Skip to main content
SpringerLink
Log in

High-grain diets altered rumen fermentation and epithelial bacterial community and resulted in rumen epithelial injuries of goats

  • Applied Microbial and Cell Physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

This study evaluated the effects of high-grain diets on the rumen fermentation, epithelial bacterial community, morphology of rumen epithelium, and local inflammation of goats during high-grain feeding. Twelve 8-month-old goats were randomly assigned to two different diets, a hay diet or a high-grain diet (65% grain, HG). At the end of 7 weeks of treatment, samples of rumen content and rumen epithelium were collected. Rumen pH was lower (P < 0.05), but the levels of volatile fatty acids and lipopolysaccharides were higher (P < 0.05) in the HG group than those in the hay group. The principal coordinate analysis indicated that HG diets altered the rumen epithelial bacterial community, with an increase in the proportion of genus Prevotella and a decrease in the relative abundance of the genera Shuttleworthia and Fibrobacteres. PICRUSt analysis suggested that the HG-fed group had a higher (P < 0.05) relative abundance of gene families related to energy metabolism; folding, sorting, and degradation; translation; metabolic diseases; and immune system. Furthermore, HG feeding resulted in the rumen epithelial injury and upregulated (P < 0.05) the gene expressions of IL-1β and IL-6, and the upregulations were closely related to the rumen pH, LPS level, and rumen epithelial bacteria abundance. In conclusion, our results indicated that the alterations in the rumen environment and epithelial bacterial community which were induced by HG feeding may result in the damage and local inflammation in the rumen epithelium, warranting further study of rumen microbial–host interactions in the HG feeding model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Al-Sadi RM, Ma TY (2007) IL-1β causes an increase in intestinal epithelial tight junction permeability. J Immunol 178:4641–4649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bekele AZ, Koike S, Kobayashi Y (2010) Genetic diversity and diet specificity of ruminal Prevotella revealed by 16S rRNA gene-based analysis. FEMS Microbiol Lett 305:49–57

    Article  CAS  PubMed  Google Scholar 

  • Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EA (2010) The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12:1842–1854

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Penner GB, Li M, Oba M, Guan LL (2011) The epithelial tissue associated bacterial diversity changes in the rumen of beef cattle during dietary transition to high grain diets. Appl Environ Microbiol 77:5770–5781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Oba M, Guan LL (2012) Variation of bacterial communities and expression of Toll-like receptor genes in the rumen of steers differing in susceptibility to subacute ruminal acidosis. Vet Microbiol 159:451–459

    Article  CAS  PubMed  Google Scholar 

  • Cheng KJ, Wallace RJ (1979) The mechanism of passage of endogenous urea through the rumen wall and the role of ureolytic epithelial bacteria in the urea flux. Br J Nutr 42:553–557

    Article  CAS  PubMed  Google Scholar 

  • Chinese Science and Technology Committee (1988) Regulations for the Administration of Affairs Concerning Experimental Animals. Beijing, China

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  CAS  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dionissopoulos L, Steele M, AlZahal O, McBride B (2012) Adaptation to high grain diets proceeds through minimal immune system stimulation and differences in extracellular matrix protein expression in a model of subacute ruminal acidosis in nonlactating dairy cows. Am J Anim Vet Sci 7:84–91

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

  • Fernando SC, Purvis HT, Najar FZ, Sukharnikov LO, Krehbiel CR, Nagaraja TG, Roe BA, DeSilva U (2010) Rumen microbial population dynamics during adaptation to a high-grain diet. Appl Environ Microbiol 76:7482-7490

  • Gozho GN, Krause DO, Plaizier JC (2006) Rumen lipopolysaccharide and inflammation during grain adaptation and subacute ruminal acidosis in steers. J Dairy Sci 89:4404–4413

    Article  CAS  PubMed  Google Scholar 

  • Graham C, Simmons NL (2005) Functional organization of the bovine rumen epithelium. Am J Physiol Regul Integr Comp Physiol 288:R173-R181

  • Hook SE, Steele MA, Northwood KS, Dijkstra J, France J, Wright AD, McBride BW (2011) Impact of subacute ruminal acidosis (SARA) adaptation and recovery on the density and diversity of bacteria in the rumen of dairy cows. FEMS Microbiol Ecol 78:275-284

