Advertisement

Analysis of the bovine rumen microbiome reveals a diversity of Sus-like polysaccharide utilization loci from the bacterial phylum Bacteroidetes

  • Carly P. RosewarneEmail author
  • Phillip B. Pope
  • Jane L. Cheung
  • Mark Morrison
Short Communication

Abstract

Several unique Sus-like polysaccharide utilization loci (PULs) were identified from bacteria resident in bovine rumen microbiomes through functional screening of a fosmid library. The loci were phylogenetically assigned to the genus Prevotella within the phylum Bacteroidetes. These findings were augmented by a bioinformatic re-evaluation of ruminal Prevotella genomes, revealing additional loci not previously reported in the literature. Analysis of Bacteroidales-affiliated genomes reconstructed from a bovine rumen metagenome in a previous study further expanded the diversity of Sus-like PULs resident in this microbiome. Our findings suggest that Sus-like systems represent an important mechanism for degradation of a range of plant-derived glycans in ruminants.

Keywords

Bacteroidetes Carbohydrate Active Enzyme Fosmid Library Functional Screening Fosmid Clone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This research was supported by funds provided to Meat and Livestock Australia project number B.CCH.1005, as part of the Reducing Emissions from Livestock Research Program, and by a Marie Curie International Incoming Fellowship from the European Commission (awarded to PBP; PIIF-GA-2010-274303). We are grateful to Honglei Chen for preparation of amplicons for 454 pyrosequencing, to Ivan Gregor and Alice McHardy for assistance with PhyloPythiaS, and to Nigel Tomkins for assistance with sample collection.

Supplementary material

10295_2013_1395_MOESM1_ESM.doc (195 kb)
Supplementary material 1 (DOC 195 kb)

