Feeding a high concentration diet induces unhealthy alterations in the composition and metabolism of ruminal microbiota and host response in a goat model

Frontiers in Microbiology

Volumn 8, Issue FEB, 2017, Pages

  Hua, Canfeng ^a   Tian, Jing ^a   Tian, Ping ^a   Cong, Rihua ^b   Luo, Yanwen ^a   Geng, Yali ^a   Tao, Shiyu ^a   Ni, Yingdong ^a   Zhao, Ruqian ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

Bacteria; Gene expression regulation; Goat; Metabolism; Rumen

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CASPASE 3; CASPASE 8; CATALASE; COMPLEMENTARY DNA; DNA 16S; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUCOCORTICOID; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 8; LACTIC ACID; PHOSPHORUS; PROTEIN BAX; RNA 16S; SODIUM PROTON EXCHANGE PROTEIN 2; SODIUM PROTON EXCHANGE PROTEIN 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL GENE; CELL PH; CONTROLLED STUDY; DIET SUPPLEMENTATION; DNA EXTRACTION; DYSBIOSIS; FATTY ACID TRANSPORT; FERMENTATION; GENE EXPRESSION; GOAT; IMMUNE RESPONSE; MASS FRAGMENTOGRAPHY; MICROBIAL DIVERSITY; MICROBIAL METABOLISM; MICROBIOME; NONHUMAN; POPULATION ABUNDANCE; PYROSEQUENCING; REAL TIME POLYMERASE CHAIN REACTION; RUMEN FLUID; RUMEN MICROORGANISM; SPECIES COMPOSITION;

EID: 85014572391     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00138     Document Type: Article

References (67)

1. Ametaj, B., Koenig, K., Dunn, S., Yang, W., Zebeli, Q., and Beauchemin, K. (2009). Backgrounding and finishing diets are associated with inflammatory responses in feedlot steers. J. Anim. Sci. 87, 1314-1320. doi: 10.2527/jas.2008-1196.
2. Ariko, T., Kass, M., Henno, M., Fievez, V., Kärt, O., Kaart, T., et al. (2015). The effect of replacing barley with glycerol in the diet of dairy cows on rumen parameters and milk fatty acid profile. Anim. Feed Sci. Technol. 209, 69-78. doi: 10.1016/j.anifeedsci.2015.08.004.
3. Asanuma, N., Iwamoto, M., Kawato, M., and Hino, T. (2002). Numbers of nitrate-reducing bacteria in the rumen as estimated by competitive polymerase chain reaction. Anim. Sci. J. 73, 199-205. doi: 10.1046/j.1344-3941.2002.00028.x.
4. Asanuma, N., Yokoyama, S., and Hino, T. (2015). Effects of nitrate addition to a diet on fermentation and microbial populations in the rumen of goats, with special reference to Selenomonas ruminantium having the ability to reduce nitrate and nitrite. Anim. Sci. J. 86, 378-384. doi: 10.1111/asj.12307.
5. Bal, M. A., Coors, J. G., and Shaver, R. D. (1997). Impact of the maturity of corn for use as silage in the diets of dairy cows on intake, digestion, and milk production. J. Dairy Sci. 80, 2497-2503. doi: 10.3168/jds. S0022-0302(97)76202-7.
6. Berg, J., Brandt, K. K., Al-Soud, W. A., Holm, P. E., Hansen, L. H., Sørensen, S. J., et al. (2012). Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Appl. Environ. Microbiol. 78, 7438-7446. doi: 10.1128/AEM.01071-12.
7. Boerman, J. P., Potts, S. B., VandeHaar, M. J., Allen, M. S., and Lock, A. L. (2015). Milk production responses to a change in dietary starch concentration vary by production level in dairy cattle. J. Dairy Sci. 98, 4698-4706. doi: 10.3168/jds.2014-8999.
8. Bunthof, C. J., Bloemen, K., Breeuwer, P., Rombouts, F. M., and Abee, T. (2001). Flow cytometric assessment of viability of lactic acid bacteria. Appl. Environ. Microbiol. 67, 2326-2335. doi: 10.1128/AEM.67.5.2326-2335.2001.
