Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China

BMC Microbiology

André-Denis G Wright¹  Fu He Yang²  Yi Feng Yang²  Chao Xu²  Kai Ying Wang²  Kun Bao²  Guang Yu Li²  Han Lu Liu²  Zhi Peng Li² 

[1] Department of Animal Science, University of Vermont, 570 Main Street, Burlington, VT 05405-0148, USA;Department of Economical Animal Nutrition and Feed Science, Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, JiLin, China

关键词: Tannin;    Fiber;    Prevotella;    Ecology;   

Others  :  1143563
DOI  :  10.1186/1471-2180-13-151

 received in 2013-03-04, accepted in 2013-07-01,  发布年份 2013

【 摘 要 】

Background

Sika deer (Cervus nippon) have different dietary preferences to other ruminants and are tolerant to tannin-rich plants. Because the rumen bacteria in domestic Sika deer have not been comprehensively studied, it is important to investigate its rumen bacterial population in order to understand its gut health and to improve the productivity of domestic Sika deer.

Results

The rumen bacterial diversity in domestic Sika deer (Cervus nippon) fed oak leaves- (OL group) and corn stalks-based diets (CS group) were elucidated using 16S rRNA gene libraries and denaturing gradient gel electrophoresis (DGGE). Overall, 239 sequences were examined from the two groups, 139 clones from the OL group were assigned to 57 operational taxonomic units (OTUs) and 100 sequences from the CS group were divided into 50 OTUs. Prevotella-like sequences belonging to the phylum Bacteroidetes were the dominant bacteria in both groups (97.2% OL and 77% CS), and sequences related to Prevotella brevis were present in both groups. However, Prevotella shahii-like, Prevotella veroralis-like, Prevotella albensis-like, and Prevotella salivae-like sequences were abundant in the OL group compared to those in the CS group, while Succinivibrio dextrinosolvens-like and Prevotella ruminicola-like sequences were prevalent in the CS group. PCR-DGGE showed that bacterial communities clustered with respect to diets and the genus Prevotella was the dominant bacteria in the rumen of domestic Sika deer. However, the distribution of genus Prevotella from two groups was apparent. In addition, other fibrolytic bacteria, such as Clostridium populeti and Eubacterium cellulosolvens were found in the rumen of domestic Sika deer.

Conclusions

The rumen of domestic Sika deer harbored unique bacteria which may represent novel species. The bacterial composition appeared to be affected by diet, and sequences related to Prevotella spp. may represent new species that may be related to the degradation of fiber biomass or tannins. Moreover, the mechanism and biological functions of Prevotella spp. in the rumen ecosystem, and synergistic interactions with other microorganisms should be noticed.

