Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Linking rumen function to animal response by application of metagenomics techniques

J. L. Firkins A B , S. K. R. Karnati A and Z. Yu A
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, The Ohio State University, Columbus, OH 43210, USA.

B Corresponding author. Email: firkins.1@osu.edu

Australian Journal of Experimental Agriculture 48(7) 711-721 https://doi.org/10.1071/EA08028
Submitted: 11 January 2008  Accepted: 30 March 2008   Published: 20 June 2008

Abstract

Metagenomics techniques applied to the rumen microbiota have demonstrated tremendous diversity originally among populations of bacteria and, more recently, among the methanogenic archaea, including those associated with protozoa. Although with some potential limitations, cluster analyses of sequences recovered from clone libraries have revealed differences in populations among animals fed forage v. grain, including amylolytic ruminococci and novel groups of clostridia adhering to the rumen particulates. Rapid profiling procedures, such as denaturing gradient gel electrophoresis (DGGE), can be used to infer likely differences in community structure of bacteria and archaea among numerous replicates of animals and times after feeding diets that are more representative of intense ruminant animal production. Metagenomics procedures also are being applied to issues related to ruminal output of fatty acid isomers influencing milk fat composition and consumer acceptance, the environmental impact of nitrogen in animal waste and methane emissions, and future potential approaches to improve ruminal fibre digestibility. If varying concentrations of ruminal metabolites and fluxes quantified from microbial processes can be combined with results from metagenomics applied to rumen microbiota, then we should reduce the unexplained variability in models in which the prediction of nutrient supply to the intestine is synchronised with nutritional guidelines for more efficient feed conversion by ruminants.


Acknowledgements

The studies in our laboratories were supported by National Research Initiative Competitive Grant no. 2003–35206–12872 from the USDA Cooperative State Research, Education, and Extension Service.


References


Allen MS (2000) Effects of diet on short-term regulation of feed intake by lactating dairy cattle. Journal of Dairy Science 83, 1598–1624.
CAS | PubMed |
[Verified 9 April 2008]

Karnati SKR, Sylvester JT, Noftsger SM, Yu Z, St-Pierre NR, Firkins JL (2007) Assessment of ruminal bacterial populations and protozoal generation time in cows fed different methionine sources. Journal of Dairy Science 90, 798–809.
CAS | PubMed |
open url image1

Klieve AV, Hennessey D, Ouwerkerk D, Forster RJ, Mackie RI, Attwood GT (2003) Establishing populations of Megasphaera elsdenii YE34 and Butyrivibrio fibrisolvens YE44 in the rumen of cattle fed high grain diets. Journal of Applied Microbiology 95, 621–630.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Klieve AV, O’Leary MN, McMillen L, Ouwerkerk D (2007) Ruminococcus bromii, identification and isolation as a dominant community member in the rumen of cattle fed a barley diet. Journal of Applied Microbiology 103, 2065–2073.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kocherginskaya S, Aminov RI, White BA (2001) Analysis of the rumen bacterial diversity under two different diet conditions using denaturing gradient gel electrophoresis, random sequencing, and statistical ecology approaches. Anaerobe 7, 119–134.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Koenig KM, Ivan M, Teferedegne BT, Morgavi DP, Rode LM, Ibrahim IM, Newbold CJ (2007) Effect of dietary Enterolobium cyclocarpum on microbial protein flow and nutrient digestibility in sheep maintained fauna-free, with total mixed fauna or with Entodinium caudatum monofauna.  British Journal of Nutrition 98, 504–516.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Konstantinidis K, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: Advancements and challenges ahead. Current Opinion in Microbiology 10, 504–509.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Krause DO, Bunch RJ, Conlan LL, Kennedy PM, Smith WJ, Mackie RI, McSweeney CS (2001) Repeated ruminal dosing of Ruminococcus spp. does not result in persistence, but changes in other microbial populations occur that can be measured with quantitative 16S-rRNA-based probes. Microbiology 147, 1719–1729.
CAS | PubMed |
open url image1

Krause DO, Denman SE, Mackie RI, Morrison M, Rae AL, Attwood GT, McSweeney CS (2003) Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiology Reviews 27, 663–693.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Larue R, Yu Z, Parisi VA, Egan AR, Morrison M (2005) Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing. Environmental Microbiology 7, 530–543.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Leggewie C, Henning H, Schmeisser C, Streit WR, Jaeger KE (2006) A novel transposon for functional expression of DNA libraries. Journal of Biotechnology 123, 281–287.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Love JL, Scholes P, Gilpin B, Savill M, Lin S, Samuel L (2006) Evaluation of uncertainty in quantitative real-time PCR. Journal of Microbiological Methods 67, 349–356.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Maia MRG, Chaudhary LC, Figueres L, Wallace RJ (2007) Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie Van Leeuwenhoek 91, 303–314.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

McAllister TA, Newbold CJ (2008) Redirecting rumen fermentation to reduce methanogenesis. Australian Journal of Experimental Agriculture 48, 7–13.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Mouriño F, Akkarawongsa R, Weimer PJ (2001) Initial pH as a determinant of cellulose digestion rate by mixed ruminal microorganisms in vitro. Journal of Dairy Science 84, 848–859.
PubMed |
open url image1

Nagaraja TG, Titgemeyer EC (2007) Ruminal acidosis in beef cattle: the current microbiological and nutritional outlook. Journal of Dairy Science 90(E. Suppl), E17–E38.
PubMed |
open url image1

