Abstract
The cecum plays an important role in the feed fermentation of ruminants. However, information is very limited regarding the cecal microbiota and their methane production. In the present study, the cecal content from twelve local Chinese goats, fed with either a hay diet (0% grain) or a high-grain diet (71.5% grain), were used to investigate the bacterial and archaeal community and their methanogenic potential. Microbial community analysis was determined using high-throughput sequencing of 16S rRNA genes and real-time PCR, and the methanogenesis potential was assessed by in vitro fermentation with ground corn or hay as substrates. Compared with the hay group, the high-grain diet significantly increased the length and weight of the cecum, the proportions of starch and crude protein, the concentrations of volatile fatty acids and ammonia nitrogen, but decreased the pH values (P < 0.05). The high-grain diet significantly increased the abundances of bacteria and archaea (P < 0.05) and altered their community. For the bacterial community, the genera Bifidobacterium, Prevotella, and Treponema were significantly increased in the high-grain group (P < 0.05), while Akkermansia, Oscillospira, and Coprococcus were significantly decreased (P < 0.05). For the archaeal community, Methanosphaera stadtmanae was significantly increased in the high-grain group (P < 0.05), while Methanosphaera sp. ISO3-F5 was significantly decreased (P < 0.05). In the in vitro fermentation with grain as substrate, the cecal microorganisms from the high-grain group produced a significantly higher amount of methane and volatile fatty acids (P < 0.05), and produced significantly lower amount of lactate (P < 0.05). Conclusively, high-grain diet led to more fermentable substrates flowing into the hindgut of goats, resulting in an enhancement of microbial fermentation and methane production in the cecum.
Similar content being viewed by others
References
Ametaj BN, Zebeli Q, Saleem F, Psychogios N, Lewis MJ, Dunn SM, Xia J, Wishart DS (2010) Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows. Metabolomics 6(4):583–594
AOAC (2000) Official methods of analysis of AOAC International, 17th edn. AOAC International, Gaithersburg
Aronesty E (2011) ea-utils: command-line tools for processing biological sequencing data. http://code.google.com/p/ea-utils
Barker SB, Summerson WH (1941) The colorimetric determination of lactic acid in biological material. J Biol Chem 138:535–554
Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumine reads. Appl Environ Microbiol 77:3846–3852
Belzer C, de Vos WM (2012) Microbes inside—from diversity to function: the case of Akkermansia. ISME J 6:1449–1458
Blais Lecours P, Marsolais D, Cormier Y, Berberi M, Haché C, Bourdages R, Duchaine C (2014) Increased prevalence of Methanosphaera stadtmanae in inflammatory bowel diseases. PLoS ONE 9(2):e87734
Brugère JF, Borrel G, Gaci N, Tottey W, O’Toole PW, Malpuech-Brugère C (2014) Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 5(1):5–10
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
de Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K, Whitman WB (eds) (2009) Bergey’s manual of systematic bacteriology. Volume 3: The Firmicutes, 2nd edn. Springer, New York, pp 736–1190
Denman SE, McSweeney CS (2006) Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiol Ecol 58:572–582
Dennis KL, Wang Y, Blatner NR, Wang S, Saadalla A, Trudeau E, Roers A, Weaver CT, Lee JJ, Gilbert JA, Chang EB, Khazaie K (2013) Adenomatous polyps are driven by microbe-instigated focal inflammation and are controlled by IL-10—producing T cells. Cancer Res 73:5905–5913
Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469–1476
Dixon RM, Nolan JV (1982) Studies of the large intestine of sheep. 1. Fermentation and absorption in sections of the large intestine. Br J Nutr 47:289–300
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200
Faichney GJ (1968) Volatile fatty acids in the caecum of the sheep. Aust J Biol Sci 21:177–180
