Rumen bacterial, archaeal, and fungal diversity of dairy cows in response to ingestion of lauric or myristic acid

Journal of Animal Science

Volumn 90, Issue 12, 2012, Pages 4449-4457

  Hristov, A N ^a   Callaway, T R ^b   Lee, C ^c   Dowd, S E ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b ARS USDA College Station   (France)

^c MR DNA (Molecular Research LP)   (France)

Author keywords

Dairy cow; Microbial ecology; Ruminal protozoa

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS); BACTEROIDES; BOS; BUTYRIVIBRIO; CLOSTRIDIUM; LACTOBACILLUS; METHANOBREVIBACTER; METHANOSPHAERA; OLSENELLA; PREVOTELLA; PROTOZOA; RUMINOCOCCUS;

EID: 84882620172     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2011-4624     Document Type: Article

References (66)

1. Bailey, M. T., S. E. Dowd, J. D. Galley, A. R. Hufnagle, R. G. Allen, and M. Lyte. 2011. Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immu-nomodulation. Brain Behav. Immun. 25:397-407.
2. Bailey, M. T., S. E. Dowd, N. M. A. Parry, J. D. Galley, D. B. Schauer, and M. Lyte. 2010. Stressor exposure disrupts commensal microbi-al populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect. Immun. 78:1509-1519.
3. Bird, S. H., and R. A. Leng. 1978. The effects of defaunation of the rumen on the growth of cattle on low protein high energy diets. Br. J. Nutr. 40:163-167.
4. Boadi, D., C. Benchaar, J. Chiquette, and D. Massé. 2004. Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review. Can. J. Anim. Sci. 84:319-335.
5. Bryant, M. P., and L. A. Burkey. 1952. Numbers and some predominant groups of bacteria in the rumen of cows fed different rations. J. Dairy Sci. 36:218-224.
6. Callaway, T. R., S. E. Dowd, T. S. Edrington, R. C. Anderson, N. Krueger, N. Bauer, P. J. Kononoff, and D. J. Nisbet. 2010. Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). J. Anim. Sci. 88:3977-3983.
7. Capone, K. A., S. E. Dowd, G. N. Stamatas, and J. Nikolovski. 2011. Diversity of the human skin microbiome early in life. J. Invest. Dermatol. 131:2026-2032.
8. Carroll, E. J., and R. E. Hungate. 1955. Formate dissimilation and methane production in bovine rumen contents. Arch. Biochem. Bio-phys. 56:525-533.
9. Chen, M., and M. J. Wolin. 1977. Infl uence of CH4 production by Meth-anobacterium ruminantium on the fermentation of glucose and lactate by Selenomonas ruminanatium. Appl. Environ. Microbiol. 34:756-759.
10. Chiquette, J., G. Talbot, F. Markwell, N. Nili, and R. J. Forster. 2007. Repeated ruminal dosing of Ruminococcus fl avefaciens NJ along with a probiotic mixture in forage or concentrate-fed dairy cows: Effect on ruminal fermentation, cellulolytic populations and in sacco digestibility. Can. J. Anim. Sci. 87:237-249.
11. Coleman, G. S. 1975. The inter-relationships between rumen ciliate protozoa and bacteria. Pages 149-164 in Digestion and Metabolism in the Ruminant. I. W. McDonald and A. C. Warner, ed. Univ. of New England Publ. Unit, Armidale, Australia.
12. Coleman, G. S. 1986. The distribution of carboxymethylcellulase be-tween fractions taken from the rumen of sheep containing no protozoa or one of fi ve different protozoal populations. J. Agric. Sci. 106:121-127.
13. Dahllof, I. 2002. Molecular community analysis of microbial diversity. Curr. Opin. Biotechnol. 13:213-217.
14. Dehority, B. A. 1993. Laboratory Manual for Classifi cation and Morphology of Rumen Ciliate Protozoa. CRC Press, Boca Raton, FL.
