Metagenomic insights into the carbohydrate-active enzymes carried by the microorganisms adhering to solid digesta in the rumen of cows

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Wang, Lingling ^a   Hatem, Ayat ^a,b   Catalyurek, Umit V ^a,b   Morrison, Mark ^a,c   Yu, Zhongtang ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Ohio State University   (United States)

^c CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ARABINOFURANOSIDASE; ALPHA LEVO FUCOSIDASE; ALPHA MANNOSIDASE; BETA GALACTOSIDASE; BETA GLUCOSIDASE; BETA MANNOSIDASE; CELLULASE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; CONTIG; ENDO 1,4 BETA XYLANASE; GLUCAN SYNTHASE; GLYCOSIDASE; POLYSACCHARIDE; XYLAN 1,4 BETA XYLOSIDASE; XYLAN ENDO 1,3 BETA XYLOSIDASE;

ARTICLE; CARBOHYDRATE METABOLISM; CATTLE; CONTROLLED STUDY; FIRMICUTES; FOSMID; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PYROSEQUENCING; RUMINANT STOMACH; SIGNAL TRANSDUCTION; SPECIES COMPARISON; TRANSCRIPTION REGULATION;

ANIMALS; BACTERIAL PROTEINS; CATTLE; CELLULASES; CELLULOSE; DIGESTION; ENDO-1,4-BETA XYLANASES; GLYCOSIDE HYDROLASES; METAGENOME; MICROBIAL CONSORTIA; MOLECULAR SEQUENCE ANNOTATION; PHYLOGENY; RUMEN; RUMINANTS; XYLANS;

EID: 84892399148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078507     Document Type: Article

References (40)