Gray FV (1947) The digestion of cellulose by sheep. The extent of cellulose digestion at successive levels of the alimentary tract. J Exp Bio 24(1–2):15
Gressley TF, Hall MB, Armentano LE (2011) Ruminant nutrition symposium: productivity, digestion, and health responses to hindgut acidosis in ruminants. J Anim Sci 89:1120–1130
Jayaprakash G, Sathiyabarathi M, Robert MA, Tamilmani T (2016) Rumen-protected choline: a significance effect on dairy cattle nutrition. Vet World 9(8):837–841
Jiang Y, Ogunade IM, Arriola KG, Qi M, Vyas D, Staples CR, Adesogan AT (2017) Effects of the dose and viability of saccharomyces cerevisiae. 2. Ruminal fermentation, performance of lactating dairy cows, and correlations between ruminal bacteria abundance and performance measures. J Dairy Sci 100:1–17
Jin W, Meng Z, Wang J, Cheng Y, Zhu W (2017) Effect of nitrooxy compounds with different molecular structures on the rumen methanogenesis, metabolic profile, and methanogenic community. Curr Microbiol 74(8):891–898
Konikoff T, Gophna U (2016) Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol 24(7):523–524
Lang K, Schuldes J, Klingl A, Poehlein A, Daniel R, Brunea A (2015) New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of “Candidatus Methanoplasma termitum”. Appl Environ Microbiol 81(4):1338–1352
Langille MG, 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 Biotechnol 31:814–821
Leiva T, Cooke RF, Brandão AP, Marques RS, Vasconcelos JL (2015) Effects of rumen-protected choline supplementation on metabolic and performance responses of transition dairy cows. J Anim Sci 93(4):1896–1904
Li S, Khafipour E, Krause DO, Kroeker A, Rodriguez-Lecompte JC, Gozho GN, Plaizier JC (2012) Effects of subacute ruminal acidosis challenges on fermentation and endotoxins in the rumen and hindgut of dairy cows. J Dairy Sci 95(1):294–303
Li M, Jin W, Li Y, Zhao L, Cheng Y, Zhu W (2016) Spatial dynamics of the bacterial community structure in the gastrointestinal tract of red kangaroo (Macropus rufus). World J Microbiol Biotechnol 32(6):98
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(3):416–427
Liu J, Pu YY, Xie Q, Wang JK, Liu JX (2015) Pectin induces an in vitro rumen microbial population shift attributed to the pectinolytic treponema group. Curr Microbiol 70(1):67–74. https://doi.org/10.1007/s00284-014-0672-y
Mackie RI, Aminov RI, Hu W, Klieve AV, Ouwerkerk D, Sundset MA, Kamagata Y (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(11):6808–6815
Makkar HPS, Sharma OP, Dawra RK, Negi SS (1982) Simple determination of microbial protein in rumen liquor. J Dairy Sci 65:2170–2173
Mao S, Zhang M, Liu J, Zhu W (2015) Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Sci Rep 5:16116
Mao SY, Huo WJ, Zhu WY (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(2):525–541
Martin C, Philippeau C, Michalet-Doreau B (1999) Effect of wheat and corn variety on fiber digestion in beef steers fed high-grain diets. J Anim Sci 77:2269–2278
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618
Menke KH, Rabb L, Salewski A, Steingass H, Fritz D, Schneider W (1979) The estimation of the digestibility and metabolisable energy content of ruminant feedstuffs from the gas production when they are incubated with rumen liquor in vitro. J Agric Sci 93:217–222
Oren A, Garrity GM (2015) The correct name of the type species of the genus Methanocorpusculum. Request for an opinion. Int J Syst Evol Microbiol 65:2013–2014
Paster BJ, Canale-Parola E (1985) Treponema saccharophilum sp. nov., a large pectinolytic spirochete from the bovine rumen. Appl Environ Microbiol 50:212–219
Patel TR, Jure KG, Jones GA (1981) Catabolism of phloroglucinol by the rumen anaerobe coprococcus. Appl Environ Microbiol 42(6):1010–1017
Plaizier JC, Li S, Tun HM, 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. Front Microbiol 7:2128
Popova M, Morgavi DP, Martin C (2013) Methanogens and methanogenesis in the rumens and ceca of lambs fed two different high-grain-content diets. Appl Environ Microbiol 79(6):1777–1786
