Changes in bacterial diversity associated with epithelial tissue in the beef cow rumen during the transition to a high-grain diet

Applied and Environmental Microbiology

Volumn 77, Issue 16, 2011, Pages 5770-5781

  Chen, Yanhong ^a   Penner, Gregory B ^a,b   Li, Meiju ^a   Oba, Masahito ^a   Guan, Le Luo ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; BACTERIAL COMMUNITY; BACTERIAL DIVERSITY; BACTERIAL POPULATION; BEEF HEIFERS; COMMUNITY IS; CONTROL GROUPS; COPY NUMBER; EPITHELIAL TISSUE; FATTY ACID METABOLISM; FIRMICUTES; GRADIENT GEL ELECTROPHORESIS; IN-CONTROL; ISOVALERATE; MOLAR PROPORTIONS; PCR-DGGE; PROTEOBACTERIA; QUANTITATIVE REAL TIME PCR;

BACTERIA; ELECTROPHORESIS; GENES; NUTRITION; POLYMERASE CHAIN REACTION; POPULATION STATISTICS; RNA; TISSUE; VOLATILE FATTY ACIDS;

BACTERIOLOGY;

RNA 16S; VOLATILE FATTY ACID;

ADAPTIVE RADIATION; BACTERIUM; CATTLE; DIET; ELECTROKINESIS; ESTIMATION METHOD; FATTY ACID; GEL; GENE EXPRESSION; METABOLISM; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; QUANTITATIVE ANALYSIS; SPECIES DIVERSITY;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; BACTERIAL GENE; BACTEROIDETES; BIOPSY; BIOTA; CATTLE; CEREAL; CHEMISTRY; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; FEMALE; FERMENTATION; GENE DOSAGE; GENETIC VARIABILITY; GENETICS; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGY; PH; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; PROTEOBACTERIA; RANDOMIZED CONTROLLED TRIAL; RNA GENE; RUMINANT STOMACH;

ANIMAL FEED; ANIMALS; BACTEROIDETES; BIOPSY; BIOTA; CATTLE; CEREALS; DENATURING GRADIENT GEL ELECTROPHORESIS; FATTY ACIDS, VOLATILE; FEMALE; FERMENTATION; GENE DOSAGE; GENES, BACTERIAL; GENES, RRNA; GENETIC VARIATION; HYDROGEN-ION CONCENTRATION; INTESTINAL MUCOSA; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; RUMEN;

BACTERIA (MICROORGANISMS); BACTEROIDETES; BOVINAE; FIRMICUTES; LACHNOSPIRACEAE; PROTEOBACTERIA; RUMINOBACTER; TREPONEMA SP.;

EID: 80052627204     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00375-11     Document Type: Article

References (52)