1. Weimer PJ (1996) Why don't ruminal bacteria digest cellulose faster? J Dairy Sci 79:1496-1502.
2. N, Wyman C, Dale B, Elander R, Lee YY, et al. (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96:673-686.
3. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, et al. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463-467.
4. Brulc JM, Antonopoulos DA, Miller ME, Wilson MK, Yannarell AC, et al. (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci U S A 106:1948-1953.
5. Pope PB, Mackenzie AK, Gregor I, Smith W, Sundset MA, et al. (2012) Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS One 7:e38571.
6. Del Pozo MV, Fernández-Arrojo L, Gil-Martínez J, Montesinos A, Chernikova TN, et al. (2012) Microbial b-glucosidases from cow rumen metagenome enhance the saccharification of lignocellulose in combination with commercial cellulase cocktail. Biotechnol Biofuels 5:73.
7. Dai X, Zhu Y, Luo Y, Song L, Liu D, et al. (2012) Metagenomic insights into the fibrolytic microbiome in yak rumen. PLoS One 7:e40430.
8. Michalet-Doreau B, Fernandez I, Peyron C, Millet L, Fonty G (2001) Fibrolytic activities and cellulolytic bacterial community structure in the solid and liquid phases of rumen contents. Reprod Nutr Dev 41:187-194.
9. Pope PB, Denman SE, Jones M, Tringe SG, Barry K, et al. (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.
10. Nelson KE, Zinder SH, Hance I, Burr P, Odongo D, et al. (2003) Phylogenetic analysis of the microbial populations in the wild herbivore gastrointestinal tract: insights into an unexplored niche. Environ Microbiol 5: 1212-1220.
11. Sundset MA, Praesteng KE, Cann IK, Mathiesen SD, Mackie RI (2007) Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microb Ecol 54: 424-438.
12. An D, Dong X, Dong Z (2005) Prokaryote diversity in the rumen of yak (Bos grunniens) and Jinnan cattle (Bos taurus) estimated by 16S rDNA homology analyses. Anaerobe 11: 207-215.
13. Yang S, Ma S, Chen J, Mao H, He Y, et al. (2010) 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 37: 2063-2073.
14. Kittelmann S, Janssen PH (2011) Characterization of rumen ciliate community composition in domestic sheep, deer, and cattle, feeding on varying diets, by means of PCR-DGGE and clone libraries. FEMS Microbiology Ecology 75: 468-481.
15. Tajima K, Aminov RI, Nagamine T, Matsui H, Nakamura M, et al. (2001) Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Appl Environ Microbiol 67: 2766-2774.
16. Hook SE, Steele MA, Northwood KS, Wright AD, McBride BW (2011) Impact of high-concentrate feeding and low ruminal pH on methanogens and protozoa in the rumen of dairy cows. Microb Ecol 62: 94-105.
17. McHardy AC, Martín HG, Tsirigos A, Hugenholtz P, Rigoutsos I (2007) Accurate phylogenetic classification of variable-length DNA fragments. Nat Methods 4:63-72.
18. Patil KR, Haider P, Pope PB, Turnbaugh PJ, Morrison M, et al. (2011) Taxonomic metagenome sequence assignment with structured output models. Nat Methods 8:191-192.
19. Wood J, Scott KP, Avgustin G, Newbold CJ, Flint HJ (1998) Estimation of the relative abundance of different Bacteroides and Prevotella ribotypes in gut samples by restriction enzyme profiling of PCR-amplified 16S rRNA gene sequences. Appl Environ Microbiol 64:3683-3689.
20. 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.
21. 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.
22. Ballouz S, Francis AR, Lan R, Tanaka MM (2010) Conditions for the Evolution of Gene Clusters in Bacterial Genomes. PLoS Comput Biol 6: e1000672. doi:10.1371/journal.pcbi.1000672
23. Ricard G, McEwan NR, Dutilh BE, Jouany JP, Macheboeuf D, et al. (2006) Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7:22.
24. Ferrer M, Golyshina OV, Chernikova TN, Khachane AN, Reyes-Duarte D, et al. (2005) Novel hydrolase diversity retrieved from a metagenome library of bovine rumen microflora. Environ Microbiol 7:1996-2010.
25. Mackenzie AK, Pope PB, Pedersen HL, Gupta R, Morrison M, et al. (2012) Two SusD-like proteins encoded within a polysaccharide utilization locus of an uncultured ruminant Bacteroidetes phylotype bind strongly to cellulose. Appl Environ Microbiol 78:5935-5937.
26. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, et al. (2011) Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts. PLoS Biol 9: e1001221. doi:10.1371/journal.pbio.1001221
27. Firkins JL, Yu Z (2006) Characterisation and quantification of the microbial populations of the rumen. In: Sejrsen K, Hvelplund T, Nielsen MO, editors. Ruminant physiology: Digestion, metabolism and impact of nutrition on gene expression, immunology and stress. Wageningen, The Netherlands: Wageningen Academic Publisher. pp. 19-54.
28. Miron J, Ben-Ghedalia D, Morrison M (2001) Invited review: adhesion mechanisms of rumen cellulolytic bacteria. J Dairy Sci 84: 1294-1309.
29. Larue R, Yu Z, Parisi VA, Egan AR, Morrison M (2005) Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing. Environ Microbiol 7:530-543.
30. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11-15.
31. Sambrook J, Russel DW (2001) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
32. Ghangas GS, Hu YJ, Wilson DB (1989) Cloning of a Thermomonospora fusca xylanase gene and its expression in Escherichia coli and Streptomyces lividans. J Bacteriol 171:2963-2969.
33. Kwon KS, Lee J, Kang HG, Hah YC (1994) Detection of beta-Glucosidase Activity in Polyacrylamide Gels with Esculin as Substrate. Appl Environ Microbiol 60:4584-4586.
34. Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43:777-780.
35. Chevreux B, Wetter T, Suhai S (1999) Genome Sequence Assembly Using Trace Signals and Additional Sequence Information. in German Conference on Bioinformatics (Hannover, Germany), pp 45-56.
36. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829.
37. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:233-238.
38. Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC (2010) CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20:1574-1584.
39. Patil KR, Roune L, McHardy AC (2012) The PhyloPythiaS web server for taxonomic assignment of metagenome sequences. PLoS One 7:e38581.
40. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552-1560.