9. Castillo, C., Benedito, J., Méndez, J., Pereira, V., Lopez-Alonso, M., Miranda, M., et al. (2004). Organic acids as a substitute for monensin in diets for beef cattle. Anim. Feed Sci. Technol. 115, 101-116. doi: 10.1016/j.anifeedsci.2004.02.001.
10. Chatton, E., and Pérard, C. (1913). Schizophytes du caecum du cobaye. I. Oscillospira guilliermondi n.g., n.sp. C. R. Sceances Soc. Biol. 74, 1159-1162.
11. Chesson, A., Provan, G. J., Russell, W. R., Scobbie, L., Richardson, A. J., and Stewart, C. (1999). Hydroxycinnamic acids in the digestive tract of livestock and humans. J. Sci. Food Agric. 79, 373-378. doi: 10.1002/(SICI)1097-0010(19990301)79:3<373::AID-JSFA257>3.0.CO;2-6.
12. Connor, E., Li, R., Baldwin, R., and Li, C. (2010). Gene expression in the digestive tissues of ruminants and their relationships with feeding and digestive processes. Animal 4, 993-1007. doi: 10.1017/S1751731109991285.
13. Counillon, L., and Pouysségur, J. (2000). The expanding family of eucaryotic Na+/H+ exchangers. J. Biol. Chem. 275, 1-4. doi: 10.1074/jbc.275.1.1.
14. Davies, D., Theodorou, M., and Newbold, J. (2007). Biotransformation and fermentation-exploiting the rumen and silo. IGER Innov. 11, 37-41.
15. DeFrain, J. M., Hippen, A. R., Kalscheur, K. F., and Jardon, P. W. (2004). Feeding glycerol to transition dairy cows: effects on blood metabolites and lactation performance. J. Dairy Sci. 87, 4195-4206. doi: 10.3168/jds. S0022-0302(04)73564-X.
16. Evans, J. D., and Martin, S. A. (2000). Effects of thymol on ruminal microorganisms. Curr. Microbiol. 41, 336-340. doi: 10.1007/s002840010145.
17. Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J. P., Druart, C., Bindels, L. B., et al. (2013). Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U.S.A. 110, 9066-9071. doi: 10.1073/pnas.1219451110.
18. Gabel, G., Aschenbach, J. R., and Muller, F. (2002). Transfer of energy substrates across the ruminal epithelium: implications and limitations. Anim. Health Res. Rev. 3, 15-30. doi: 10.1079/AHRR200237.
19. Geissinger, O., Herlemann, D. P., Mörschel, E., Maier, U. G., and Brune, A. (2009). The ultramicrobacterium "Elusimicrobium minutum" gen. nov., sp. nov., the first cultivated representative of the termite group 1 phylum. Appl. Environ. Microbiol. 75, 2831-2840. doi: 10.1128/AEM.02697-08.
20. Groot, J. (1998). Correlation between electrophysiological phenomena and transport of macromolecules in intestinal epithelium. Vet. Q. 20, 45-49. doi: 10.1080/01652176.1998.9694968.
21. Gruys, E., Toussaint, M. J., Niewold, T. A., and Koopmans, S. J. (2005). Acute phase reaction and acute phase proteins. J. Zhejiang Univ. Sci. B 6, 1045-1056. doi: 10.1631/jzus.2005.B1045.
22. Harmsen, H. J., Wildeboer-Veloo, A. C., Grijpstra, J., Knol, J., Degener, J. E., and Welling, G. W. (2000). Development of 16S rRNA-based probes for the Coriobacterium group and the atopobium cluster and their application for enumeration of Coriobacteriaceaein human feces from volunteers of different age groups. Appl. Environ. Microbiol. 66, 4523-4527. doi: 10.1128/AEM.66.10.4523-4527.2000.
23. Hook, S. E., Steele, M. A., Northwood, K. S., Wright, A.-D. G., and McBride, B. W. (2011). Impact of high-concentrate feeding and low ruminal pH on methanogens and protozoa in the rumen of dairy cows. Microb. Ecol. 62, 94-105. doi: 10.1007/s00248-011-9881-0.
24. Hristov, A. N., Callaway, T. R., Lee, C., and Dowd, S. E. (2012). Rumen bacterial, archaeal, and fungal diversity of dairy cows in response to ingestion of lauric or myristic acid. J. Anim. Sci. 90, 4449-4457. doi: 10.2527/jas.2011-4624.
