Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-30T18:54:50.948Z Has data issue: false hasContentIssue false

A rapid shift to high-grain diet results in dynamic changes in rumen epimural microbiome in sheep

Published online by Cambridge University Press:  18 December 2018

H. Seddik
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
L. Xu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
Y. Wang
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
S. Y. Mao*
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, Jiangsu Province, China
*
Get access

Abstract

The rapid shift to high-grain (HG) diets in ruminants can affect the function of the rumen epithelium, but the dynamic changes in the composition of the epithelium-associated (epimural) bacterial community in sheep still needs further investigation. Twenty male lambs were randomly allocated to four groups (n = 5). Animals of the first group received hay diet and represented a control group (CON). Simultaneously, animals in the other three groups (HG groups) were rapidly shifted to an HG diet (60% concentrate)which continued for 7 (HG7), 14 (HG14) and 28 (HG28) days, correspondingly. Results showed that ruminal pH dramatically decreased due to the rapid shift to the HG diet (P <0.001), while, the concentrations of butyrate (P <0.001), lactate (P = 0.001), valerate (P = 0.008) and total volatile fatty acids (P = 0.001) increased. Diversity estimators showed a dramatic decrease after the shift without recovering as the HG feeding continued. The principal coordinates analysis showed that CON group clustered separately from all HG groups with the presence of significant difference only between HG7 and HG28 (P = 0.034). The non-parametric multivariate analysis (npmv R-package) deduced that the primary significant differences in phyla and phylogenetic investigation of communities by reconstruction of unobserved states (PICRUSt)-predicted Kyoto Encyclopedia of Genes and Genomes (KEGGs) was attributed mainly to the diet composition (P <0.001, P = 0.001) compared to its application period (P = 0.140, 0.545) which showed a significant effect only on the genus (P = 0.001) and the operational taxonomic units (OTUs) level (P = 0.011). The Kruskal–Wallis test deduced that six phyla showed a significant effect due to the shift in diet composition. At the genus level, HG feeding altered the abundance of 12 taxa, four of which showed a significant variation due to the duration of the HG diet application. Similarly, we found that 21 OTUs showed significant variations due to the duration of the HG diet application. Furthermore, the genes abundance predicted by PICRUSt revealed that the HG feeding significantly affected seven metabolic pathways identified in the KEGG. Particularly, the abundance of gene families associated with carbohydrates metabolism were significantly higher in HG feeding groups (P = 0.027). Collectively, these results revealed that the rapid transition to an HG diet causes dramatic alterations in ruminal fermentation and the composition and function of ruminal epithelium-associated microbiome in sheep, while, the duration of the HG diet application causes drastic alterations to the abundance of some species.

