Bacterial Community Composition and Fermentation Patterns in the Rumen of Sika Deer (Cervus nippon) Fed Three Different Diets

Microbial Ecology

Volumn 69, Issue 2, 2015, Pages 307-318

  Li, Zhipeng ^a   Wright, André Denis G ^b   Liu, Hanlu ^a   Bao, Kun ^a   Zhang, Tietao ^a   Wang, Kaiying ^a   Cui, Xuezhe ^a   Yang, Fuhe ^a   Zhang, Zhigang ^c   Li, Guangyu ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b UNIVERSITY OF VERMONT   (United States)

^c KUNMING INSTITUTE OF ZOOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S; VOLATILE FATTY ACID;

ANALYSIS; ANIMAL; ANIMAL FOOD; BACTERIUM; CHEMISTRY; CLASSIFICATION; DEER; DIET; DIGESTION; DNA SEQUENCE; FERMENTATION; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; MAIZE; MALE; METABOLISM; MICROBIOLOGY; RUMINANT STOMACH; SILAGE; VETERINARY;

ANIMAL FEED; ANIMALS; BACTERIA; DEER; DIET; DIGESTION; DNA, BACTERIAL; FATTY ACIDS, VOLATILE; FERMENTATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; RNA, RIBOSOMAL, 16S; RUMEN; SEQUENCE ANALYSIS, DNA; SILAGE; ZEA MAYS;

EID: 84925490614     PISSN: 00953628     EISSN: 1432184X     Source Type: Journal    
DOI: 10.1007/s00248-014-0497-z     Document Type: Article

References (70)