25. Jami, E., Israel, A., Kotser, A., and Mizrahi, I. (2013). Exploring the bovine rumen bacterial community from birth to adulthood. ISME J. 7, 1069-1079. doi: 10.1038/ismej.2013.2.
26. Johnson, K. A., and Johnson, D. E. (1995). Methane emissions from cattle. J. Anim. Sci. 73, 2483-2492. doi: 10.2527/1995.7382483x.
27. Khafipour, E., Li, S., Plaizier, J. C., and Krause, D. O. (2009). Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Appl. Environ. Microbiol. 75, 7115-7124. doi: 10.1128/aem.00739-09.
28. Khampa, S., Wanapat, M., Wachirapakorn, C., Nontaso, N., Wattiaux, M., and Rowlison, P. (2006). Effect of levels of sodium DL-malate supplementation on ruminal fermentation efficiency of concentrates containing high levels of cassava chip in dairy steers. Asian Australas. J. Anim. Sci. 19:368. doi: 10.5713/ajas.2006.368.
29. Kiela, P. R., Hines, E. R., Collins, J. F., and Ghishan, F. K. (2001). Regulation of the rat NHE3 gene promoter by sodium butyrate. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G947-G956.
30. Kirat, D., Masuoka, J., Hayashi, H., Iwano, H., Yokota, H., Taniyama, H., et al. (2006). Monocarboxylate transporter 1 (MCT1) plays a direct role in short-chain fatty acids absorption in caprine rumen. J. Physiol. 576, 635-647. doi: 10.1113/jphysiol.2006.115931.
31. Klevenhusen, F., Hollmann, M., Podstatzky-Lichtenstein, L., Krametter-Frotscher, R., Aschenbach, J. R., and Zebeli, Q. (2013). Feeding barley grain-rich diets altered electrophysiological properties and permeability of the ruminal wall in a goat model. J. Dairy Sci. 96, 2293-2302. doi: 10.3168/jds.2012-6187.
32. Koike, S., Handa, Y., Goto, H., Sakai, K., Miyagawa, E., Matsui, H., et al. (2010). Molecular monitoring and isolation of previously uncultured bacterial strains from the sheep rumen. Appl. Environ. Microbiol. 76, 1887-1894. doi: 10.1128/aem.02606-09.
33. Kristensen, S. (1974). Ruminal bioshynthesis of aromatic amino acids from arylacetic acids, glucose, shikimic acid and phenol. Br. J. Nutr. 31, 357-365. doi: 10.1079/BJN19740044.
34. Li, F., Yang, X. J., Cao, Y. C., Li, S. X., Yao, J. H., Li, Z. J., et al. (2014). Effects of dietary effective fiber to rumen degradable starch ratios on the risk of sub-acute ruminal acidosis and rumen content fatty acids composition in dairy goat. Anim. Feed Sci. Technol. 189, 54-62. doi: 10.1016/j.anifeedsci.2013.12.011.
35. Liu, Q., Wang, C., Yang, W., Dong, Q., Dong, K., Huang, Y., et al. (2009). Effects of malic acid on rumen fermentation, urinary excretion of purine derivatives and feed digestibility in steers. Animal 3, 32-39. doi: 10.1017/S1751731108003364.
36. Lu, Y. C., Yeh, W. C., and Ohashi, P. S. (2008). LPS/TLR4 signal transduction pathway. Cytokine 42, 145-151. doi: 10.1016/j.cyto.2008.01.006.
37. Mackie, R. I., Aminov, R. I., Hu, W., Klieve, A. V., Ouwerkerk, D., Sundset, M. A., et al. (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.
38. Mao, S., Zhang, R., Wang, D., and Zhu, W. (2013). Impact of subacute ruminal acidosis (SARA) adaptation on rumen microbiota in dairy cattle using pyrosequencing. Anaerobe 24, 12-19. doi: 10.1016/j.anaerobe.2013.08.003.