Ohene-Adjei S, Teather RM, Ivan M, Forster RJ (2007) Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Applied and Environmental Microbiology 73, 4609–4618.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Paillard D, McKain N, Chaudhary LC, Walker ND, Pizette F , et al. (2007) Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen. Antonie Van Leeuwenhoek 91, 417–422.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Palackal N, Lyon CS, Zaidi S, Luginbül P, Dupree P , et al. (2007) A multifunctional hybrid glycosyl hydrolase discovered in an uncultured microbial consortium from ruminant gut. Applied Microbiology and Biotechnology 74, 113–124.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pinares-Patiño CS, Clark H (2008) Reliability of the sulfur hexafluoride tracer techniques for methane emission measurement from individual animals: an overview. Australian Journal of Experimental Agriculture 48, 223–229.
Crossref | GoogleScholarGoogle Scholar | open url image1

Potter EL, Dehority BA (1973) Effects of changes in feed level, starvation, and level of feed after starvation upon the concentration of rumen protozoa in the ovine. Applied Microbiology 26, 692–698.
CAS | PubMed |
open url image1

Russell JB, Mantovani HC (2002) The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. Journal of Molecular Microbiology and Biotechnology 4, 347–355.
CAS | PubMed |
open url image1

Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the gordian knot. Genome Biology 6, 229.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Selinger LB, Forsberg CW, Cheng K-J (1996) The rumen: a unique source of enzymes for enhancing livestock production. Anaerobe 2, 263–284.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Shinkai T, Kobayashi T (2007) Localization of ruminal cellulolytic bacteria on plant fibrous materials as determined by fluorescence in situ hybridization and real-time PCR. Applied and Environmental Microbiology 73, 1646–1652.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Stewart CS , Flint HJ , Bryant MP (1997) The rumen bacteria. In ‘The rumen microbial ecosystem’. (Eds PN Hobson, CS Stewart) pp. 10–72. (Blackie Academic & Professional: New York)

Sylvester JT, Karnati SKR, Yu Z, Morrison M, Firkins JL (2004) Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. Journal of Nutrition 134, 3378–3384.
CAS | PubMed |
open url image1

Sylvester JT, Karnati SKR, Yu Z, Newbold CJ, Firkins JL (2005) Evaluation of a real-time PCR assay for measuring the ruminal pool and duodenal flow of protozoal nitrogen. Journal of Dairy Science 88, 2083–2095.
CAS | PubMed |
open url image1

Sylvester JT (2005) Development and evaluation of new techniques to quantify ruminal pool size and duodenal flow of protozoal nitrogen. PhD Dissertation. The Ohio State University, Columbus, OH.

Tajima K, Arai S, Ogata K, Nagamine T, Matsui H, Nakamura M, Aminov RI, Benno Y (2000) Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe 6, 273–284.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Takenaka A, D’Silva CG, Kudo H, Itabashi H, Cheng K-J (1999) Molecular cloning, expression, and characterization of an endo-beta-1,4-glucanase cDNA from Epidinium caudatum. Journal of General and Applied Microbiology 45, 57–61.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Tringe SG, Rubin EM (2005) Metagenomics: DNA sequencing of environmental samples. Nature Reviews. Genetics 6, 805–814.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Walker ND , Newbold CJ , Wallace RJ (2005) Nitrogen metabolism in the rumen. In ‘Nitrogen and phosphorus nutrition of cattle’. (Eds E Pfeffer, A Hristov) pp. 71–115. (CABI Publishing: Cambridge, MA)

Willems A, Amat-Marco M, Collins MD (1996) Phylogenetic analysis of Butyrivibrio strains reveals three distinct groups of species within the Clostridium subphylum of the Gram-positive bacteria. International Journal of Systematic Bacteriology 46, 195–199.
CAS | PubMed |
open url image1

Wright A-DG, Auckland CH, Lynn DH (2007) Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Applied and Environmental Microbiology 73, 4206–4210.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yáñez-Ruiz DR, Scollan ND, Merry RJ, Newbold CJ (2006) Contribution of rumen protozoa to duodenal flow of nitrogen, conjugated linoleic acid and vaccenic acid in steers fed silages differing in their water-soluble carbohydrate content. British Journal of Nutrition 96, 861–869.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yáñez-Ruiz DR, Williams S, Newbold CJ (2007) The effect of absence of protozoa on rumen biohydrogenation and the fatty acid composition of lamb muscle. British Journal of Nutrition 97, 938–948.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yu Z, Morrison M (2004) Comparisons of different hypervariable regions of rrs genes for use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 70, 4800–4806.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yu Z, Yu M, Morrison M (2006) Improved serial analysis of V1 ribosomal sequence tags (SARST-V1) provides a rapid, comprehensive, sequence-based characterization of bacterial diversity and community composition. Applied and Environmental Microbiology 8, 603–611.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Yu Z, García-González R, Schanbacher FL, Morrison M (2008) Evaluations of different hypervariable regions of archaeal 16S rRNA genes in profiling of methanogens by Archaea-specific PCR and denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 74, 889–893.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yun J, Ryu S (2005) Screening for novel enzymes from metagenome and SIGEX, as a way to improve it. Microbial Cell Factories 4, 8.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhu YX, Wang JQ, Ma RL, Huang L, Dong ZY (2007) Construction and analysis of rumen bacterial artificial chromosome library from a dairy cow rumen microflora. Acta Microbiologica Sinica [In Chinese] 47, 213–216.
CAS | PubMed |
open url image1