1. Acinas, S. G., L. A. Marcelino, V. Klepac-Ceraj, and F. P. Martin. 2004. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186:2629-2635.
2. Ben-Dov, E., O. H. Shapiro, N. Siboni, and A. Kushmaro. 2006. Advantage of using inosine at the 3' termini of 16S rRNA gene universal primers for the study of microbial diversity. Appl. Environ. Microbiol. 72:6902-6906.
3. Case, R. J., et al. 2007. Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl. Environ. Microbiol. 73:278-288.
4. Cheng, K. J., and J. W. Costerton. 1986. Microbial adhesion and colonization within the digestive tract. Soc. Appl. Bacteriol. Symp. Ser. 13:239-261.
5. Cheng, K. J., C. B. M. Bailey, R. Hironaka, and J. W. Costerton. 1979. A technique for depletion of bacteria adherent to the epithelium of the bovine rumen. Can. J. Anim. Sci. 59:207-209.
6. Cheng, K. J., R. P. McCowan, and J. W. Costerton. 1979. Adherent epithelial bacteria in ruminants and their roles in digestive tract function. Am. J. Clin. Nutr. 32:139-148.
7. Cho, S. J., et al. 2006. 16S rDNA analysis of bacterial diversity in three fractions of cow rumen. J. Microbiol. Biotechnol. 16:92-101.
8. Crosby, L. D., and C. S. Criddle. 2003. Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34:790-794.
9. Dahllöf, I., H. Baillie, and S. Kjelleberg. 2000. rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecies heterogeneity. Appl. Environ. Microbiol. 66:3376-3380.
10. Fay, J. P., K. J. Cheng, and J. W. Costerton. 1979. Production of alkaline phosphatase by epithelial cells and adherent bacteria of the bovine rumen and abomasum. Can. J. Microbiol. 25:932-936.
11. Fromin, N., et al. 2002. Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ. Microbiol. 4:634-643.
12. Fuente, G. D. L., K. Skirnisson, and B. A. Dehority. 2006. Rumen ciliate fauna of Icelandic cattle, sheep, goats and reindeer. Zootaxa 1377:47-60.
13. Ghorbani, G. R., D. P. Morgavi, K. A. Beauchemin, and J. A. Z. Leedle. 2002. Effects of bacterial direct-fed microbials on ruminal fermentation, blood variables, and the microbial population of feedlot cattle. J. Anim. Sci. 80: 1977-1986.
14. Guan, L. L., et al. 2003. Detection and identification of Lactobacillus species in crops of broilers of different ages by using PCR-denaturing gradient gel electrophoresis and amplified ribosomal DNA restriction analysis. Appl. Environ. Microbiol. 69:6750-6757.
15. Hernandez-Sanabria, E., et al. 2010. Correlation of particular bacterial PCR-denaturing gradient gel electrophoresis patterns with bovine ruminal fermentation parameters and feed efficiency traits. Appl. Environ. Microbiol. 76:6338-6350.
16. Hungate, R. E. 1966. The rumen and its microbes. Academic Press, New York, NY.
17. Klappenbach, J. A., J. M. Dunbar, and T. M. Schmidt. 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66:1328-1333.
18. Kocherginskaya, S. A., R. I. Aminov, and B. A. White. 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.
19. Konishi, I., et al. 2009. Phylogenetic analyses and detection of viridans streptococci based on sequences and denaturing gradient gel electrophoresis of the rod shape-determining protein gene. J. Oral Microbiol. doi:10.3402/ jom.v1i0.2015.
20. Küpfer, M., P. Kuhnert, B. M. Korczak, R. Peduzzi, and A. Demarta. 2006. Genetic relationships of Aeromonas strains inferred from 16S rRNA, gyrB and rpoB gene sequences. Int. J. Syst. Evol. Microbiol. 56:2743-2751.
21. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 115-175. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. Wiley, New York, NY.
22. Ley, R. E., et al. 2008. Evolution of mammals and their gut microbes. Science 320:1647-1651.
23. Li, M., G. B. Penner, E. Hernandez-Sanabria, M. Oba, and L. L. Guan. 2009. Effects of sampling location and time, and host animal on assessment of bacterial diversity and fermentation parameters in the bovine rumen. J. Appl. Microbiol. 107:1924-1934.
24. Martin, C., G. Fonty, and B. Michalet-Doreau. 2002. Factors affecting the fibrolytic activity of the digestive microbial ecosystems in ruminants, p. 1-17. In S. A. Martin (ed.), Gastrointestinal microbiology in animals. Research Signpost, Trivandrum, Kerala, India.
25. McCowan, R. P., K. J. Cheng, C. B. M. Bailey, and J. W. Costerton. 1978. Adhesion of bacteria to epithelial cell surfaces within the reticulo-rumen of cattle. Appl. Environ. Microbiol. 35:149-155.