【 授权许可】

   
2013 Li et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Hiura T, Hashidoko Y, Kobayashi Y, Tahara S: Effective degradation of tannic acid by immobilized rumen microbes of a sika deer (Cervus nippon yesoensis) in winter. Anim Feed Sci Technol 2010, 155(1):1-8.
• [2]Clauss M, Lason K, Gehrke J, Lechner-Doll M, Fickel J, Grune T, Jurgen Streich W: Captive roe deer (Capreolus capreolus) select for low amounts of tannic acid but not quebracho: fluctuation of preferences and potential benefits. Comp Biochem Physiol B Biochem Mol Biol 2003, 136(2):369-382.
• [3]Wright A-DG, Klieve AK: Does the complexity of the rumen microbial ecology preclude methane mitigation? Animal Feed Sci. Technol. 2011, 166-167:248-253.
• [4]Tajima K, Arai S, Ogata K, Nagamine T, Matsui H, Nakamura M, Aminov RI, Benno Y: Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe 2000, 6(5):273-284.
• [5]An DD, Dong XZ, Dong ZY: Prokaryote diversity in the rumen of yak (Bos grunniens) and Jinnan cattle (Bos taurus) estimated by 16S rDNA homology analyses. Anaerobe 2005, 11(4):207-215.
• [6]Pei CX, Liu QA, Dong CS, Li HQ, Jiang JB, Gao WJ: Diversity and abundance of the bacterial 16S rRNA gene sequences in forestomach of alpacas (Lama pacos) and sheep (Ovis aries). Anaerobe 2010, 16(4):426-432.
• [7]Yang LY, Chen J, Cheng XL, Xi DM, Yang SL, Deng WD, Mao HM: Phylogenetic analysis of 16S rRNA gene sequences reveals rumen bacterial diversity in Yaks (Bos grunniens). Mol Biol Rep 2010, 37(1):553-562.
• [8]Aagnes TH, Sormo W, Mathiesen SD: Ruminal microbial digestion in free-living, in captive lichen-ded, and in Starved Reindeer (Rangifer tarandus tarandus) in winter. Appl Environ Microbiol 1995, 61(2):583-591.
• [9]Edwards JE, McEwan NR, Travis AJ, Wallace RJ: 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie Leeuwenhoek Int J Gen Mol Microbiol 2004, 86(3):263-281.
• [10]Ichimura Y, Yamano H, Takano T, Koike S, Kobayashi Y, Tanaka K, Ozaki N, Suzuki M, Okada H, Yamanaka M: Rumen microbes and fermentation of wild sika deer on the Shiretoko peninsula of Hokkaido Island, Japan. Ecol Res 2004, 19(4):389-395.
• [11]Kocherginskaya SA, Aminov RI, White BA: Analysis of the rumen bacterial diversity under two different diet conditions using denaturing gradient gel electrophoresis, random sequencing, and statistical ecology approaches. Anaerobe 2001, 7(3):119-134.
• [12]Shi PJ, Meng K, Zhou ZG, Wang YR, Diao QY, Yao B: The host species affects the microbial community in the goat rumen. Lett Appl Microbiol 2008, 46(1):132-135.
• [13]Lozupone C, Knight R: UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005, 71(12):8228-8235.
• [14]Cho SJ, Cho KM, Shin EC, Lim WJ, Hong SY, Choi BR, Kang JM, Lee SM, Kim YH, Kim H, et al.: 16S rDNA analysis of bacterial diversity in three fractions of cow rumen. J Microbiol Biotechnol 2006, 16(1):92-101.
• [15]Yang SL, Ma SC, Chen J, Mao HM, He YD, Xi DM, Yang LY, He TB, Deng WD: Bacterial diversity in the rumen of Gayals (Bos frontalis), Swamp buffaloes (Bubalus bubalis) and Holstein cow as revealed by cloned 16S rRNA gene sequences. Mol Biol Rep 2010, 37(4):2063-2073.
• [16]Cunha IS, Barreto CC, Costa OYA, Bomfim MA, Castro AP, Kruger RH, Quirino BF: Bacteria and archaea community structure in the rumen microbiome of goats (Capra hircus) from the semiarid region of Brazil. Anaerobe 2011, 17(3):118-124.
• [17]Li MJ, Zhou M, Adamowicz E, Basarab JA, Guan LL: Characterization of bovine ruminal epithelial bacterial communities using 16S rRNA sequencing, PCR-DGGE, and qRT-PCR analysis. Vet Microbiol 2012, 155(1):72-80.
• [18]Pope PB, Mackenzie AK, Gregor I, Smith W, Sundset MA, McHardy AC, Morrison M, Eijsink VG: Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS One 2012, 7(6):e38571.
• [19]Kim M, Morrison M, Yu Z: Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol Ecol 2011, 76(1):49-63.
• [20]Bae HD, McAllister TA, Yanke J, Cheng KJ, Muir AD: Effects of condensed tannins on endoglucanase activity and filter paper digestion by Fibrobacter succinogenes S85. Appl Environ Microbiol 1993, 59(7):2132-2138.
• [21]McSweeney CS, Palmer B, McNeill DM, Krause DO: Microbial interactions with tannins: nutritional consequences for ruminants. Anim Feed Sci Technol 2001, 91(1–2):83-93.
• [22]Jones GA, McAllister TA, Muir AD, Cheng KJ: Effects of sainfoin (Onobrychis viciifolia Scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacteria. Appl Environ Microbiol 1994, 60(4):1374-1378.
• [23]Min BR, Attwood GT, McNabb WC, Molan AL, Barry TN: The effect of condensed tannins from Lotus corniculatus on the proteolytic activities and growth of rumen bacteria. Anim Feed Sci Technol 2005, 121(1–2):45-58.
• [24]Koike S, Yoshitani S, Kobayashi Y, Tanaka K: Phylogenetic analysis of fiber-associated rumen bacterial community and PCR detection of uncultured bacteria. FEMS Microbiol Lett 2003, 229(1):23-30.
• [25]Stevenson DM, Weimer PJ: 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 2007, 75(1):165-174.
• [26]Sundset MA, Praesteng KE, Cann IK, Mathiesen SD, Mackie RI: Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microb Ecol 2007, 54(3):424-438.
• [27]Bekele AZ, Koike S, Kobayashi Y: Genetic diversity and diet specificity of ruminal Prevotella revealed by 16S rRNA gene-based analysis. FEMS Microbiol Lett 2010, 305(1):49-57.