  • Hu ZH, Yu HQ, Zhu RF (2005) Influence of particle size and pH on anaerobic degradation of cellulose by ruminal microbes. Int Biodeter Biodegr 55:233–238

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khafipour E, Krause DO, Plaizier JC (2009a) A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. J Dairy Sci 92:1060–1070

    Article  CAS  PubMed  Google Scholar 

  • Khafipour E, Li S, Plaizier JC, Krause DO (2009b) Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Appl Environ Microbiol 75:7115–7124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleen JL, Hooijer GA, Rehage J, Noordhuizen JP (2003) Subacute ruminal acidosis (SARA): a review. J Vet Med A 50:406-414

  • Konishi H, Fujiya M, Kohgo Y (2015) Host–microbe interactions via membrane transport systems. Environ Microbiol 17:931–937

    Article  PubMed  Google Scholar 

  • Krause KM, Oetzel GR (2006) Understanding and preventing subacute ruminal acidosis in dairy herds: a review. Anim Feed Sci Tech 126:215–236

    Article  CAS  Google Scholar 

  • Kuzinski J, Zitnan R, Albrecht E, Viergutz T, Schweigel-Röntgen M (2012) Modulation of vH+-ATPase is part of the functional adaptation of sheep rumen epithelium to high-energy diet. Am J Physiol Regul Integr Comp Physiol 303:R909–R920

    Article  CAS  PubMed  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotech 31:814–821

    Article  CAS  Google Scholar 

  • Li MJ, Zhou M, Adamowicz E, Basarab JA, Guan LL (2012) Characterization of bovine ruminal epithelial bacterial communities using 16S rRNA sequencing, PCR-DGGE, and qRT-PCR analysis. Vet Microbiol 155:72–80

    Article  CAS  PubMed  Google Scholar 

  • Liu JH, Xu TT, Liu YJ, Zhu WY, Mao SY (2013) A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats. Am J Physiol Regul Integr Comp Physiol 305:R232–R241

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Xu T, Zhu W, Mao S (2014) High-grain feeding alters caecal bacterial microbiota composition and fermentation and results in caecal mucosal injury in goats. Br J Nutr 112:416–427

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maes M, Kubera M, Leunis JC (2008) The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett 29:117–124

    PubMed  Google Scholar 

  • Mani V, Weber TE, Baumgard LH, Gabler NK (2012) Endotoxin, inflammation and intestinal function in livestock. J Anim Sci 90:1452–1465

    Article  CAS  PubMed  Google Scholar 

  • Mao SY, Zhang G, Zhu WY (2008) Effect of disodium fumarate on ruminal metabolism and rumen bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. Anim Feed Sci Tech 140:293-306

  • Metzler-Zebeli BU, Schmitz-Esser S, Klevenhusen F, Podstatzky-Lichtenstein L, Wagner M, Zebeli Q (2013) Grain-rich diets differently alter ruminal and colonic abundance of microbial populations and lipopolysaccharide in goats. Anaerobe 20:65–73

    Article  CAS  PubMed  Google Scholar 

  • Mortensen PB, Clausen MR (1996) Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl 216:132–148

    Article  CAS  PubMed  Google Scholar 

  • O’Grady L, Doherty ML, Mulligan FJ (2008) Subacute ruminal acidosis (SARA) in grazing Irish dairy cows. Vet J 176:44–49

    Article  PubMed  Google Scholar 

  • Penner GB, Aschenbach JR, Gäbel G, Rackwitz R, Oba M (2009) Epithelial capacity for apical uptake of short chain fatty acids is a key determinant for intraruminal pH and the susceptibility to subacute ruminal acidosis in sheep. J Nutr 139:1714–1720

    Article  CAS  PubMed  Google Scholar 

  • Penner GB, Steele MA, Aschenbach JR, McBride BW (2011) Ruminant nutrition symposium: molecular adaptation of ruminal epithelia to highly fermentable diets. J Anim Sci 89:1108-1119

  • Petri RM, Schwaiger T, Penner GB, Beauchemin KA, Forster RJ, McKinnon JJ, McAllister TA (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

