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Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE (Open Access)

Comparison of microbial diversity in rumen and small intestine of Xinong Saanen dairy goats using 16S rRNA gene high-throughput sequencing

Cong Li https://orcid.org/0000-0003-2588-4781 A , Yanan Geng A , Ping Wang A , Huaiping Shi A and Jun Luo A B
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, No. 22 Xinong Road, Yangling, Shaanxi 712100, China.

B Corresponding author. Email: luojun@nwsuaf.edu.cn

Animal Production Science - https://doi.org/10.1071/AN20459
Submitted: 13 October 2020  Accepted: 12 July 2021   Published online: 17 August 2021

Journal Compilation © CSIRO 2021 Open Access CC BY

Abstract

Context: Gastrointestinal microorganisms play an important role in ruminant digestion and metabolism, immune regulation and disease prevention and control. Different parts of the digestive tract have different functions and microbial community structures.

Aims: This study aims to explore the microbial diversity in the rumen and the small intestine of Xinong Saanen dairy goats.

Methods: Rumen fluid and jejunum fluid from three Xinong Saanen dairy bucks with the average slaughter weight of 33.93 ± 0.68 kg were collected and analysed for microbial diversity, by using 16S rRNA gene high-throughput sequencing.

Key results: In total, 1118 operational taxonomic units (OTUs) were identified, with 1020 OTUs and 649 OTUs being clustered to rumen and jejunum samples respectively. Alpha-diversity indices were significantly (P < 0.05) different between rumen and jejunum, as indicated by the fact that the rumen microbial community diversity, richness and uniformity/evenness were higher than those of jejunum. At the phylum level, the dominant phyla in the rumen were Bacteroidetes (66.7%) and Firmicutes (25.1%), accounting for 91.8% of the rumen microorganisms. The dominant phylum in the jejunum was Firmicutes, accounting for 73.0% of the jejunum microorganisms. At the genus level, the dominant bacteria in the rumen were Prevotella_1, norank_f_Bacteroidales_BS11_gut_group, Rikenellaceae_RC9_gut_group, Christensenellaceae_R-7_group and Family_XIII_AD3011_group, whereas the dominant bacteria in the jejunum were Omboutsia, Aeriscardovia, Intestinibacter, unclassified_f_Peptostreptococcaceae and unclassified_f_Bifidobacteriaceae. Clusters of Orthologous Groups (COG) and Kyoto Encyclopedia of Genes and Genomes (KEGG) results showed that the major functions of microorganisms in the rumen and jejunum were carbohydrate metabolism, amino acid metabolism, nucleotide metabolism, membrane transport and translation. Interestingly, fructose and mannose metabolism and peptidoglycan biosynthesis were abundant in the rumen, while homologous recombination and nucleotide excision repair were abundant in the jejunum.

Conclusions: Our study clarified the differences in microbial diversity and community structure between the rumen and the jejunum in Xinong Saanen dairy goats. Prevotella was the most predominant genus in the rumen, compared with Romboutsia, Bifidobacterium as well as Peptostreptococcaceae genera, which were the predominant genera in the jejunum.

Implications: In combination with the functional prediction of microorganisms and the metabolic characteristics of different parts of the digestive tract in ruminants, our findings provided information for further exploring the relationship among genes, species and functions of microorganisms and their hosts’ nutritional and physiological functions.

Keywords: 16S rRNA gene high-throughput sequencing, dairy goats, functional prediction, microbial diversity.