15. Dowd, S. E., T. R. Callaway, Y. Sun, T. McKeehan, R. G. Hagevoort, and T. S. Edrington. 2008a. Evaluation of the bacterial diversity in the feces of cattle using bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8:125-132.
16. Dowd, S. E., Y. Sun, P. R. Secor, D. D. Rhoads, B. M. Wolcott, G. A. James, and R. D. Wolcott. 2008b. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol. 8:43-58.
17. Drasar, B. S., and P. A. Barrow. 1985. Intestinal microbiology. Pages 19-40 in Intestinal Microbiology, Aspects of Microbiology. B. S. Drasar and P. A. Barrow, ed. Am. Soc. Microbiol. Press, Washington, DC.
18. Faciola, A. P., G. A. Broderick, A. N. Hristov, and M. I. Leão. 2005. Effect of feeding different levels of lauric acid on ruminal protozoa, and milk production in dairy cows. J. Dairy Sci. 88(Suppl. 1):178.
19. Faciola, A. P., G. A. Broderick, A. N. Hristov, and J. A. Pires. 2008. Effect of four levels of lauric acid on ruminal protozoa, milk production and composition in dairy cows. J. Dairy Sci. 91(Suppl. 1):76. (Abstr.)
20. Fernando, S. C., H. T. Purvis, F. Z. Najar, L. O. Sukharnikov, C. R. Kre-hbiel, T. G. Nagaraja, B. A. Roe, and U. DeSilva. 2010. Rumen microbial population dynamics during adaptation to a high-grain diet. Appl. Environ. Microbiol. 76:7482-7490.
21. Finlay, B. J., G. Esteban, K. J. Clarke, A. G. Williams, T. M. Embley and R. R. Hirt. 1994. Some rumen ciliates have endosymbiotic metha-nogens. FEMS Microbiol Lett. 117:157-162.
22. Gontcharova, V. Y., R. D. Wolcott, E. B. Hollister, T. J. Gentry, S. E. Dowd. 2010. Black box chimera check (b2c2): A windows-based software for batch depletion of chimeras from bacterial 16s rRNA gene datasets. Open Microbiol. J. 4:47-52.
23. Handl, S., S. E. Dowd, J. F. Garcia-Mazcorro, J. M. Steiner, and J. S. Suchodolski. 2011. Massive parallel 16s rRNA gene pyrosequenc-ing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol. 76:301-310.
24. Helaszek, C. T., and B. A. White. 1991. Cellobiose uptake and metabolism by Ruminococcus fl avefaciens. Appl. Environ. Microbiol. 57:64-68.
25. Henderson, C. 1973. The effects of fatty acids on pure cultures of rumen bacteria. J Agric. Sci. 81:107-112.
26. Hristov, A. N., M. Ivan, and T. A. McAllister. 2004. In vitro effects of individual fatty acids on protozoal numbers and on fermentation products in ruminal fl uid from cattle fed a high concentrate, barley-based diet. J. Anim. Sci. 82:2693-2704.
27. Hristov, A. N., M. Ivan, L. M. Rode, and T. A. McAllister. 2001. Fermentation characteristics and ruminal ciliate protozoal populations in cattle fed medium- or high-concentrate barley-based diets. J. Anim. Sci. 79:515-524.
28. Hristov, A. N., and J.-P. Jouany. 2005. Factors affecting the effi ciency of nitrogen utilization in the rumen. Pages 117-166 in Nitrogen and Phosphorus Nutrition of Cattle: Reducing the Environmental Impact of Cattle Operations. E. Pfeffer and A. N. Hristov, ed. CAB Int., Wallingford, UK
29. Hristov, A. N., C. Lee, T. Cassidy, M. Long, K. Heyler, B. Corl, and R. Forster. 2011. Effects of lauric and myristic acids on ruminal fermentation, production, and milk fatty acid composition in lactating dairy cows. J. Dairy Sci. 94:382-395.
30. Hristov, A. N., M. Vander Pol, M. Agle, S. Zaman, C. Schneider, P. Nde-gwa, V. K. Vaddella, K. Johnson, K. J. Shingfield, and S. K. R. Karnati. 2009. Effect of lauric acid and coconut oil on ruminal fermentation, digestion, ammonia losses from manure, and milk fatty acid composition in lactating cows. J. Dairy Sci. 92:5561-5582.