26. McCowan, R. P., K. J. Cheng, and J. W. Costerton. 1980. Adherent bacterial populations on the bovine rumen wall: distribution patterns of adherent bacteria. Appl. Environ. Microbiol. 39:233-241.
27. Mitsumori, M., N. Ajisaka, K. Tajima, H. Kajikawa, and M. Kurihara. 2002. Detection of Proteobacteria from the rumen by PCR using methanotrophspecific primers. Lett. Appl. Microbiol. 35:251-255.
28. Nagaraja, T. G., and E. C. Titgemeyer. 2007. Ruminal acidosis in beef cattle: the current microbiological and nutritional outlook. J. Dairy Sci. 90:E17- E38.
29. Nicol, G. W., L. A. Glover, and J. I. Prosser. 2003. Spatial analysis of archaeal community structure in grassland soil. Appl. Environ. Microbiol. 69:7420-7429.
30. Penner, G. B., K. A. Beauchemin, and T. Mutsvangwa. 2006. An evaluation of the accuracy and precision of a stand-alone submersible continuous ruminal pH measurement system. J. Dairy Sci. 89:2132.
31. Powell, S. M., S. H. Ferguson, J. P. Bowman, and I. Snape. 2006. Using real-time PCR to assess changes in the hydrocarbon-degrading microbial community in Antarctic soil during bioremediation. Microb. Ecol. 52:523-532.
32. Rieu, F., G. Fonty, B. Gaillard, and P. Gouet. 1990. Electron microscopy study of the bacteria adherent to the rumen wall in young conventional lambs. Can. J. Microbiol. 36:140-144.
33. Russell, J. B. 2002. Rumen microbiology and its role in ruminant nutrition. Cornell University, Ithaca, NY.
34. Russell, J. B., M. R. Garner, and J. P. Flint. 2002. Allisonella histiformans, sp. nov., a novel bacterium that produces histamine, utilizes histidine as its sole energy source, and could play a role in bovine and equine laminitis. Syst. Appl. Microbiol. 25:498-506.
35. Sadet, S., C. Martin, B. Meunier, and D. P. Morgavi. 2007. PCR-DGGE analysis reveals a distinct diversity in the bacterial population attached to the rumen epithelium. Animal 1:939-944.
36. Sadet-Bourgeteau, S., C. Martin, and D. P. Morgavi. 2010. Bacterial diversity dynamics in rumen epithelium of wethers fed forage and mixed concentrate forage diets. Vet. Microbiol. 146:98-104.
37. Santos, S. R., and H. Ochman. 2004. Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ. Microbiol. 6:754-759.
38. SAS Institute. 1998. SAS user's guide, version 7. SAS Institute, Inc., Cary, NC.
39. Schwartzkopf-Genswein, K. S., et al. 2003. Effect of bunk management on feeding behavior, ruminal acidosis and performance of feedlot cattle: A review. J. Anim. Sci. 81:E149-E158.
40. Silveira, C., M. Oba, W. Z. Yang, and K. A. Beauchemin. 2007. Selection of barley grain affects ruminal fermentation, starch digestibility, and productivity of lactating dairy cows. J. Dairy Sci. 90:2860-2869.
41. Stevenson, D. M., and P. J. Weimer. 2007. Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl. Microbiol. Biotechnol. 75:165-174.
42. Stewart, C. S., H. J. Flint, and M. P. Bryant. 1997. The rumen bacteria, p:10-72. In P. N. Hobson and C. S. Stewart (ed.), The rumen microbial ecosystem, 2nd ed. Springer-Verlag, New York, NY.
43. Tajima, K., et al. 1999. Rumen bacterial diversity as determined by sequence analysis of 16S rDNA libraries. FEMS Microbiol. Ecol. 29:159-169.
44. Tajima, K., et al. 2000. Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe 6:273-284.
45. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies formultiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
46. Varel, V. H., and B. A. Dehority. 1989. Ruminal cellulolytic bacteria and protozoa from bison, cattle-bison hybrids, and cattle fed three alfalfa-corn diets. Appl. Environ. Microbiol. 55:148-153.
47. Wallace, R. J., K. J. Cheng, D. Dinsdale, and E. R. Orskov. 1979. An independent microbial flora of the epithelium and its role in the ecomicrobiology of the rumen. Nature 279:424-426.
48. Walter, J., et al. 2001. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67: 2578-2585.
49. Walter, J., et al. 2000. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl. Environ. Microbiol. 66:297-303.
50. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
51. Weimer, P. J., D. M. Stevenson, and D. R. Mertens. 2010. Shifts in bacterial community composition in the rumen of lactating dairy cows under milk fat-depressing conditions. J. Dairy. Sci. 93:265-278.
52. Zhou, M., E. Hernandez-Sanabria, and L. L. Guan. 2010. Characterization of variation in rumen methanogenic communities under different dietary and host feed efficiency conditions, as determined by PCR-denaturing gradient gel electrophoresis analysis. Appl. Environ. Microbiol. 76:3776-3786.