Cecum microbial communities from steers differing in feed efficiency

Journal of Animal Science

Volumn 93, Issue 11, 2015, Pages 5327-5340

  Myer, P R ^a,b   Wells, J E ^a   Smith, T P L ^a   Kuehn, L A ^a   Freetly, H C ^a  

^a U S MEAT ANIMAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

16S ribosomal ribonucleic acid; Cecum; Feed efficiency; Microbiome; Operational taxonomic units

Indexed keywords

BACTERIAL RNA; RNA 16S;

ANALYSIS; ANIMAL; ANIMAL FOOD; BACTERIUM; BOVINE; CECUM; CLASSIFICATION; ENERGY METABOLISM; GENETICS; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; PHYSIOLOGY; RUMEN;

ANIMAL FEED; ANIMALS; BACTERIA; CATTLE; CECUM; ENERGY METABOLISM; MALE; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; RUMEN;

EID: 84975456380     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2015-9415     Document Type: Article

References (50)

1. Abo-Ismail, M. K., G. Vander Voort, J. J. Squires, K. C. Swanson, I. B. Mandell, X. Liao, P. Stothard, S. Moore, G. Plastow, and S. P. Miller. 2014. Single nucleotide polymorphisms for feed efficiency and performance in crossbred beef cattle. BMC Genet. 15:14. doi:10.1186/1471-2156-15-14.
2. Armstrong, D. G., and R. R. Smithard. 1979. The fate of carbohydrates in the small and large intestines of the ruminant. Proc. Nutr. Soc. 38:283-294. doi:10.1079/PNS19790050.
3. Aronesty, E. 2011. ea-utils: Command-line tools for processing biological sequencing data. http://code.google.com/p/ea-utils. (Accessed 14 January 2014)
4. Arthur, P. F., R. M. Herd, J. F. Wilkins, and J. A. Archer. 2005. Maternal productivity for Angus cows divergently selected for post-weaning residual feed intake. Aust. J. Exp. Agric. 45:985-993. doi:10.1071/EA05052.
5. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc., B 57:289-300.
6. Biddle, A., L. Stewart, J. Blanchard, and S. Leschine. 2013. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5:627-640. doi:10.3390/d5030627.
7. Blankenberg, D., A. Gordon, G. Von Kuster, N. Coraor, J. Taylor, A. Nekrutenko, and the Galaxy Team. 2010. Manipulation of FASTQ data with Galaxy. Bioinformatics 26:1783-1785. doi:10.1093/bioinformatics/btq281.
8. Caporaso, J. G., J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, and R. Knight. 2010. Qiime allows analysis of high throughput community sequencing data. Nat. Methods 7:335-336. doi:10.1038/nmeth.f.303.
9. Chung, H., S. J. Pamp, J. A. Hill, N. J. Surana, and S. M. Edelman. 2012. Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149:1578-1593. doi:10.1016/j. cell.2012.04.037.
10. Cotta, M. A. 1992. Interaction of ruminal bacteria in the production and utilization of maltooligosaccharides from starch. Appl. Environ. Microbiol. 58:48-54.
11. Cuiv, P. O., E. S. Klaassens, A. S. Durkin, D. M. Harkins, L. Foster, J. McCorrison, M. Torralba, K. E. Nelson, and M. Morrison. 2011. Draft genome sequence of Turicibacter sanguinis PC909, isolated from human feces. J. Bacteriol. 193:1288-1289. doi:10.1128/ JB.01328-10.
12. Daniel, H., A. M. Gholami, D. Berry, C. Desmarchelier, H. Hahne, G. Loh, S. Mondot, P. Lepage, M. Rothballer, A. Walker, C. Bohm, M. Wenning, M. Wagner, M. Blaut, P. Schmitt-Kopplin, B. Kuster, D. Haller, and T. Clavel. 2014. High-fat diet alters gut microbiota physiology in mice. ISME J. 8:295-308. doi:10.1038/ismej.2013.155. de
13. Oliveira, M. N., K. A. Jewell, F. S. Freitas, L. A. Benjamin, M. R. Tótola, A. C. Borges, C. A. Moraesa, and G. Suen. 2013. Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer. Vet. Microbiol. 164:307-314. doi:10.1016/j.vetmic.2013.02.013.
14. DeSantis, T. Z., P. Hugenholtz, N. Larsen, M. Rojas, E. L. Brodie, K. Keller, T. Huber, D. Dalevi, P. Hu, and G. L. Andersen. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069-5072. doi:10.1128/AEM.03006-05.
15. Edgar, R. C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. doi:10.1093/bioinformatics/ btq461.
16. Eren, A. M., M. L. Sogin, H. G. Morrison, J. H. Vineis, J. C. Fisher, R. J. Newton, and S. L. McLellan. 2015. A single genus in the gut microbiome reflects host preference and specificity. ISME J. 9:90-100. doi:10.1038/ismej.2014.97.
