmathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:2002-7.
43. Snyers L, Hellings P, Bovy-Kesler C, et al. Occurrence of hydrogenosomes in the rumen ciliates Ophryoscolecidae. FEBS Lett 1982;137:35-9.
44. Sylvester JT, Karnati SKR, Yu ZT, et al. Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. J Nutr 2004;134:3378-84.
45. Tymensen LD, Beauchemin KA, McAllister TA. Structures of freeliving and protozoa-associated methanogen communities in the bovine rumen differ according to comparative analysis of 16S rRNA and mcrA genes. Microbiol-SGM 2012;158:1808-17.
46. Ushida K. Symbiotic methanogens and rumen ciliates. In:Hackstein JHP (ed). (Endo) Symbiotic Methanogens. Heidelberg:Springer, 2010.
47. Ushida K, Jouany JP. Methane production associated with rumen-ciliated protozoa and its effect on protozoan activity. Lett Appl Microbiol 1996;23:129-32.
48. Van Soest PJ, Robertson JB, Lewis BA. Methods of dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 1991;74:3583-97.
49. Wallace RJ, Rooke JA, Duthie C-A, et al. Archaeal abundance in post-mortem ruminal digesta may help predict methane emissions from beef cattle. Sci Rep 2014;4:5892.
50. Weimer PJ, Stevenson DM, Mantovani HC, et al. Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. J Dairy Sci 2010;93:5902-12.
51. Williams AG. Rumen holotrich ciliate protozoa. Microbiol Rev 1986;50:25-49.
52. Williams AG. The metabolic activity of rumen protozoa. In:Nolan JN, Leng RA, Demeyer DI (eds). The Roles of Protozoa and Fungi in Ruminant Digestion. Armidale, Australia: Penambul Books, 1989.
53. Williams AG, Coleman GS. The Rumen Protozoa. New York:Springer-Verlag Inc., 1992.
54. Wolk A, Vessby B, Ljung H, et al. Evaluation of a biological marker of dairy fat intake. Am J Clin Nutr 1998;68:291-5.
55. Yáñez-Ruiz DR, Hart KJ, Martin-Garcia AI, et al. Diet composition at weaning affects the rumen microbial population and methane emissions by lambs. Aust J Exp Agr 2008;48:186-8.
56. Yanez-Ruiz DR, Macias B, Pinloche E, et al. The persistence of bacterial and methanogenic archaeal communities residing in the rumen of young lambs. FEMS Microbiol Ecol 2010;72:272-8.
57. Yáñez-Ruiz DR, Williams S, Newbold CJ. The effect of absence of protozoa on rumen biohydrogenation and the fatty acid composition of lamb muscle. Brit J Nutr 2007;97:938-48.