References

Avgustin G, Wallace RJ, Flint HJ (1997) Phenotypic diversity among ruminal isolates of Prevotella ruminicola: proposal of Prevotella brevis sp. nov., Prevotella bryantii sp. nov., and Prevotella albensis sp. nov. and redefinition of Prevotella ruminicola. International Journal of Systematic Bacteriology 47, 284–288.
Phenotypic diversity among ruminal isolates of Prevotella ruminicola: proposal of Prevotella brevis sp. nov., Prevotella bryantii sp. nov., and Prevotella albensis sp. nov. and redefinition of Prevotella ruminicola.Crossref | GoogleScholarGoogle Scholar | 9103611PubMed |

Baurhoo B, Mustafa A (2014) Short communication: effects of molasses supplementation on performance of lactating cows fed high-alfalfa silage diets. Journal of Dairy Science 97, 1072–1076.
Short communication: effects of molasses supplementation on performance of lactating cows fed high-alfalfa silage diets.Crossref | GoogleScholarGoogle Scholar | 24315324PubMed |

Bekele AZ, Koike S, Kobayashi Y (2010) Genetic diversity and diet specificity of ruminal Prevotella revealed by 16S rRNA gene-based analysis. FEMS Microbiology Letters 305, 49–57.
Genetic diversity and diet specificity of ruminal Prevotella revealed by 16S rRNA gene-based analysis.Crossref | GoogleScholarGoogle Scholar | 20158525PubMed |

Brulc JM, Antonopoulos DA, Miller ME, Wilson MK, Yannarell AC, Dinsdale EA, Edwards RE, Frank ED, Emerson JB, Wacklin P, Coutinho PM, Henrissat B, Nelson KE, White BA (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proceedings of the National Academy of Sciences of the United States of America 106, 1948–1953.
Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases.Crossref | GoogleScholarGoogle Scholar | 19181843PubMed |

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, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.
QIIME allows analysis of high-throughput community sequencing data.Crossref | GoogleScholarGoogle Scholar | 20383131PubMed |

Carberry CA, Kenny DA, Kelly AK, Waters SM (2014) Quantitative analysis of ruminal methanogenic microbial populations in beef cattle divergent in phenotypic residual feed intake (RFI) offered contrasting diets. Journal of Animal Science and Biotechnology 5, 41
Quantitative analysis of ruminal methanogenic microbial populations in beef cattle divergent in phenotypic residual feed intake (RFI) offered contrasting diets.Crossref | GoogleScholarGoogle Scholar | 25276350PubMed |

Combes S, Michelland RJ, Monteils V, Cauquil L, Soulie V, Tran NU, Gidenne T, Fortun-Lamothe L (2011) Postnatal development of the rabbit caecal microbiota composition and activity. FEMS Microbiology Ecology 77, 680–689.
Postnatal development of the rabbit caecal microbiota composition and activity.Crossref | GoogleScholarGoogle Scholar | 21658088PubMed |

de Oliveira MN, Jewell KA, Freitas FS, Benjamin LA, Totola MR, Borges AC, Moraes CA, Suen G (2013) Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer. Veterinary Microbiology 164, 307–314.
Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer.Crossref | GoogleScholarGoogle Scholar | 23490556PubMed |

DeFrain JM, Hippen AR, Kalscheur KF, Jardon PW (2004) Feeding glycerol to transition dairy cows: effects on blood metabolites and lactation performance. Journal of Dairy Science 87, 4195–4206.
Feeding glycerol to transition dairy cows: effects on blood metabolites and lactation performance.Crossref | GoogleScholarGoogle Scholar | 15545383PubMed |

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. Applied and Environmental Microbiology 72, 5069–5072.
Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.Crossref | GoogleScholarGoogle Scholar | 16820507PubMed |

DeVries TJ, Gill RM (2012) Adding liquid feed to a total mixed ration reduces feed sorting behavior and improves productivity of lactating dairy cows. Journal of Dairy Science 95, 2648–2655.
Adding liquid feed to a total mixed ration reduces feed sorting behavior and improves productivity of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 22541492PubMed |

Di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA, Thomas BC, Goodrich JK, Bell JT, Spector TD, Banfield JF, Ley RE (2013) The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife 2, e01102
The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 24137540PubMed |