17. Federation of Animal Science Societies (FASS). 2010. Guide for the care and use of agricultural animals in agricultural research and teaching. 3rd ed. FASS, Savoy, IL.
18. Galyean, M. L., C. Ponce, and J. Schutz. 2011. The future of beef production in North America. Anim. Front. 1:29-36. doi:10.2527/ af.2011-0013.
19. Haas, B. J., D. Gevers, A. M. Earl, M. Feldgarden, D. V. Ward, G. Giannoukos, D. Ciulla, D. Tabbaa, S. K. Highlander, E. Sodergren, B. Methé, T. Z. DeSantis, J. F. Petrosino, R. Knight, and B. W. Birren The Human Microbiome Consortium 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21:494-504. doi:10.1101/gr.112730.110.
20. Hernandez-Sanabria, E., L. A. Goonewardene, Z. Wang, O. N. Durunna, S. S. Moore, and L. L. Guan. 2012. Impact of feed efficiency and diet on adaptive variations in the bacterial community in the rumen fluid of cattle. Appl. Environ. Microbiol. 78:1203-1214. doi:10.1128/AEM.05114-11.
21. Ismail, N. A., S. H. Ragab, A. A. ElBaky, A. R. Shoeib, Y. Alhosary, and D. Fekry. 2010. Frequency of Firmicutes and Bacteroidetes in gut microbiota of obese and normal weight Egyptian children and adults. Arch. Med. Sci. 7:501-507.
22. Jami, E., B. A. White, and I. Mizrahi. 2014. Potential role of the bovine rumen microbiome in modulating milk composition and feed efficiency. PLoS ONE 9:e85423. doi:10.1371/journal.pone.0085423.
23. Kim, M., J. Kim, L. A. Kuehn, J. L. Bono, E. D. Berry, N. Kalchayanand, H. C. Freetly, A. K. Benson, and J. E. Wells. 2014. Investigation of bacterial diversity in the feces of cattle fed different diets. J. Anim. Sci. 92:683-694. doi:10.2527/jas.2013-6841.
24. Kim, M., M. Morrison, and Z. Yu. 2011. Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol. Ecol. 76:49-63. doi:10.1111/j.1574-6941.2010.01029.x.
25. Kohl, K. D., J. Amaya, C. A. Passement, M. D. Dearing, and M. D. McCue. 2014. Unique and shared responses of the gut microbiota to prolonged fasting: A comparative study across five classes of vertebrate hosts. FEMS Microbiol. Ecol. 90:883-894. doi:10.1111/1574-6941.12442.
26. Ley, R. E., M. Hamady, C. Lozupone, P. J. Turnbaugh, R. R. Ramey, J. S. Bircher, M. L. Schlegel, T. A. Tucker, M. D. Schrenzel, R. Knight, and J. I. Gordon. 2008. Evolution of mammals and their gut microbes. Science 320:1647-1651. doi:10.1126/science.1155725.
27. Lindholm-Perry, A. K., L. A. Kuehn, W. T. Oliver, A. K. Sexten, J. R. Miles, L. A. Rempel, R. A. Cushman, and H. C. Freetly. 2013. Adipose and muscle tissue gene expression of two genes (NCAPG and LCORL) located in a chromosomal region associated with cattle feed intake and gain. PLoS ONE 8:e80882. doi:10.1371/journal.pone.0080882.
28. Lozupone, C. A., M. Hamady, S. T. Kelley, and R. Knight. 2007. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73:1576-1585. doi:10.1128/ AEM.01996-06.
29. Lozupone, C. A., and R. Knight. 2005. Unifrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228-8235. doi:10.1128/AEM.71.12.8228-8235.2005.
30. Lozupone, C. A., M. E. Lladser, D. Knights, J. Stombaugh, and R. Knight. 2011. UniFrac: An effective distance metric for microbial community comparison. ISME J. 5:169-172. doi:10.1038/ ismej.2010.133.
31. Mackie, R. I., R. I. Aminov, W. Hu, A. V. Klieve, D. Ouwerkerk, M. A. Sundset, and Y. Kamagata. 2003. Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Appl. Environ. Microbiol. 69:6808-6815. doi:10.1128/ AEM.69.11.6808-6815.2003.
32. Malmuthuge, N., and P. J. Griebel. 2014. Taxonomic identification of commensal bacteria associated with the mucosa and digesta throughout the gastrointestinal tracts of preweaned calves. Appl. Environ. Microbiol. 80:2021-2028. doi:10.1128/AEM.03864-13.
33. Mao, S., R. Zhang, D. Wang, and W. Zhu. 2012. The diversity of the fecal bacterial community and its relationship with the concentration of volatile fatty acids in the feces during subacute rumen acidosis in dairy cows. BMC Vet. Res. 8:237. doi:10.1186/1746-6148-8-237.