39. Mao, S. Y., Huo, W. J., and Zhu, W. Y. (2016). Microbiome-metabolome analysis reveals unhealthy alterations in the composition and metabolism of ruminal microbiota with increasing dietary grain in a goat model. Environ. Microbiol. 18, 525-541. doi: 10.1111/1462-2920.12724.
40. Martel, C. A., Titgemeyer, E., Mamedova, L., and Bradford, B. (2011). Dietary molasses increases ruminal pH and enhances ruminal biohydrogenation during milk fat depression. J. Dairy Sci. 94, 3995-4004. doi: 10.3168/jds.2011-4178.
41. Michelsen, C. F., Pedas, P., Glaring, M. A., Schjoerring, J. K., and Stougaard, P. (2014). Bacterial diversity in Greenlandic soils as affected by potato cropping and inorganic versus organic fertilization. Polar Biol. 37, 61-71. doi: 10.1007/s00300-013-1410-9.
42. Mikelis, C. M., Simaan, M., Ando, K., Fukuhara, S., Sakurai, A., Amornphimoltham, P., et al. (2015). RhoA and ROCK mediate histamine-induced vascular leakage and anaphylactic shock. Nat. Commun. 6:6725. doi: 10.1038/ncomms7725.
43. Nagaraja, T. G., and Titgemeyer, E. C. (2007). Ruminal acidosis in beef cattle: the current microbiological and nutritional outlook. J. Dairy Sci. 90(Suppl. 1), E17-E38. doi: 10.3168/jds.2006-478.
44. Nagata, S. (1997). Apoptosis by death factor. Cell 88, 355-365. doi: 10.1016/S0092-8674(00)81874-7.
45. Nilsson, S. A. (1963). Clinical, morphological, and experimental studies of laminitis in cattle. Acta Vet. Scand. 4(Suppl. 1):304.
46. Oba, M., Mewis, J., and Zhining, Z. (2015). Effects of ruminal doses of sucrose, lactose, and corn starch on ruminal fermentation and expression of genes in ruminal epithelial cells. J. Dairy Sci. 98, 586-594. doi: 10.3168/jds.2014-8697.
47. Petri, R., Schwaiger, T., Penner, G., Beauchemin, K., Forster, R., McKinnon, J., et al. (2013). Changes in the rumen epimural bacterial diversity of beef cattle as affected by diet and induced ruminal acidosis. Appl. Environ. Microbiol. 79, 3744-3755. doi: 10.1128/AEM.03983-12.
48. Pitta, D. W., Kumar, S., Vecchiarelli, B., Shirley, D. J., Bittinger, K., Baker, L. D., et al. (2014). Temporal dynamics in the ruminal microbiome of dairy cows during the transition period. J. Anim. Sci. 92, 4014-4022. doi: 10.2527/jas.2014-7621.
49. Poulsen, M., Schwab, C., Jensen, B. B., Engberg, R. M., Spang, A., Canibe, N., et al. (2013). Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat. Commun. 4:1428. doi: 10.1038/ncomms2432.
50. Ribeiro, C., Karnati, S., and Eastridge, M. (2005). Biohydrogenation of fatty acids and digestibility of fresh alfalfa or alfalfa hay plus sucrose in continuous culture. J. Dairy Sci. 88, 4007-4017. doi: 10.3168/jds. S0022-0302(05)73087-3.
51. Russell, J. B., O'Connor, J. D., Fox, D. G., Van Soest, P. J., and Sniffen, C. J. (1992). A net carbohydrate and protein system for evaluating cattle diets: I. Ruminal fermentation. J. Anim. Sci. 70, 3551-3561.
52. Saleem, F., Ametaj, B., Bouatra, S., Mandal, R., Zebeli, Q., Dunn, S., et al. (2012). A metabolomics approach to uncover the effects of grain diets on rumen health in dairy cows. J. Dairy Sci. 95, 6606-6623. doi: 10.3168/jds.2012-5403.
53. Seo, J., Park, T., Kwon, I., Piao, M., Lee, C., and Ha, J. K. (2013). Characterization of cellulolytic and xylanolytic enzymes of Bacillus licheniformis JK7 isolated from the rumen of a native Korean goat. Asian Australas. J. Anim. Sci. 26, 50-58. doi: 10.5713/ajas.2012.12506.