Durso LM, Harhay GP, Bono JL, Smith TP (2011) Virulence-associated and antibiotic resistance genes of microbial populations in cattle feces analyzed using a metagenomic approach. Journal of Microbiological Methods 84, 278–282.
Virulence-associated and antibiotic resistance genes of microbial populations in cattle feces analyzed using a metagenomic approach.Crossref | GoogleScholarGoogle Scholar | 21167876PubMed |

Dylag K, Hubalewska-Mazgaj M, Surmiak M, Szmyd J, Brzozowski T (2014) Probiotics in the mechanism of protection against gut inflammation and therapy of gastrointestinal disorders. Current Pharmaceutical Design 20, 1149–1155.
Probiotics in the mechanism of protection against gut inflammation and therapy of gastrointestinal disorders.Crossref | GoogleScholarGoogle Scholar | 23755726PubMed |

Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308, 1635–1638.
Diversity of the human intestinal microbial flora.Crossref | GoogleScholarGoogle Scholar | 15831718PubMed |

Guo Y, Xu X, Zou Y, Yang Z, Li S, Cao Z (2013) Changes in feed intake, nutrient digestion, plasma metabolites, and oxidative stress parameters in dairy cows with subacute ruminal acidosis and its regulation with pelleted beet pulp. Journal of Animal Science and Biotechnology 4, 31
Changes in feed intake, nutrient digestion, plasma metabolites, and oxidative stress parameters in dairy cows with subacute ruminal acidosis and its regulation with pelleted beet pulp.Crossref | GoogleScholarGoogle Scholar | 23947764PubMed |

Guo J, Li P, Liu S, Miao B, Zeng B, Jiang Y, Li L, Wang L, Chen Y, Zhang H (2020) Characterization of the Rumen Microbiota and Volatile Fatty Acid Profiles of Weaned Goat Kids under Shrub–Grassland Grazing and Indoor Feeding. Animals 10, 176
Characterization of the Rumen Microbiota and Volatile Fatty Acid Profiles of Weaned Goat Kids under Shrub–Grassland Grazing and Indoor Feeding.Crossref | GoogleScholarGoogle Scholar |

He J, Wu Z, Pan D, Guo Y, Zeng X (2017) Effect of selenylation modification on antitumor activity of peptidoglycan from Lactobacillus acidophilus. Carbohydrate Polymers 165, 344–350.
Effect of selenylation modification on antitumor activity of peptidoglycan from Lactobacillus acidophilus.Crossref | GoogleScholarGoogle Scholar | 28363558PubMed |

He J, Yi L, Hai L, Ming L, Gao W, Ji R (2018) Characterizing the bacterial microbiota in different gastrointestinal tract segments of the Bactrian camel. Scientific Reports 8, 654
Characterizing the bacterial microbiota in different gastrointestinal tract segments of the Bactrian camel.Crossref | GoogleScholarGoogle Scholar | 29330494PubMed |

Kim M, Morrison M, Yu Z (2011) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiology Ecology 76, 49–63.
Status of the phylogenetic diversity census of ruminal microbiomes.Crossref | GoogleScholarGoogle Scholar | 21223325PubMed |

Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology 31, 814
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences.Crossref | GoogleScholarGoogle Scholar |

LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Current Opinion in Biotechnology 24, 160–168.
Bacteria as vitamin suppliers to their host: a gut microbiota perspective.Crossref | GoogleScholarGoogle Scholar | 22940212PubMed |

Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews. Microbiology 6, 776–788.
Worlds within worlds: evolution of the vertebrate gut microbiota.Crossref | GoogleScholarGoogle Scholar | 18794915PubMed |

Li B, Zhang K, Li C, Wang X, Chen Y, Yang Y (2019) Characterization and Comparison of Microbiota in the Gastrointestinal Tracts of the Goat (Capra hircus) During Preweaning Development. Frontiers in Microbiology 10, 2125
Characterization and Comparison of Microbiota in the Gastrointestinal Tracts of the Goat (Capra hircus) During Preweaning Development.Crossref | GoogleScholarGoogle Scholar | 31572331PubMed |

Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71, 8228–8235.
UniFrac: a new phylogenetic method for comparing microbial communities.Crossref | GoogleScholarGoogle Scholar | 16332807PubMed |

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. Current Microbiology 67, 341–350.
Use of pyrosequencing to characterize the microbiota in the ileum of goats fed with increasing proportion of dietary grain.Crossref | GoogleScholarGoogle Scholar | 23636494PubMed |

Martel CA, Titgemeyer EC, Mamedova LK, Bradford BJ (2011) Dietary molasses increases ruminal pH and enhances ruminal biohydrogenation during milk fat depression. Journal of Dairy Science 94, 3995–4004.
Dietary molasses increases ruminal pH and enhances ruminal biohydrogenation during milk fat depression.Crossref | GoogleScholarGoogle Scholar | 21787935PubMed |

Mitchell LA, Wang A, Stracquadanio G, Kuang Z, Wang X, Yang K, Richardson S, Martin JA, Zhao Y, Walker R, Luo Y, Dai H, Dong K, Tang Z, Yang Y, Cai Y, Heguy A, Ueberheide B, Fenyo D, Dai J, Bader JS, Boeke JD (2017) Synthesis, debugging, and effects of synthetic chromosome consolidation: synVI and beyond. Science 355, eaaf4831

Mitsuoka T (1996) Intestinal flora and human health. Asia Pacific Journal of Clinical Nutrition 5, 2–9.

Moschen I, Broer A, Galic S, Lang F, Broer S (2012) Significance of short chain fatty acid transport by members of the monocarboxylate transporter family (MCT). Neurochemical Research 37, 2562–2568.
Significance of short chain fatty acid transport by members of the monocarboxylate transporter family (MCT).Crossref | GoogleScholarGoogle Scholar | 22878645PubMed |

Murphey ED, Fang G, Sherwood ER (2008) Pretreatment with the Gram-positive bacterial cell wall molecule peptidoglycan improves bacterial clearance and decreases inflammation and mortality in mice challenged with Staphylococcus aureus. Critical Care Medicine 36, 3067–3073.
Pretreatment with the Gram-positive bacterial cell wall molecule peptidoglycan improves bacterial clearance and decreases inflammation and mortality in mice challenged with Staphylococcus aureus.Crossref | GoogleScholarGoogle Scholar | 18824898PubMed |

Myer PR, Wells JE, Smith TP, Kuehn LA, Freetly HC (2015) Cecum microbial communities from steers differing in feed efficiency. Journal of Animal Science 93, 5327–5340.
Cecum microbial communities from steers differing in feed efficiency.Crossref | GoogleScholarGoogle Scholar | 26641052PubMed |

Oba M, Penner GB, Whyte TD, Wierenga K (2010) Effects of feeding triticale dried distillers grains plus solubles as a nitrogen source on productivity of lactating dairy cows. Journal of Dairy Science 93, 2044–2052.
Effects of feeding triticale dried distillers grains plus solubles as a nitrogen source on productivity of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 20412919PubMed |

Patra AK, Yu Z (2015) Essential oils affect populations of some rumen bacteria in vitro as revealed by microarray (RumenBactArray) analysis. Frontiers in Microbiology 6, 297
Essential oils affect populations of some rumen bacteria in vitro as revealed by microarray (RumenBactArray) analysis.Crossref | GoogleScholarGoogle Scholar | 25914694PubMed |

Paz HA, Anderson CL, Muller MJ, Kononoff PJ, Fernando SC (2016) Rumen Bacterial Community Composition in Holstein and Jersey Cows Is Different under Same Dietary Condition and Is Not Affected by Sampling Method. Frontiers in Microbiology 7, 1206
Rumen Bacterial Community Composition in Holstein and Jersey Cows Is Different under Same Dietary Condition and Is Not Affected by Sampling Method.Crossref | GoogleScholarGoogle Scholar | 27536291PubMed |

Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, North American Consortium for Rumen Coutinho PM, Henrissat B, Nelson KE (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microbial Ecology 60, 721–729.
Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche.Crossref | GoogleScholarGoogle Scholar | 20585943PubMed |

Qian H, Lu H, Ding H, Lavoie M, Li Y, Liu W, Fu Z (2015) Analyzing Arabidopsis thaliana root proteome provides insights into the molecular bases of enantioselective imazethapyr toxicity. Scientific Reports 5, 11975
Analyzing Arabidopsis thaliana root proteome provides insights into the molecular bases of enantioselective imazethapyr toxicity.Crossref | GoogleScholarGoogle Scholar | 26153126PubMed |

Richardson SM, Mitchell LA, Stracquadanio G, Yang K, Dymond JS, DiCarlo JE, Lee D, Huang CL, Chandrasegaran S, Cai Y, Boeke JD, Bader JS (2017) Design of a synthetic yeast genome. Science 355, 1040–1044.
Design of a synthetic yeast genome.Crossref | GoogleScholarGoogle Scholar | 28280199PubMed |

Rudi K, Moen B, Sekelja M, Frisli T, Lee MR (2012) An eight-year investigation of bovine livestock fecal microbiota. Veterinary Microbiology 160, 369–377.
An eight-year investigation of bovine livestock fecal microbiota.Crossref | GoogleScholarGoogle Scholar | 22749759PubMed |

Russell JB, Diez-Gonzalez F (1997) The effects of fermentation acids on bacterial growth. Advances in Microbial Physiology 39, 205–234.
The effects of fermentation acids on bacterial growth.Crossref | GoogleScholarGoogle Scholar |

Sakthivel KM, Hariharan S (2017) Regulatory players of DNA damage repair mechanisms: role in Cancer Chemoresistance. Biomedicine and Pharmacotherapy 93, 1238–1245.
Regulatory players of DNA damage repair mechanisms: role in Cancer Chemoresistance.Crossref | GoogleScholarGoogle Scholar | 28738540PubMed |

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. Applied and Environmental Microbiology 75, 7537–7541.
Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.Crossref | GoogleScholarGoogle Scholar | 19801464PubMed |

Shanks OC, Kelty CA, Archibeque S, Jenkins M, Newton RJ, McLellan SL, Huse SM, Sogin ML (2011) Community structures of fecal bacteria in cattle from different animal feeding operations. Applied and Environmental Microbiology 77, 2992–3001.
Community structures of fecal bacteria in cattle from different animal feeding operations.Crossref | GoogleScholarGoogle Scholar | 21378055PubMed |

Singh KM, Ahir VB, Tripathi AK, Ramani UV, Sajnani M, Koringa PG, Jakhesara S, Pandya PR, Rank DN, Murty DS, Kothari RK, Joshi CG (2012) Metagenomic analysis of Surti buffalo (Bubalus bubalis) rumen: a preliminary study. Molecular Biology Reports 39, 4841–4848.
Metagenomic analysis of Surti buffalo (Bubalus bubalis) rumen: a preliminary study.Crossref | GoogleScholarGoogle Scholar | 21947953PubMed |

Singh KM, Reddy B, Patel D, Patel AK, Parmar N, Patel A, Patel JB, Joshi CG (2014) High potential source for biomass degradation enzyme discovery and environmental aspects revealed through metagenomics of Indian buffalo rumen. BioMed Research International 2014, 267189
High potential source for biomass degradation enzyme discovery and environmental aspects revealed through metagenomics of Indian buffalo rumen.Crossref | GoogleScholarGoogle Scholar | 25136572PubMed |

Sniffen CJ, O’Connor JD, Van Soest PJ, Fox DG, Russell JB (1992) A net carbohydrate and protein system for evaluating cattle diets: II. Carbohydrate and protein availability. Journal of Animal Science 70, 3562–3577.
A net carbohydrate and protein system for evaluating cattle diets: II. Carbohydrate and protein availability.Crossref | GoogleScholarGoogle Scholar | 1459919PubMed |