Type
Research Article
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Burchett, WW, Ellis, AR, Harrar, S and Bathke, A 2017. Nonparametric inference for multivariate data: the R package npmv. Journal of Statistical Software 76, 118.Google Scholar
Cheng, KJ and Costerton, JW 1980. Adherent rumen bacteria – their role in the digestion of plant material, urea and epithelial cells. In Digestive physiology and metabolism in ruminants: proceedings of the 5th international symposium on ruminant physiology, held at Clermont-Ferrand, on 3rd–7th September, 1979 (eds. Y Ruckebusch and P Thivend), pp. 227250. Springer, Netherlands, Dordrecht, Netherlands.Google Scholar
Gao, X and Oba, M 2014. Relationship of severity of subacute ruminal acidosis to rumen fermentation, chewing activities, sorting behavior, and milk production in lactating dairy cows fed a high-grain diet. Journal of Dairy Science 97, 30063016.Google Scholar
Górka, P, Schurmann, B, Walpole, M, Błońska, A, Li, S, Plaizier, J, Kowalski, Z and Penner, G 2017. Effect of increasing the proportion of dietary concentrate on gastrointestinal tract measurements and brush border enzyme activity in Holstein steers. Journal of Dairy Science 100, 45394551.Google Scholar
Indikova, I, Humphrey, TJ and Hilbert, F 2015. Survival with a helping hand: campylobacter and microbiota. Frontiers in Microbiology 6, 1266.Google Scholar
Jiao, J, Huang, J, Zhou, C and Tan, Z 2015. Taxonomic identification of ruminal epithelial bacterial diversity during rumen development in goats. Applied and Environmental Microbiology 81, 35023509.Google Scholar
Jin, D, Zhao, S, Zheng, N, Bu, D, Beckers, Y, Denman, SE, McSweeney, CS and Wang, J 2017. Differences in ureolytic bacterial composition between the rumen digesta and rumen wall based on ureC gene classification. Frontiers in Microbiology 8, 385.Google Scholar
Kellermayer, R, Dowd, SE, Harris, RA, Balasa, A, Schaible, TD, Wolcott, RD, Tatevian, N, Szigeti, R, Li, Z, Versalovic, J and Smith, CW 2011. Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice. The FASEB Journal 25, 14491460.Google Scholar
Kelly, WJ, Cookson, AL, Altermann, E, Lambie, SC, Perry, R, Teh, KH, Otter, DE, Shapiro, N, Woyke, T and Leahy, SC 2016. Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract. Scientific Reports 6, 30768.Google Scholar
Kleen, JL, Hooijer, GA, Rehage, J and Noordhuizen, JPTM 2003. Subacute ruminal acidosis (SARA): a review. Journal of Veterinary Medicine Series A 50, 406414.Google Scholar
Klindworth, A, Pruesse, E, Schweer, T, Peplies, J, Quast, C, Horn, M and Glöckner, FO 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research 41, e1e1.Google Scholar
Laanbroek, HJ, Abee, T and Voogd, IL 1982. Alcohol conversion by Desulfobulbus propionicus Lindhorst in the presence and absence of sulfate and hydrogen. Archives of Microbiology 133, 178184.Google Scholar
Lamendella, R, Santo Domingo, JW, Ghosh, S, Martinson, J and Oerther, DB 2011. Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiology 11, 103.Google Scholar
Lima, FS, Oikonomou, G, Lima, SF, Bicalho, MLS, Ganda, EK, de Oliveira Filho, JC, Lorenzo, G, Trojacanec, P and Bicalho, RC 2015. Prepartum and postpartum rumen fluid microbiomes: characterization and correlation with production traits in dairy cows. Applied and Environmental Microbiology 81, 13271337.Google Scholar
Lin, M, Guo, W, Meng, Q, Stevenson, DM, Weimer, PJ and Schaefer, DM 2013. Changes in rumen bacterial community composition in steers in response to dietary nitrate. Applied Microbiology and Biotechnology 97, 87198727.Google Scholar
Liu, JH, Xu, TT, Liu, YJ, Zhu, WY and Mao, SY 2013. A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 305, R232R241.Google Scholar
Mann, E, Wetzels, SU, Wagner, M, Zebeli, Q and Schmitz-Esser, S 2018. Metatranscriptome sequencing reveals insights into the gene expression and functional potential of rumen wall bacteria. Frontiers in Microbiology 9, 43.Google Scholar
Mao, S, Zhang, M, Liu, J and Zhu, W 2015. Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Scientific Reports 5, 16116.Google Scholar
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, 1219.Google Scholar