31. Hungate, R. E. 1950. The anaerobic mesophilic cellulolytic bacteria. Bacterial Rev. 14:1-49.
32. Iannotti, E. L., D. Kafkewitz, M. J. Wolin, and M. P. Bryant. 1973. Glucose fermentation products of Ruminococcus albus grown in continuous culture with Vibrio succinogenes: Changes caused by interspecies transfer of H2. J. Bacteriol. 114:1231-1240.
33. Imai, S., and K. Ogimoto. 1978. Scanning electron and fl uorescent microscopic studies on the attachment of spherical bacteria to ciliate protozoa in the ovine rumen. Jpn. J. Vet. Sci. 40:9-19.
34. Irbis, C., and K. Ushida. 2004. Detection of methanogens and proteo-bacteria from a single cell of rumen ciliate protozoa. J. Gen. Appl. Microbiol. 50:203-212.
35. Ishak, H. D., R. Plowes, R. Sen, K. Kellner, E. Meyer, D. A. Estrada, S. E. Dowd, and U. G. Mueller. 2011. Bacterial diversity in Solenop-sis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 pyrosequencing. Microbiol. Ecol. 61:821-831.
36. Joblin, K. N. 1990. Bacterial and protozoal interactions with ruminal fungi. Pages 311-324 in Microbial and plant opportunities to improve lignocellulose utilisation by ruminants. D. E. Akin, L. G. Ljungdahl, J. R. Wilson, and P. J. Harris, eds. Elsevier, New York
37. Jouany, J. P., D. I. Demeyer, and J. Grain. 1988. Effect of defaunating the rumen. Anim. Feed Sci. Technol. 21:229-265.
38. Jouany, J. P., F. Mathieu, J. Senaud, J. Bohatier, G. Bertin, and M. Mer-cier. 1999. Infl uence of protozoa and fungal additives on ruminal pH and redox potential. S. Afr. J. Anim. Sci. 29:64-66.
39. Kurihara, Y., T. Takechi, and F. Shibata. 1978. Relationship between bacteria and ciliate protozoa in the rumen of sheep fed on a purifi ed diet. J. Agric. Sci. 90:373-381.
40. Lee, M. J., P. J. Schreurs, A. C. Messer, and S. H. Zinder. 1987. Association of methanogenic bacteria with fl agellated protozoa from a termite hindgut. Curr. Microbiol. 15:337-341.
41. Lou, J., K. A. Dawson, and H. J. Strobel. 1997. Glycogen formation by ruminal bacterium Prevotella ruminicola. Appl. Environ. Micro-biol. 63:1483-1488.
42. Lyte, M. 2010. The microbial organ in the gut as a driver of homeostasis and disease. Med. Hypotheses 74: 634-638.
43. McAllister, T. A., and C. J. Newbold. 2008. Redirecting rumen fermentation to reduce methanogenesis. Aust. J. Exp. Agric. 48:7-13.
44. Morgavi, D. P., J. P. Jouany, and C. Martin. 2008. Changes in methane emission and rumen fermentation parameters induced by refauna-tion in sheep. Aust. J. Exp. Agric. 48:69-72.
45. Mosoni, P., C. Martin, E. Forano, and D. P. Morgavi. 2011. 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. 89:783-791.
46. Nocker, A., M. Burr, and A. K. Camper. 2007. Genotypic microbial community profi ling: A critical technical review. Microbiol. Ecol. 54:276-289.
47. Odongo, N. E., M. M. Or-Rashid, E. Kebreab, J. France, and B. W. Mc-Bride. 2007. Effect of supplementing myristic acid in dairy cow rations on ruminal methanogenesis and fatty acid profi le in milk. J. Dairy Sci. 90:1851-1858.
48. Ohene-Adjei, S., R. M. Teather, M. Ivan, and R. J. Forster. 2007. Post-inoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Appl. Environ. Micro-biol. 73:4609-4618.
49. Orpin, C. G. 1977. Studies on the defaunation of the ovine rumen using dioctyl sodium sulphosuccinate. J. Appl. Bacteriol. 43:309-318.
50. Pitta, D. W., E. Pinchak, S. E. Dowd, J. Osterstock, V. Gontcharova, E. Ruminal microbial profi le of cows fed fatty acids