1. Wright ADG, Klieve AV (2011) Does the complexity of the rumen microbial ecology preclude methane mitigation? Anim Feed Sci Technol 166–167:248–253. doi:10.1016/j.anifeedsci.2011.04.015
2. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto J-M, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65. doi:10.1038/nature08821
3. Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 70:567–590
4. Kobayashi Y (2006) Inclusion of novel bacteria in rumen microbiology: need for basic and applied science. Anim Sci J 77:375–385. doi:10.1111/j.1740-0929.2006.00362.x
5. Li Z, Liu H, Li G, Bao K, Wang K, Xu C, Yang Y, Yang F, Wright ADG (2013) Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China. BMC Microbiol 13:151
6. Hiura T, Hashidoko Y, Kobayashi Y, Tahara S (2010) Effective degradation of tannic acid by immobilized rumen microbes of a sika deer (Cervus nippon yesoensis) in winter. Anim Feed Sci Technol 155:1–8. doi:10.1016/j.anifeedsci.2009.09.015
7. Yang Y (2010) Effects of tannins on the nutrition utilization and growth of young Sika deer (Cervus nippon) (in Chinese). Master, Chinese Academy of Agricultural Sciences
8. Wang XX, Li XB, Zhao CX, Hu P, Chen H, Liu ZX, Liu GW, Wang Z (2012) Correlation between composition of the bacterial community and concentration of volatile fatty acids in the rumen during the transition period and ketosis in dairy cows. Appl Environ Microbiol 78:2386–2392. doi:10.1128/AEM.07545-11
9. Hernandez-Sanabria E, Guan LL, Goonewardene LA, Li MJ, Mujibi DF, Stothard P, Moore SS, Leon-Quintero MC (2010) Correlation of particular bacterial PCR-denaturing gradient gel electrophoresis patterns with bovine ruminal fermentation parameters and feed efficiency traits. Appl Environ Microbiol 76:6338–6350. doi:10.1128/Aem.01052-10
10. Carberry CA, Kenny DA, Han S, McCabe MS, Waters SM (2012) Effect of phenotypic residual feed intake and dietary forage content on the rumen microbial community of beef cattle. Appl Environ Microbiol 78:4949–4958. doi:10.1128/Aem.07759-11
11. Hernandez-Sanabria E, Goonewardene LA, Wang ZQ, Durunna ON, Moore SS, Guan LL (2012) Impact of feed efficiency and diet on adaptive variations in the bacterial community in the rumen fluid of cattle. Appl Environ Microbiol 78:1203–1214. doi:10.1128/Aem.05114-11
12. Mao SY, Zhang RY, Wang DS, Zhu WY (2012) The diversity of the fecal bacterial community and its relationship with the concentration of volatile fatty acids in the feces during subacute rumen acidosis in dairy cows. BMC Vet Res 8:237. doi:10.1186/1746-6148-8-237
13. Ursell LK, Haiser HJ, Van Treuren W, Garg N, Reddivari L, Vanamala J, Dorrestein PC, Turnbaugh PJ, Knight R (2014) The intestinal metabolome: an intersection between microbiota and host. Gastroenterology 146:1470–1476. doi:10.1053/j.gastro.2014.03.001
14. Mao S, Huo W, Zhu W (2013) Use of pyrosequencing to characterize the microbiota in the ileum of goats fed with increasing proportion of dietary grain. Curr Microbiol 67:341–350. doi:10.1007/s00284-013-0371-0
15. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7:335–336. doi:10.1038/Nmeth.F.303
16. Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Meth 7:668–669. doi:10.1038/nmeth0910-668b
17. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
18. 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. doi:10.1128/AEM.03006-05
19. 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. doi:10.1093/bioinformatics/btp636
20. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, Petrosino JF, Knight R, Birren BW, Consortium HM (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. doi:10.1101/gr.112730.110
21. Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, Sinelnikov I, Budwill K, Nesbo CL, Wishart DS (2012) METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res 40:W88–W95. doi:10.1093/nar/gks497
22. Zhang Z, Geng J, Tang X, Fan H, Xu J, Wen X, Ma Z, Shi P (2014) Spatial heterogeneity and co-occurrence patterns of human mucosal-associated intestinal microbiota. ISME J 8:881–893. doi:10.1038/ismej.2013.185
23. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431–432. doi:10.1093/bioinformatics/btq675
24. Kim M, Morrison M, Yu Z (2011) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol Ecol 76:49–63. doi:10.1111/j.1574-6941.2010.01029.x