Spence C, Wells WG, Smith CJ (2006) Characterization of the primary starch utilization operon in the obligate anaerobe Bacteroides fragilis: Regulation by carbon source and oxygen. Journal of Bacteriology 188, 4663–4672.
Characterization of the primary starch utilization operon in the obligate anaerobe Bacteroides fragilis: Regulation by carbon source and oxygen.Crossref | GoogleScholarGoogle Scholar | 16788175PubMed |

Swedlow J, Danuser G (2012) Scale integration: the structure and dynamics of macromolecular assemblies, cells and tissues. Current Opinion in Cell Biology 24, 1–3.
Scale integration: the structure and dynamics of macromolecular assemblies, cells and tissues.Crossref | GoogleScholarGoogle Scholar | 22342264PubMed |

Thoetkiattikul H, Mhuantong W, Laothanachareon T, Tangphatsornruang S, Pattarajinda V, Eurwilaichitr L, Champreda V (2013) Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing. Current Microbiology 67, 130–137.
Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing.Crossref | GoogleScholarGoogle Scholar | 23471692PubMed |

Thorens B, Mueckler M (2010) Glucose transporters in the 21st Century. American Journal of Physiology. Endocrinology and Metabolism 298, E141–E145.
Glucose transporters in the 21st Century.Crossref | GoogleScholarGoogle Scholar | 20009031PubMed |

Vallimont JE, Bargo F, Cassidy TW, Luchini ND, Broderick GA, Varga GA (2004) Effects of replacing dietary starch with sucrose on ruminal fermentation and nitrogen metabolism in continuous culture. Journal of Dairy Science 87, 4221–4229.
Effects of replacing dietary starch with sucrose on ruminal fermentation and nitrogen metabolism in continuous culture.Crossref | GoogleScholarGoogle Scholar | 15545386PubMed |

Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267.
Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.Crossref | GoogleScholarGoogle Scholar | 17586664PubMed |

Wang LQ, Zhao F, Liu F, Meng XC (2013) Live/dead state is not the factor influencing adhesion ability of Bifidobacterium animalis KLDS2.0603. Journal of Microbiology 51, 584–589.
Live/dead state is not the factor influencing adhesion ability of Bifidobacterium animalis KLDS2.0603.Crossref | GoogleScholarGoogle Scholar |

Wang J, Wang F, Chu L, Wang H, Zhong Z, Liu Z, Gao J, Duan H (2014) High genetic diversity and novelty in eukaryotic plankton assemblages inhabiting saline lakes in the Qaidam basin. PLoS One 9, e112812
High genetic diversity and novelty in eukaryotic plankton assemblages inhabiting saline lakes in the Qaidam basin.Crossref | GoogleScholarGoogle Scholar | 25549339PubMed |

Wang J, Fan H, Han Y, Zhao J, Zhou Z (2017) Characterization of the microbial communities along the gastrointestinal tract of sheep by 454 pyrosequencing analysis. Asian-Australasian Journal of Animal Sciences 30, 100–110.
Characterization of the microbial communities along the gastrointestinal tract of sheep by 454 pyrosequencing analysis.Crossref | GoogleScholarGoogle Scholar | 27383798PubMed |

Wang Y, Zhang H, Zhu L, Xu Y, Liu N, Sun X, Hu L, Huang H, Wei K, Zhu R (2018) Dynamic Distribution of Gut Microbiota in Goats at Different Ages and Health States. Frontiers in Microbiology 9, 2509
Dynamic Distribution of Gut Microbiota in Goats at Different Ages and Health States.Crossref | GoogleScholarGoogle Scholar | 30405569PubMed |

Weimer PJ (2015) Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Frontiers in Microbiology 6, 296
Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations.Crossref | GoogleScholarGoogle Scholar | 25914693PubMed |