34. McCann, J. C., L. M. Wiley, T. D. Forbes, F. M. Rouquette Jr., and L. O. Tedeschi. 2014. Relationship between the rumen microbiome and residual feed intake efficiency of Brahman bulls stocked on bermudagrass pastures. PLoS ONE 9:e91864. doi:10.1371/journal. pone.0091864.
35. Moretó, M., and A. Pérez-Bosque. 2009. Dietary plasma proteins, the intestinal immune system, and the barrier functions of the intestinal mucosa. J. Anim. Sci. 87(E. Suppl.)E92-E100. doi:10.2527/ jas.2008-1381.
36. Mulder, I. E., B. Schmidt, M. Lewis, M. Delday, C. R. Stokes, M. Bailey, R. I. Aminov, B. P. Gill, J. R. Pluske, C. D. Mayer, C. Musk, and D. Kelly. 2011. Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity. PLoS ONE 6:e28279. doi:10.1371/journal.pone.0028279.
37. Myer, P. R., T. P. L. Smith, J. E. Wells, L. A. Kuehn, and H. C. Freetly. 2015. Rumen microbiome from steers differing in feed efficiency. PLoS ONE 10:e0129174. doi:10.1371/journal.pone.0129174.
38. Patel, V., A. K. Patel, N. R. Parmar, A. B. Patel, B. Reddy, and C. G. Joshi. 2014. Characterization of the rumen microbiome of Indian Kankrej cattle (Bos indicus) adapted to different forage diet. Appl. Microbiol. Biotechnol. 98:9749-9761. doi:10.1007/ s00253-014-6153-1.
39. Price, M. N., P. S. Dehal, and A. P. Arkin. 2010. FastTree 2-Approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi:10.1371/journal.pone.0009490.
40. Reti, K. L., M. C. Thomas, L. J. Yanke, L. B. Selinger, and G. D. Inglis. 2013. Effect of antimicrobial growth promoter administration on the intestinal microbiota of beef cattle. Gut Pathog. 5:8. doi:10.1186/1757-4749-5-8.
41. Rettedal, E., S. Vilain, S. Lindblom, K. Lehnert, C. Scofield, S. George, S. Clay, R. S. Kaushik, A. J. Rosa, D. Francis, and V. S. Brözel. 2009. Alteration of the ileal microbiota of weanling piglets by the growth-promoting antibiotic chlortetracycline. Appl. Environ. Microbiol. 75:5489-5495. doi:10.1128/AEM.02220-08.
42. Saatchi, M., J. E. Beever, J. E. Decker, D. B. Faulkner, H. C. Freetly, S. L. Hansen, H. Yampara-Iquise, K. A. Johnson, S. D. Kachman, M. S. Kerley, J. Kim, D. D. Loy, E. Marques, H. L. Neibergs, E. J. Pollak, R. D. Schnabel, C. M. Seabury, D. W. Shike, W. M. Snelling, M. L. Spangler, R. L. Weaber, D. J. Garrick, and J. F. Taylor. 2014. QTLs associated with dry matter intake, metabolic mid-test weight, growth and feed efficiency have little overlap across 4 beef cattle studies. BMC Genomics 15:1004. doi:10.1186/1471-2164-15-1004.
43. Shanks, O. C., C. A. Kelty, S. Archibeque, M. Jenkins, R. J. Newton, S. L. McLellan, S. M. Huse, and M. L. Sogin. 2011. Community structures of fecal bacteria in cattle from different animal feeding operations. Appl. Environ. Microbiol. 77:2992-3001. doi:10.1128/AEM.02988-10.
44. Sherman, E. L., J. D. Nkrumah, and S. S. Moore. 2010. Whole genome single nucleotide polymorphism associations with feed intake and feed efficiency in beef cattle. J. Anim. Sci. 88:16-22. doi:10.2527/jas.2008-1759.
45. Stanley, D., S. E. Denman, R. J. Hughes, M. S. Geier, T. M. Crowley, H. Chen, V. R. Haring, and R. J. Moore. 2012. Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl. Microbiol. Biotechnol. 96:1361-1369. doi:10.1007/s00253-011-3847-5.
46. Weese, J. S., T. Shury, and M. D. Jelinski. 2014. The fecal microbiota of semi-free-ranging wood bison (Bison bison athabascae). BMC Vet. Res. 10:120. doi:10.1186/1746-6148-10-120.
47. Weimer, P. J. 2015. Redundancy, resilience, and host specificity of the ruminal microbiota: Implications for engineering improved ruminal fermentations. Front. Microbiol. 6:296. doi:10.3389/ fmicb.2015.00296.
48. Weimer, P. J., D. M. Stevenson, H. C. Mantovani, and S. L. C. Man. 2010. Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. J. Dairy Sci. 93:5902-5912. doi:10.3168/jds.2010-3500.
49. Wirsenius, S., C. Azar, and G. Berndes. 2010. How much land is needed for global food production under scenarios of dietary changes and livestock productivity increases in 2030? Agric. Syst. 103:621-638. doi:10.1016/j.agsy.2010.07.005.
50. Yu, Z., and M. Morrison. 2004. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36:808-813.