25. Stevenson DM, Weimer PJ (2007) Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 75:165–174. doi:10.1007/s00253-006-0802-y
26. Wu S, Baldwin RL, Li W, Li C, Connor EE, Li RW (2012) The bacterial community domposition of the bovine rumen detected using pyrosequencing of 16S rRNA genes. Metagenomics 1:1–11. doi:10.4303/mg/235571
27. Jami E, Mizrahi I (2012) Composition and similarity of bovine rumen microbiota across individual animals. PLoS One 7:e33306. doi:10.1371/journal.pone.0033306
28. Gruninger RJ, Sensen CW, McAllister TA, Forster RJ (2014) Diversity of rumen bacteria in Canadian cervids. PLoS One 9:e89682. doi:10.1371/journal.pone.0089682
29. 1H nuclear magnetic resonance spectroscopy. Appl Environ Microbiol 78:5983–5993. doi:10.1128/AEM.00104-12
30. de Oliveira MNV, Jewell KA, Freitas FS, Benjamin LA, Tótola MR, Borges AC, Moraes CA, Suen G (2013) Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer. Vet Microbiol 164:307–314. doi:10.1016/j.vetmic.2013.02.013
31. Kong Y, Teather R, Forster R (2010) Composition, spatial distribution, and diversity of the bacterial communities in the rumen of cows fed different forages. FEMS Microbiol Ecol 74:612–622. doi:10.1111/j.1574-6941.2010.00977.x
32. Zened A, Combes S, Cauquil L, Mariette J, Klopp C, Bouchez O, Troegeler-Meynadier A, Enjalbert F (2013) Microbial ecology of the rumen evaluated by 454 GS FLX pyrosequencing is affected by starch and oil supplementation of diets. FEMS Microbiol Ecol 83:504–514. doi:10.1111/1574-6941.12011
33. Ishaq SL, Wright ADG (2012) Insight into the bacterial gut microbiome of the North American moose (Alces alces). BMC Microbiol 12:212. doi:10.1186/1471-2180-12-212
34. Gulino LM, Ouwerkerk D, Kang AYH, Maguire AJ, Kienzle M, Klieve AV (2013) Shedding light on the microbial community of the Macropod foregut using 454-amplicon pyrosequencing. PLoS One 8:e61463. doi:10.1371/journal.pone.0061463
35. Shepherd ML, Swecker WS Jr, Jensen RV, Ponder MA (2012) Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons. FEMS Microbiol Lett 326:62–68. doi:10.1111/j.1574-6968.2011.02434.x
36. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651. doi:10.1126/science.1155725
37. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–108. doi:10.1126/science.1208344
38. Pope PB, Denman SE, Jones M, Tringe SG, Barry K, Malfatti SA, McHardy AC, Cheng JF, Hugenholtz P, McSweeney CS, Morrison M (2010) Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores. Proc Natl Acad Sci U S A 107:14793–14798. doi:10.1073/pnas.1005297107
39. Pope PB, Mackenzie AK, Gregor I, Smith W, Sundset MA, McHardy AC, Morrison M, Eijsink VG (2012) Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS One 7:e38571. doi:10.1371/journal.pone.0038571
40. Matsui H, Ogata K, Tajima K, Nakamura M, Nagamine T, Aminov RI, Benno Y (2000) Phenotypic characterization of polysaccharidases produced by four Prevotella type strains. Curr Microbiol 41:45–49. doi:10.1007/s002840010089
41. Kabel MA, Yeoman CJ, Han Y, Dodd D, Abbas CA, de Bont JA, Morrison M, Cann IK, Mackie RI (2011) Biochemical characterization and relative expression levels of multiple carbohydrate esterases of the xylanolytic rumen bacterium Prevotella ruminicola 23 grown on an ester-enriched substrate. Appl Environ Microbiol 77:5671–5681. doi:10.1128/AEM.05321-11
42. Cotta MA (1992) Interaction of ruminal bacteria in the production and utilization of maltooligosaccharides from starch. Appl Environ Microbiol 58:48–54
43. Gardner RG, Wells JE, Russell JB, Wilson DB (1995) The cellular location of Prevotella ruminicola beta-1,4-D-endoglucanase and its occurrence in other strains of ruminal bacteria. Appl Environ Microbiol 61:3288–3292
44. Krause DO, Denman SE, Mackie RI, Morrison M, Rae AL, Attwood GT, McSweeney CS (2003) Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiol Rev 27:663–693. doi:10.1016/S0168-6445(03)00072-X
45. 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. doi:10.1111/j.1574-6968.2010.01911.x
46. Ramsak A, Peterka M, Tajima K, Martin JC, Wood J, Johnston MEA, Aminov RI, Flint HJ, Avgustin G (2000) Unravelling the genetic diversity of ruminal bacteria belonging to the CFB phylum. FEMS Microbiol Ecol 33:69–79. doi:10.1016/S0168-6496(00)00049-0
47. Purushe J, Fouts D, Morrison M, White B, Mackie R, Coutinho P, Henrissat B, Nelson K (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 60:721–729. doi:10.1007/s00248-010-9692-8
48. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227. doi:10.1038/nature11053
49. Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, Turroni S, Biagi E, Peano C, Severgnini M, Fiori J, Gotti R, De Bellis G, Luiselli D, Brigidi P, Mabulla A, Marlowe F, Henry AG, Crittenden AN (2014) Gut microbiome of the Hadza hunter-gatherers. Nat Commun 5:3654. doi:10.1038/ncomms4654
50. Lettat A, Benchaar C (2013) Diet-induced alterations in total and metabolically active microbes within the rumen of dairy cows. PLoS One 8:E60978. doi:10.1371/journal.pone.0060978
51. Belanche A, Doreau M, Edwards JE, Moorby JM, Pinloche E, Newbold CJ (2012) Shifts in the rumen microbiota due to the type of carbohydrate and level of protein ingested by dairy cattle are associated with changes in rumen fermentation. J Nutr 142:1684–1692. doi:10.3945/jn.112.159574
52. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK (2008) Coupled ferredoxin and crotonyl coenzyme a (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J Bacteriol 190:843–850. doi:10.1128/JB.01417-07
53. Johnson KA, Johnson DE (1995) Methane emissions from cattle. J Anim Sci 73:2483–2492
54. Ross EM, Moate PJ, Marett L, Cocks BG, Hayes BJ (2013) Investigating the effect of two methane-mitigating diets on the rumen microbiome using massively parallel sequencing. J Dairy Sci 96:6030–6046. doi:10.3168/jds.2013-6766
55. Cotta M, Forster R (2006) The family Lachnospiraceae, including the genera Butyrivibrio, Lachnospira and Roseburia. In: Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) Dworkin, M. The Prokaryotes, Springer US, pp 1002–1021
56. Li RW, Wu S, Baldwin RLT, Li W, Li C (2012) Perturbation dynamics of the rumen microbiota in response to exogenous butyrate. PLoS One 7:e29392. doi:10.1371/journal.pone.0029392
57. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66:1654–1661. doi:10.1128/AEM.66.4.1654-1661.2000
58. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217:133–139. doi:10.1111/j.1574-6968.2002.tb11467.x
59. Louis P, Flint HJ (2009) Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294:1–8. doi:10.1111/j.1574-6968.2009.01514.x
60. McSweeney CS, Palmer B, McNeill DM, Krause DO (2001) Microbial interactions with tannins: nutritional consequences for ruminants. Anim Feed Sci Technol 91:83–93. doi:10.1016/S0377-8401(01)00232-2
61. Min B, Attwood G, McNabb W, Molan A, Barry T (2005) The effect of condensed tannins from Lotus corniculatus on the proteolytic activities and growth of rumen bacteria. Anim Feed Sci Technol 121:45–58
62. Andries JI, Buysse FX, De Brabander DL, Cottyn BG (1987) Isoacids in ruminant nutrition: their role in ruminal and intermediary metabolism and possible influences on performances—a review. Anim Feed Sci Technol 18:169–180. doi:10.1016/0377-8401(87)90069-1
63. Biddle A, Stewart L, Blanchard J, Leschine S (2013) Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5:627–640. doi:10.3390/d5030627
64. Newbold CJ, Lopez S, Nelson N, Ouda JO, Wallace RJ, Moss AR (2005) Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. Br J Nutr 94:27–35. doi:10.1079/BJN20051445
65. Wang YY, Zhang YL, Wang JB, Meng L (2009) Effects of volatile fatty acid concentrations on methane yield and methanogenic bacteria. Biomass Bioenergy 33:848–853. doi:10.1016/j.biombioe.2009.01.007
66. Christophersen CT, Wright ADG, Vercoe PE (2008) In vitro methane emission and acetate: propionate ratio are decreased when artificial stimulation of the rumen wall is combined with increasing grain diets in sheep. J Anim Sci 86:384–389. doi:10.2527/jas.2007-0373
67. Pope PB, Smith W, Denman SE, Tringe SG, Barry K, Hugenholtz P, McSweeney CS, McHardy AC, Morrison M (2011) Isolation of Succinivibrionaceae implicated in low methane emissions from Tammar wallabies. Science 333:646–648. doi:10.1126/science.1205760
68. Stackebrandt E, Hespell R (2006) The family Succinivibrionaceae. In: Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, Dworkin M (eds) The Prokaryotes. Springer, New York, pp 419–429
69. Allison MJ (1978) Production of branched-chain volatile fatty acids by certain anaerobic bacteria. Appl Environ Microbiol 35:872–877
70. Gorosito AR, Russell JB, Vansoest PJ (1985) Effect of carbon-4 and carbon-5 volatile fatty acids on digestion of plant-cell wall in vitro. J Dairy Sci 68:840–847