Wen C, Yan W, Sun C, Ji C, Zhou Q, Zhang D, Zheng J, Yang N (2019) The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens. The ISME Journal 13, 1422–1436.
The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens.Crossref | GoogleScholarGoogle Scholar | 30728470PubMed |

Xie ZX, Li BZ, Mitchell LA, Wu Y, Qi X, Jin Z, Jia B, Wang X, Zeng BX, Liu HM, Wu XL, Feng Q, Zhang WZ, Liu W, Ding MZ, Li X, Zhao GR, Qiao JJ, Cheng JS, Zhao M, Kuang Z, Wang X, Martin JA, Stracquadanio G, Yang K, Bai X, Zhao J, Hu ML, Lin QH, Zhang WQ, Shen MH, Chen S, Su W, Wang EX, Guo R, Zhai F, Guo XJ, Du HX, Zhu JQ, Song TQ, Dai JJ, Li FF, Jiang GZ, Han SL, Liu SY, Yu ZC, Yang XN, Chen K, Hu C, Li DS, Jia N, Liu Y, Wang LT, Wang S, Wei XT, Fu MQ, Qu LM, Xin SY, Liu T, Tian KR, Li XN, Zhang JH, Song LX, Liu JG, Lv JF, Xu H, Tao R, Wang Y, Zhang TT, Deng YX, Wang YR, Li T, Ye GX, Xu XR, Xia ZB, Zhang W, Yang SL, Liu YL, Ding WQ, Liu ZN, Zhu JQ, Liu NZ, Walker R, Luo Y, Wang Y, Shen Y, Yang H, Cai Y, Ma PS, Zhang CT, Bader JS, Boeke JD, Yuan YJ (2017) ‘Perfect’ designer chromosome V and behavior of a ring derivative Science 355, eaaf4704

Yang Y, Yin Y, Chen X, Chen C, Xia Y, Qi H, Baker PN, Zhang H, Han TL (2019) Evaluating different extraction solvents for GC–MS based metabolomic analysis of the fecal metabolome of adult and baby giant pandas. Scientific Reports 9, 12017.

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. Scientific Reports 6, 20329
Grain-rich diets altered the colonic fermentation and mucosa-associated bacterial communities and induced mucosal injuries in goats.Crossref | GoogleScholarGoogle Scholar | 26841945PubMed |

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 Microbiology Ecology 83, 504–514.
Microbial ecology of the rumen evaluated by 454 GS FLX pyrosequencing is affected by starch and oil supplementation of diets.Crossref | GoogleScholarGoogle Scholar | 22974422PubMed |

Zhang H, Shao M, Huang H, Wang S, Ma L, Wang H, Hu L, Wei K, Zhu R (2018) The Dynamic Distribution of Small-Tail Han Sheep Microbiota across Different Intestinal Segments. Frontiers in Microbiology 9, 32
The Dynamic Distribution of Small-Tail Han Sheep Microbiota across Different Intestinal Segments.Crossref | GoogleScholarGoogle Scholar | 29445360PubMed |

Zhang L, Jiang X, Li A, Waqas M, Gao X, Li K, Xie G, Zhang J, Mehmood K, Zhao S, Wangdui B, Li J (2020) Characterization of the microbial community structure in intestinal segments of yak (Bos grunniens). Anaerobe 61, 102115
Characterization of the microbial community structure in intestinal segments of yak (Bos grunniens).Crossref | GoogleScholarGoogle Scholar | 31711887PubMed |

Zubiria I, Garcia-Rodriguez A, Atxaerandio R, Ruiz R, Benhissi H, Mandaluniz N, Lavin JL, Abecia L, Goiri I (2019) Effect of Feeding Cold-Pressed Sunflower Cake on Ruminal Fermentation, Lipid Metabolism and Bacterial Community in Dairy Cows. Animals 9, 755
Effect of Feeding Cold-Pressed Sunflower Cake on Ruminal Fermentation, Lipid Metabolism and Bacterial Community in Dairy Cows.Crossref | GoogleScholarGoogle Scholar |