51. Youn, K. Dorton, I. Yoon, B. R. Min, J. D. Fulford, T. A. Wicker-sham, and D. P. Malinowski. 2010. Rumen bacterial diversity dynamics associated with changing from bermudagrass hay to grazed winter wheat diets. Microbiol. Ecol. 59:511-522.
52. Roesch, L. F., R. R. Fulthorpe, A. Riva, G. Casella, A. K. M. Hadwin, A. D. Kent, S. H. Daroub, F. A. O. Camargo, W. G. Farmerie, and E. W. Triplett. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1:283-290.
53. Romulo, B., S. H. Bird, and R. A. Leng. 1986. The effects of defauna-tion on digestibility and rumen fungi counts in sheep fed high fi bre diets. Proc. Aust. Soc. Anim. Prod. 16:327-330.
54. Romulo, B., S. H. Bird, and R. A. Leng. 1989. Combined effects of defaunation and protein supplementation on intake, digestibility, N retention and fungi counts in sheep fed straw based diet. Pages 285-288 in The Roles of Protozoa and Fungi in Ruminant Digestion. J. V. Nolan, R. A. Leng, and D. I. Demeyer, ed. Penambul Books, Armidale, Australia.
55. Russell, J. B. 1983. Fermentation of Peptides by Bacteroides ruminicola B14. Appl. Environ. Microbiol. 45:1566-1574.
56. Russell, J. B. 2002. Rumen Microbiology and Its Role in Ruminant Nutrition. J. B. Russell Publ., Ithaca, N Y.
57. Shoemaker, N. B., K. L. Anderson, S. L. Smithson, G. R. Wang, and A. A. Salyers. 1991. Conjugal transfer of a shuttle vector from the human colonic anaerobe Bacteroides uniformis to the ruminal anaerobe Prevotella (Bacteroides) ruminicola B14. Appl. Environ. Microbiol. 57:2114-2120.
58. Smith, D. M., D. E. Snow, E. Rees, A. M. Zischkau, J. D. Hanson, R. D. Wolcott, Y. Sun, J. White, S. Kumar, and S. E. Dowd. 2010. Evaluation of the bacterial diversity of pressure ulcers using bTEFAP pyrosequencing. BMC Med. Genomics 3:41. doi:10.1186/1755-8794-3-41.
59. Stumm, C. K., H. J. Gijzen, and G. D. Vogels. 1982. Association of meth-anogenic bacteria with ovine rumen ciliates. Br. J. Nutr. 47:95-99.
60. Tokura, M., I. Chagan, K. Ushida, and Y. Kojima. 1999. Phylogenetic study of methanogens associated with rumen ciliates. Curr. Micro-biol. 39:123-128.
61. Vogels, G. D., W. F. Hoppe, and C. K. Stumm. 1980. Association of methanogenic bacteria with rumen ciliates. Appl. Environ. Micro-biol. 40:608-612.
62. Wallace, R. J., N. McKain, N. R. McEwan, A. E. Miyagaw, L. C. Chaud-hary, T. P. King, N. D. Walker, J. H. Apajalahti, and C. J. Newbold. 2003. Eubacterium pyruvativorans sp. nov., a novel non-saccharo-lytic anaerobe from the rumen that ferments pyruvate and amino acids, forms caproate and utilizes acetate and propionate. Int. J. Syst. Evol. Microbiol. 53:965-970.
63. Williams, A. G., and G. S. Coleman. 1988. Rumen ciliate protozoa. Pages 77-128 in The Rumen Microbial Ecosystem. P. N. Hobson, ed. Elsevier, Amsterdam, the Netherlands.
64. Williams, A. G., and C. G. Harfoot. 1976. Factors affecting the uptake and metabolism of soluble carbohydrates by the rumen ciliate Dasytricha ruminantium isolated from ovine rumen contents by fi ltration. J. Gen. Microbiol. 96:125-136.
65. Williams, W. L., L. O. Tedeschi, P. J. Kononoff, T. R. Callaway, S. E. Dowd, K. Karges, and M. L. Gibson. 2010. Evaluation of in vitro gas production and rumen bacterial populations fermenting corn milling (co)products. J. Dairy Sci. 93:4735-4743.
66. Yabuuchi, Y., M. Tani, Y. Matsushita, H. Otsuka, and Y. Kobayashi. 2007. Effects of lauric acid on physical, chemical and microbial characteristics in the rumen of steers on a high grain diet. Anim. Sci. J. 78:387-394.