54. Slyter, L., Oltjen, R., Kern, D., and Weaver, J. (1968). Microbial species including ureolytic bacteria from the rumen of cattle fed purified diets. J. Nutr. 94, 185-192.
55. Soriano, F. D., Polan, C. E., and Miller, C. N. (2000). Milk production and composition, rumen fermentation parameters, and grazing behavior of dairy cows supplemented with different forms and amounts of corn grain. J. Dairy Sci. 83, 1520-1529. doi: 10.3168/jds. S0022-0302(00)75024-7.
56. Strater, J., Wellisch, I., Riedl, S., Walczak, H., Koretz, K., Tandara, A., et al. (1997). CD95 (APO-1/Fas)-mediated apoptosis in colon epithelial cells: a possible role in ulcerative colitis. Gastroenterology 113, 160-167. doi: 10.1016/S0016-5085(97)70091-X.
57. Sun, X., Wang, Y., Chen, B., and Zhao, X. (2015). Partially replacing cornstarch in a high-concentrate diet with sucrose inhibited the ruminal trans-10 biohydrogenation pathway in vitro by changing populations of specific bacteria. J. Anim. Sci. Biotechnol. 6:57. doi: 10.1186/s40104-015-0051-y.
58. Tao, S., Duanmu, Y., Dong, H., Ni, Y., Chen, J., Shen, X., et al. (2014a). High concentrate diet induced mucosal injuries by enhancing epithelial apoptosis and inflammatory response in the hindgut of goats. PLoS ONE 9:e111596. doi: 10.1371/journal.pone.0111596.
59. Tao, S., Duanmu, Y., Dong, H., Tian, J., Ni, Y., and Zhao, R. (2014b). A high-concentrate diet induced colonic epithelial barrier disruption is associated with the activating of cell apoptosis in lactating goats. BMC Vet. Res. 10:235. doi: 10.1186/s12917-014-0235-2.
60. Taxis, T. M., Wolff, S., Gregg, S. J., Minton, N. O., Zhang, C., Dai, J., et al. (2015). The players may change but the game remains: network analyses of ruminal microbiomes suggest taxonomic differences mask functional similarity. Nucleic Acids Res. 43, 9600-9612. doi: 10.1093/nar/gkv973.
61. Underwood, W. (1992). Rumen lactic acidosis: 1. Epidemiology and pathophysiology. Comp. Contin. Educ. Pract. Vet. 14, 1127-1133.
62. Vallimont, J., Bargo, F., Cassidy, T., Luchini, N., Broderick, G., and Varga, G. (2004). Effects of replacing dietary starch with sucrose on ruminal fermentation and nitrogen metabolism in continuous culture. J. Dairy Sci. 87, 4221-4229. doi: 10.3168/jds. S0022-0302(04)73567-5.
63. Wojdasiewicz, P., Poniatowski, L. A., and Szukiewicz, D. (2014). The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediat. Inflamm. 2014:561459. doi: 10.1155/2014/561459.
64. Yanagita, K., Manome, A., Meng, X.-Y., Hanada, S., Kanagawa, T., Tsuchida, T., et al. (2003). Flow cytometric sorting, phylogenetic analysis and in situ detection of Oscillospira guillermondii, a large, morphologically conspicuous but uncultured ruminal bacterium. Int. J. Syst. Evol. Microbiol. 53, 1609-1614. doi: 10.1099/ijs.0.02541-0.
65. Zebeli, Q., and Metzler-Zebeli, B. U. (2012). Interplay between rumen digestive disorders and diet-induced inflammation in dairy cattle. Res. Vet. Sci. 93, 1099-1108. doi: 10.1016/j.rvsc.2012.02.004.
66. Zhao, L., Meng, Q., Ren, L., Liu, W., Zhang, X., Huo, Y., et al. (2015). Effects of nitrate addition on rumen fermentation, bacterial biodiversity and abundance. Asian Australas. J. Anim. Sci. 28, 1433-1441. doi: 10.5713/ajas.15.0091.
67. Zhou, Z., Yu, Z., and Meng, Q. (2012). Effects of nitrate on methane production, fermentation, and microbial populations in in vitro ruminal cultures. Bioresour. Technol. 103, 173-179. doi: 10.1016/j.biortech.2011.10.013.