McCowan, R, Cheng, K, Bailey, C and Costerton, J 1978. Adhesion of bacteria to epithelial cell surfaces within the reticulo-rumen of cattle. Applied and Environmental Microbiology 35, 149155.Google Scholar
Mertens, D 1997. Creating a system for meeting the fiber requirements of dairy cows. Journal of Dairy Science 80, 14631481.Google Scholar
Morotomi, M, Nagai, F and Watanabe, Y 2012. Description of Christensenella minuta gen. nov., sp. nov., isolated from human faeces, which forms a distinct branch in the order Clostridiales, and proposal of Christensenellaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology 62, 144149.Google Scholar
Ni, YH, Chua, HH and Chou, HCC 2015. 166 Dysbiosis of syntrophococcus and Bifidobacterium in infancy is the signature of allergic diseases development. Gastroenterology 148, S-44S-44.Google Scholar
Petri, R, Schwaiger, T, Penner, G, Beauchemin, K, Forster, R, McKinnon, J and McAllister, T 2013. Changes in the rumen epimural bacterial diversity of beef cattle as affected by diet and induced ruminal acidosis. Applied and Environmental Microbiology 79, 37443755.Google Scholar
Plaizier, J, Krause, D, Gozho, G and McBride, B 2008. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. The Veterinary Journal 176, 2131.Google Scholar
Plaizier, JC, Li, S, Tun, HM and Khafipour, E 2017. Nutritional models of experimentally-induced subacute ruminal acidosis (SARA) differ in their impact on rumen and hindgut bacterial communities in dairy cows. Frontiers in Microbiology 7, 2128.Google Scholar
Pourazad, P, Khiaosa-Ard, R, Qumar, M, Wetzels, S, Klevenhusen, F, Metzler-Zebeli, B and Zebeli, Q 2016. Transient feeding of a concentrate-rich diet increases the severity of subacute ruminal acidosis in dairy cattle. Journal of Animal Science 94, 726738.Google Scholar
Russell, J, Garner, M and Flint, J 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. Systematic and Applied Microbiology 25, 498506.Google Scholar
Stewart, D 1977. Biochemical and biological studies on the lipopolysaccharide of Bacteroides nodosus. Research in veterinary science 23, 319325.Google Scholar
Wang, Y, Xu, L, Liu, J, Zhu, W and Mao, S 2017. A high grain diet dynamically shifted the composition of mucosa-associated microbiota and induced mucosal injuries in the colon of sheep. Frontiers in Microbiology 8, 2080.Google Scholar
Wetzels, SU, Mann, E, Metzler-Zebeli, BU, Pourazad, P, Qumar, M, Klevenhusen, F, Pinior, B, Wagner, M, Zebeli, Q and Schmitz-Esser, S 2016. Epimural indicator phylotypes of transiently-induced subacute ruminal acidosis in dairy cattle. Frontiers in Microbiology 7, 274.Google Scholar
Wetzels, SU, Mann, E, Pourazad, P, Qumar, M, Pinior, B, Metzler-Zebeli, BU, Wagner, M, Schmitz-Esser, S and Zebeli, Q 2017. Epimural bacterial community structure in the rumen of Holstein cows with different responses to a long-term subacute ruminal acidosis diet challenge. Journal of Dairy Science 100, 18291844.Google Scholar
Ye, H, Liu, J, Feng, P, Zhu, W and Mao, S 2016. Grain-rich diets altered the colonic fermentation and mucosa-associated bacterial communities and induced mucosal injuries in goats. Scientific Reports 6, 20329.Google Scholar
Ze, X, Duncan, SH, Louis, P and Flint, HJ 2012. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. The ISME Journal 6, 15351543.Google Scholar
Zhang, R, Ye, H, Liu, J and Mao, S 2017. High-grain diets altered rumen fermentation and epithelial bacterial community and resulted in rumen epithelial injuries of goats. Applied Microbiology and Biotechnology 101, 69816992.Google Scholar
Zhao, L, Meng, Q, Ren, L, Liu, W, Zhang, X, Huo, Y and Zhou, Z 2015. Effects of nitrate addition on rumen fermentation, bacterial biodiversity and abundance. Asian-Australasian Journal of Animal Sciences 28, 1433.Google Scholar
Zhao, S, Wang, J and Bu, D 2014. Pyrosequencing-based profiling of bacterial 16 S rRNA genes identifies the unique Proteobacteria attached to the rumen epithelium of bovines. Journal of Dairy Science 97, 869870.Google Scholar
Supplementary material: File

Seddik et al. supplementary material

Seddik et al. supplementary material 1

Download Seddik et al. supplementary material(File)
File 273.6 KB