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, Coutinho PM, Nelson KE (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microbial Ecol 60:721–729

    Article  Google Scholar 

  • Ransom-Jones E, Jones DL, McCarthy AJ, McDonald JE (2012) The Fibrobacteres: an important phylum of cellulose-degrading bacteria. Microb Ecol 63:267–281

    Article  CAS  PubMed  Google Scholar 

  • Sadet S, Martin C, Meunier B, Morgavi DP (2007) PCR-DGGE analysis reveals a distinct diversity in the bacterial population attached to the rumen epithelium. Animal 1:939-944

  • Sadet-Bourgeteau S, Martin C, Morgavi DP (2010) Bacterial diversity dynamics in rumen epithelium of wethers fed forage and mixed concentrate forage diets. Vet Microbiol 146:98-104

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Z, Seyfert HM, Löhrke B, Schneider F, Zitnan R, Chudy A, Kuhla S, Hammon HM, Blum JW, Martens H, Hagemeister H, Voigt J (2004) An energy-rich diet causes rumen papillae proliferation associated with more IGF type 1 receptors and increased plasma IGF-1 concentrations in young goats. J Nutr 134:11-17

  • Steerl MA, Vandervoort G, AlZahal O, Hook SE, Matthews JC, McBride BW (2011a) Rumen epithelial adaptation to high-grain diets involves the coordinated regulation of genes involved in cholesterol homeostasis. Physiol Genomics 43:308–316

  • Steele MA, Croom J, Kahler M, AlZahal O, Hook SE, Plaizier K, McBride BW (2011b) Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis. Am J Physiol Regul Integr Comp Physiol 300:R1515–R1523

    Article  CAS  PubMed  Google Scholar 

  • Stewart CS, Flint HJ, Bryant MP (1997) The rumen bacteria. In: Hobson PN, Stewart CS (eds) The rumen microbial ecosystem. Springer Netherlands, Dordrecht, pp 10–72

    Chapter  Google Scholar 

  • Suzuki T, Yoshinaga N, Tanabe S (2011) Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 286:31263–31271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima K, Arai S, Ogata K, Nagamine T, Matsui H, Nakamura M, Aminov RI, Benno Y (2000) Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe 6:273–284

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye H, Liu J, Feng P, Zhu W, Mao S (2016) Grain-rich diets altered the colonic fermentation and mucosa-associated bacterial communities and induced mucosal injuries in goats. Sci Rep 6:20329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zebeli Q, Dijkstra J, Tafaj M, Steingass H, Ametaj BN, Drochner W (2008) Modeling the adequacy of dietary fiber in dairy cows based on the responses of ruminal pH and milk fat production to composition of the diet. J Dairy Sci 91:2046-2066

  • Zhou M, Hernandez-Sanabria E, Guan LL (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

Download references

Acknowledgements

SM, JL, and RZ designed the study; RZ and HY conducted the study and collected the data; RZ, HY, and SM analyzed the data; JL helped with the manuscript writing; RZ, HY, and SM wrote the paper; and SM had primary responsibility for the final content. All authors have read and approved the final manuscript.

Author information

Authors and Affiliations

  1. Key Laboratory of Zoonosis of Liaoning Province, College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang, Liaoning Province, 110866, China

    Ruiyang Zhang

  2. Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu Province, 210095, China

    Huimin Ye, Junhua Liu & Shengyong Mao

Authors
  1. Ruiyang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huimin Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junhua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shengyong Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shengyong Mao.

Ethics declarations

Funding

This study was supported by the Natural Science Foundation of China (31372339) and the Natural Science Foundation of Jiangsu Province of China (BK20151431).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The present study was approved by the Animal Care and Use Committee of Nanjing Agricultural University. All experimental procedures and animal protocol conformed to the Regulations for the Administration of Affairs Concerning Experimental Animals (Chinese Science and Technology Committee, 1988).

Electronic supplementary material

ESM 1

(PDF 665 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, R., Ye, H., Liu, J. et al. High-grain diets altered rumen fermentation and epithelial bacterial community and resulted in rumen epithelial injuries of goats. Appl Microbiol Biotechnol 101, 6981–6992 (2017). https://doi.org/10.1007/s00253-017-8427-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8427-x

Keywords

Search

Navigation