References

  1. 1.
    Aguirre de Carcer D, Denman SE, McSweeney CS, Morrison M (2011) Strategy for modular tagged high-throughput amplicon sequencing. Appl Environ Microbiol 77:6310–6312CrossRefGoogle Scholar
  2. 2.
    Aspeborg H, Coutinho PM, Wang Y, Brumer H 3rd, Henrissat B (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12:186PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296PubMedCentralPubMedGoogle Scholar
  4. 4.
    Brulc JM, Antonopoulos DA, Berg Miller ME, Wilson MK, Yannarell AC, Dinsdale EA et al (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci USA 106:1948–1953PubMedCrossRefGoogle Scholar
  5. 5.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucl Acids Res 37:D141–D145PubMedCrossRefGoogle Scholar
  7. 7.
    D’Elia JN, Salyers AA (1996) Contribution of a neopullulanase, a pullulanase, and an alpha-glucosidase to growth of Bacteroides thetaiotaomicron on starch. J Bacteriol 178:7173–7179PubMedCentralPubMedGoogle Scholar
  8. 8.
    Dodd D, Moon Y-H, Swaminathan K, Mackie RI, Cann IKO (2010) Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. J Biol Chem 285:30261–30273PubMedCrossRefGoogle Scholar
  9. 9.
    Duan CJ, Xian L, Zhao GC, Feng Y, Pang H, Bai XL et al (2009) Isolation and partial characterisation of novel genes encoding acidic cellulases from metagenomes of buffalo rumens. J Appl Microbiol 107:245–256PubMedCrossRefGoogle Scholar
  10. 10.
    Gardner RG, Wells JE, Fields MW, Wilson DB, Russell JB (1997) A Prevotella ruminicola B14 operon encoding extracellular polysaccharide hydrolases. Curr Microbiol 35:274–277PubMedCrossRefGoogle Scholar
  11. 11.
    Hess M, Sczyrba A, Egan R, Kim T-W, Chokhawala H, Schroth G et al (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467PubMedCrossRefGoogle Scholar
  12. 12.
    Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucl Acids Res 36:W5–W9PubMedCrossRefGoogle Scholar
  13. 13.
    Kelly W, Leahy SC, Altermann A, Yeoman CJ, Dunne JC, Kong Z et al (2010) The glycobiome of the rumen bacterium Butyrivibrio proteoclasticus B316T highlights adaptation to a polysaccharide-rich environment. PLoS ONE 5:e11942PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS et al (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Mackenzie AK, Pope PB, Pedersen HL, Gupta R, Morrison M, Willats WGT, Eijsink VGH (2012) Two SusD-like proteins encoded within a polysaccharide utilization locus of an uncultured ruminant Bacteroidetes bind strongly to cellulose. Appl Environ Microbiol 78:5935–5937PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Markowitz VM, Chen IMA, Chu K, Szeto E, Palaniappan K, Grechkin Y et al (2012) IMG/M: the integrated metagenome data management and comparative analysis system. Nucl Acids Res 40:D123–D129PubMedCrossRefGoogle Scholar
  17. 17.
    Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP et al (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9:e1001221PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Martens EC, Koropatkin NM, Smith TJ, Gordon JI (2009) Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem 284:24673–24677PubMedCrossRefGoogle Scholar
  19. 19.
    Martens EC, Chiang HC, Gordon JI (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447–457PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Matsushita O, Russell JB, Wilson DB (1991) A bacteroides ruminicola 1,4-β-d-endoglucanase is encoded in two reading frames. J Bacteriol 173:6919–6926PubMedCentralPubMedGoogle Scholar
  21. 21.
    Patil KR, Haider P, Pope PB, Turnbaugh PJ, Morrison M, Scheffer T, McHardy AC (2011) Taxonomic metagenome sequence assignment with structured output models. Nat Methods 8:191–192PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Pitta D, Pinchak W, Dowd S, Osterstock J, Gontcharova V, Youn E et al (2010) Rumen bacterial diversity dynamics associated with changing from bermudagrass hay to grazed winter wheat diets. Microb Ecol 59:511–522PubMedCrossRefGoogle Scholar
  23. 23.
    Pope PB, Mackenzie AK, Gregor I, Smith W, Sundset MA, McHardy AC et al (2012) Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS ONE 7:e38571PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Pope PB, Denman SE, Jones M, Tringe SG, Barry K, Malfatti SA et al (2010) Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores. Proc Natl Acad Sci USA 107:14793–14798PubMedCrossRefGoogle Scholar
  25. 25.
    Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C et al (2012) The Pfam protein families database. Nucl Acids Res 40:D290–D301PubMedCrossRefGoogle Scholar
  26. 26.
    Purushe J, Fouts D, Morrison M, White B, Mackie RI, Coutinho P et al (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 60:721–729PubMedCrossRefGoogle Scholar
  27. 27.
    Rosewarne CP, Pope PB, Denman SE, McSweeney CS, O’Cuiv P, Morrison M (2011) High-yield and phylogenetically robust methods of DNA recovery for analysis of microbial biofilms adherent to plant biomass in the herbivore gut. Microb Ecol 61:448–454PubMedCrossRefGoogle Scholar
  28. 28.
    Shipman JA, Berleman JE, Salyers AA (2000) Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J Bacteriol 182:5365–5372PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Suen G, Weimer PJ, Stevenson DM, Aylward FO, Boyum J, Deneke J et al (2011) The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE 6:e18814PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Wang L, Hatem A, Catalyurek UV, Morrison M, Zu Y (2013) Metagenomic insights into the carbohydrate active enzymes carried by the microorganisms adhering to solid digesta in the rumen of cows. PLoS ONE 8:e78507PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Yin Y, Mao X, Yang JC, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucl Acids Res 40:W445–W451PubMedCrossRefGoogle Scholar
  32. 32.
    Zhu W, Lomsadze A, Borodovsky M (2010) Ab initio gene identification in metagenomic sequences. Nucl Acids Res 38:e132PubMedCrossRefGoogle Scholar

Copyright information

© Crown Copyright 2014

Authors and Affiliations

  • Carly P. Rosewarne
    • 1
    Email author
  • Phillip B. Pope
    • 2
  • Jane L. Cheung
    • 3
  • Mark Morrison
    • 3
    • 4
  1. 1.CSIRO Animal, Food and Health SciencesRiverside Life Sciences CentreNorth RydeAustralia
  2. 2.Department of Chemistry, Biotechnology and Food ScienceNorwegian University of Life SciencesÅsNorway
  3. 3.CSIRO Animal, Food and Health SciencesQueensland Biosciences PrecinctSt LuciaAustralia
  4. 4.The University of Queensland Diamantina InstituteWoolloongabbaAustralia

Personalised recommendations