Prasad J, Gill H, Smart J, Gopal PK (1998) Selection and characterisation of Lactobacillus and Bifidobacterium strains for use as probiotics. Int Dairy J 8:993–1002
Sakamoto M, Ohkuma M (2012) Reclassification of Xylanibacter oryzae as Prevotella oryzae comb. nov., with an emended description of the genus Prevotella. Int J Syst Evol Microbiol 62:2637–2642
Seedorf H, Kittelmann S, Henderson G, Janssen PH (2014) RIM-DB: a taxonomic framework for community structure analysis of methanogenic archaea from the rumen and other intestinal environments. Peer J 2:e494
Seedorf H, Kittelmann S, Janssen PH (2015) Few highly abundant operational taxonomic units dominate within rumen methanogenic archaeal species in New Zealand sheep and cattle. Appl Environ Microbiol 81(3):986–995
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60
Shah HN, Collins DM (1990) Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in genus Bacteroides. Int J Syst Bacteriol 40(2):205–208
Söllinger A, Schwab C, Weinmaier T, Loy A, Tveit AT, Schleper C, Urich T (2016) Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiv149
Su Y, Bian G, Zhu Z, Smidt H, Zhu W (2014) Early methanogenic colonisation in the faeces of meishan and yorkshire piglets as determined by pyrosequencing analysis. Archaea 2014:547908
Theodorou MK, Williams BA, Dhanoa MS, MacAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anim Feed Sci Technol 48:185–197
Tsai CG, Gates DM, Ingledew WM, Jones GA (1976) Products of anaerobic phloroglucinol degradation by Coprococcus sp. pe15. Can J Microbiol 22(2):159–164
Van de Merwe JP, Stegeman JH (1985) Binding of Coprococcus comes to the fc portion of igg. A possible role in the pathogenesis of Crohn’s disease? Eur J Immunol 15(8):860–863
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fibre, neutral detergent fibre, and non-starch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597
Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974
Whitman WB, Bowen KN, Fonty G (2006) The methanogenic bacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (eds) Prokaryotes, 3rd edn. Springer, New York, pp 165–207
Wolin MJ, Miller TL, Stewart CS (1997) Microbe–microbe interactions. In: Hobson PN, Stewart CS (eds) Rumen microbial ecosystem, 2nd edn. Chapman & Hall, London, pp 467–491
Wright ADG, Dehority BA, Lynn DH (1997) Phylogeny of the rumen ciliates Entodinium, Epidinium and Polyplastron (Litostomatea: Entodiniomorphida) inferred from small subunit ribosomal RNA sequences. J Euk Microbiol 44:61–67
Yanagita K, Manome A, Meng XY, Hanada S, Kanagawa T, Tsuchida T, Mackie RI, Kamagata Y (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(Pt 5):1609–1614
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
Zellner G, Stackebrandt E, Messner P, Tindall BJ, Conway de Macario E, Kneifel H, Sleytr UB, Winter J (1989) Methanocorpusculaceae, fam. nov. represented by Methanocorpusculum parvum, Methanocorpusculum sinense, spec. nov. and Methanocorpusculum bavaricum, spec. nov. Arch Microbiol 151(5):381–390
Funding
This research was funded by the National Key Research and Development Program of China (2017YFD0500505), and the National Natural Science Foundation of China (31301999).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethics approval
The animal experiment was approved by the Animal Experiment Committee of Nanjing Agricultural University, in accordance with the Regulations for the Administration of Affairs Concerning Experimental Animals (The State Science and Technology Commission of China, 1988).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jin, W., Li, Y., Cheng, Y. et al. The bacterial and archaeal community structures and methanogenic potential of the cecal microbiota of goats fed with hay and high-grain diets. Antonie van Leeuwenhoek 111, 2037–2049 (2018). https://doi.org/10.1007/s10482-018-1096-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-018-1096-7