• [28]Wu S, Baldwin RL, Li W, Li C, Connor EE, Li RW: The bacterial community composition of the bovine rumen detected using pyrosequencing of 16S rRNA genes. Metagenomics 2012, 1:1-11.
• [29]Cotta MA: Interaction of ruminal bacteria in the production and utilization of maltooligosaccharides from starch. Appl Environ Microbiol 1992, 58(1):48-54.
• [30]Gardner RG, Wells JE, Russell JB, Wilson DB: The cellular location of Prevotella ruminicola beta-1,4-D-endoglucanase and its occurrence in other strains of ruminal bacteria. Appl Environ Microbiol 1995, 61(9):3288-3292.
• [31]Matsui H, Ogata K, Tajima K, Nakamura M, Nagamine T, Aminov RI, Benno Y: Phenotypic characterization of polysaccharidases produced by four Prevotella type strains. Curr Microbiol 2000, 41(1):45-49.
• [32]Krause DO, Denman SE, Mackie RI, Morrison M, Rae AL, Attwood GT, McSweeney CS: Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiol Rev 2003, 27(5):663-693.
• [33]Fernando SC, Purvis HT, Najar FZ, Sukharnikov LO, Krehbiel CR, Nagaraja TG, Roe BA, DeSilva U: Rumen microbial population dynamics during adaptation to a high-grain diet. Appl Environ Microbiol 2010, 76(22):7482-7490.
• [34]Sadet-Bourgeteau S, Martin C, Morgavi DP: Bacterial diversity dynamics in rumen epithelium of wethers fed forage and mixed concentrate forage diets. Vet Microbiol 2010, 146(1–2):98-104.
• [35]Strobel HJ: Vitamin B12-dependent propionate production by the ruminal bacterium Prevotella ruminicola 23. Appl Environ Microbiol 1992, 58(7):2331-2333.
• [36]Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, North American Consortium for Rumen B, Coutinho PM, Henrissat B, Nelson KE: Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 2010, 60(4):721-729.
• [37]Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA: Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 2008, 6(2):121-131.
• [38]Newbold CJ, Lopez S, Nelson N, Ouda JO, Wallace RJ, Moss AR: Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. Br J Nutr 2005, 94(1):27-35.
• [39]Sundset M, Edwards J, Cheng Y, Senosiain R, Fraile M, Northwood K, Praesteng KE, Glad T, Mathiesen S, Wright AD: Molecular diversity of the rumen microbiome of Norwegian Reindeer on natural summer pasture. Microb Ecol 2009, 57(2):335-348.
• [40]Kobayashi Y: Inclusion of novel bacteria in rumen microbiology: need for basic and applied science. Anim Sci J 2006, 77(4):375-385.
• [41]Whitehead TR: Analyses of the gene and amino acid sequence of the Prevotella (Bacteroides) ruminicola 23 xylanase reveals unexpected homology with endoglucanases from other genera of bacteria. Curr Microbiol 1993, 27(1):27-33.
• [42]Ramsak A, Peterka M, Tajima K, Martin JC, Wood J, Johnston MEA, Aminov RI, Flint HJ, Avgustin G: Unravelling the genetic diversity of ruminal bacteria belonging to the CFB phylum. FEMS Microbiol Ecol 2000, 33(1):69-79.
• [43]Brooker JD, O’Donovan LA, Skene I, Clarke K, Blackall L, Muslera P: Streptococcus caprinus sp. nov, a tannin-resistant ruminal bacterium from feral goats. Lett Appl Microbiol 1994, 18(6):313-318.
• [44]Sly LI, Cahill MM, Osawa R, Fujisawa T: The tannin-degrading species Streptococcus gallolyticus and Streptococcus caprinus are subjective synonyms. Int J Syst Bacteriol 1997, 47(3):893-894.
• [45]Chamkha M, Patel BK, Traore A, Garcia JL, Labat M: Isolation from a shea cake digester of a tannin-degrading Streptococcus gallolyticus strain that decarboxylates protocatechuic and hydroxycinnamic acids, and emendation of the species. Int J Syst Evol Microbiol 2002, 52(Pt 3):939-944.
• [46]Goel G, Puniya AK, Singh K: Tannic acid resistance in ruminal streptococcal isolates. J Basic Microbiol 2005, 45(3):243-245.
• [47]Eaton HL, De Lorme M, Chaney RL, Craig AM: Ovine ruminal microbes are capable of biotransforming hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX). Microb Ecol 2011, 62(2):274-286.
• [48]Hernandez-Eugenio G, Fardeau ML, Cayol JL, Patel BK, Thomas P, Macarie H, Garcia JL, Ollivierx P: Sporanaerobacter acetigenes gen. nov., sp. nov., a novel acetogenic, facultatively sulfur-reducing bacterium. Int J Syst Evol Microbiol 2002, 52(Pt 4):1217-1223.
• [49]Chen S, Dong X: Proteiniphilum acetatigenes gen. nov., sp. nov., from a UASB reactor treating brewery wastewater. Int J Syst Evol Microbiol 2005, 55(Pt 6):2257-2261.
• [50]LaMontagne MG, Michel FC, Holden PA, Reddy CA: Evaluation of extraction and purification methods for obtaining PCR-amplifiable DNA from compost for microbial community analysis. J Microbiol Methods 2002, 49(3):255-264.
• [51]Lane DJ: 16S/23S rRNA sequencing. In Nucleic acid techniques in bacteria systematics. Edited by Stackebrandt EGM. New York: Wiley; 1991:115-175.
• [52]Huber T, Faulkner G, Hugenholtz P: Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 2004, 20(14):2317-2319.
• [53]Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, et al.: The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009, 37:D141-D145.
• [54]Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al.: Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009, 75(23):7537-7541.
• [55]Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
• [56]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
• [57]Muyzer G, de Waal EC, Uitterlinden AG: Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 1993, 59(3):695-700.