Skip to main content
SpringerLink
Log in

Comparative Genome Analysis of Prevotella ruminicola and Prevotella bryantii: Insights into Their Environmental Niche

  • Genes and Genomes
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The Prevotellas comprise a diverse group of bacteria that has received surprisingly limited attention at the whole genome-sequencing level. In this communication, we present the comparative analysis of the genomes of Prevotella ruminicola 23 (GenBank: CP002006) and Prevotella bryantii B14 (GenBank: ADWO00000000), two gastrointestinal isolates. Both P. ruminicola and P. bryantii have acquired an extensive repertoire of glycoside hydrolases that are targeted towards non-cellulosic polysaccharides, especially GH43 bifunctional enzymes. Our analysis demonstrates the diversity of this genus. The results from these analyses highlight their role in the gastrointestinal tract, and provide a template for additional work on genetic characterization of these species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. 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. Int J Syst Bacteriol 47:284–288

    Article  CAS  PubMed  Google Scholar 

  2. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    Article  CAS  PubMed  Google Scholar 

  3. Bryant MP, Small N, Bouma C, Chu H (1958) Bacteroides ruminicola n. sp. and Succinimonas amylolytica; the new genus and species; species of succinic acid-producing anaerobic bacteria of the bovine rumen. J Bacteriol 76:15–23

    CAS  PubMed  Google Scholar 

  4. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238

    Article  CAS  PubMed  Google Scholar 

  5. Delcher AL, Phillippy A, Carlton J, Salzberg SL (2002) Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30:2478–2483

    Article  PubMed  Google Scholar 

  6. Downes J, Liu M, Kononen E, Wade WG (2009) Prevotella micans sp. nov., isolated from the human oral cavity. Int J Syst Evol Microbiol 59:771–774

    Article  CAS  PubMed  Google Scholar 

  7. Downes J, Sutcliffe IC, Hofstad T, Wade WG (2006) Prevotella bergensis sp. nov., isolated from human infections. Int J Syst Evol Microbiol 56:609–612

    Article  PubMed  Google Scholar 

  8. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  Google Scholar 

  9. Felsenstein J (2004) PHYLIP version 3.6 [computer progam]. Seattle: Department of Genome Sciences, University of Washington, Seattle. Available at: http://evolution.genetics.washington.edu/phylip.html. Accessed 26 Oct 2009

  10. Gardner RG, Russell JB, Wilson DB, Wang GR, Shoemaker NB (1996) Use of a modified Bacteroides–Prevotella shuttle vector to transfer a reconstructed beta-1, 4-d-endoglucanase gene into Bacteroides uniformis and Prevotella ruminicola B(1)4. Appl Environ Microbiol 62:196–202

    CAS  PubMed  Google Scholar 

  11. Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57

    Article  PubMed  Google Scholar 

  12. Holdeman LV, Good IJ, Moore WE (1976) Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl Environ Microbiol 31:359–375

    CAS  PubMed  Google Scholar 

  13. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  CAS  PubMed  Google Scholar 

  14. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1:7

    Article  PubMed  Google Scholar 

  15. Martens EC, Chiang HC, Gordon JI (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447–457

    Article  CAS  PubMed  Google Scholar 

  16. Morrison M, Daugherty SC, Nelson WC, Davidsen T, Nelson KE (2009) The FibRumBa database: a resource for biologists with interests in gastrointestinal microbial ecology, plant biomass degradation, and anaerobic microbiology. Microbial ecology 59(2):212–213

    Article  PubMed  Google Scholar 

  17. Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Nelson WC, Ketchum KA, McDonald L, Utterback TR, Malek JA, Linher KD, Garrett MM, Stewart AM, Cotton MD, Pratt MS, Phillips CA, Richardson D, Heidelberg J, Sutton GG, Fleischmann RD, Eisen JA, Fraser CM et al (1999) Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329

    Article  CAS  PubMed  Google Scholar 

  18. Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Nelson WC, Ketchum KA, McDonald L, Utterback TR, Malek JA, Linher KD, Garrett MM, Stewart AM, Cotton MD, Pratt MS, Phillips CA, Richardson D, Heidelberg J, Sutton GG, Fleischmann RD, Eisen JA, White O, Salzberg SL, Smith HO, Venter JC, Fraser CM (1999) Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329

    Article  CAS  PubMed  Google Scholar 

  19. Nierman WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE, Eisen JA, Heidelberg JF, Alley MR, Ohta N, Maddock JR, Potocka I, Nelson WC, Newton A, Stephens C, Phadke ND, Ely B, DeBoy RT, Dodson RJ, Durkin AS, Gwinn ML, Haft DH, Kolonay JF, Smit J, Craven MB, Khouri H, Shetty J, Berry K, Utterback T, Tran K, Wolf A, Vamathevan J, Ermolaeva M, White O, Salzberg SL, Venter JC, Shapiro L, Fraser CM, Eisen J (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98:4136–4141

    Article  CAS  PubMed  Google Scholar 

  20. Outten FW, Huffman DL, Hale JA, O'Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276:30670–30677

    Article  CAS  PubMed  Google Scholar 

  21. Paster BJ, Dewhirst FE, Olsen I, Fraser GJ (1994) Phylogeny of bacteroides, prevotella, and porphyromonas spp. and related bacteria. J Bacteriol 176:725–732

    CAS  PubMed  Google Scholar 

  22. Portillo MC, Gonzalez JM (2009) CRISPR elements in the Thermococcales: evidence for associated horizontal gene transfer in Pyrococcus furiosus. J Appl Genet 50:421–430

    CAS  PubMed  Google Scholar 

  23. Ramsak A, Peterka M, Tajima K, Martin JC, Wood J, Johnston ME, Aminov RI, Avgustin G (2000) Unravelling the genetic diversity of ruminal bacteria belonging to the CFB phylum. FEMS Microbiol Ecol 33:69–79

    Article  CAS  PubMed  Google Scholar 

  24. Retief JD (2000) Phylogenetic analysis using PHYLIP. Methods Mol Biol 132:243–258

    CAS  PubMed  Google Scholar 

  25. Robinson IM, Allison MJ, Bucklin JA (1981) Characterization of the cecal bacteria of normal pigs. Appl Environ Microbiol 41:950–955

    CAS  PubMed  Google Scholar 

  26. Salzberg SL, Delcher AL, Kasif S, White O (1998) Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26:544–548

    Article  CAS  PubMed  Google Scholar 

  27. Schmidt HA, von Haeseler A (2007) Maximum-likelihood analysis using TREE-PUZZLE. Curr Protoc Bioinformatics Chapter 6: Unit 6.6

  28. Shah HN, Collins DM (1990) Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. Int J Syst Bacteriol 40:205–208

    Article  CAS  PubMed  Google Scholar 

  29. Shoemaker NB, Vlamakis H, Hayes K, Salyers AA (2001) Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol 67:561–568

    Article  CAS  PubMed  Google Scholar 

  30. Sorek R, Kunin V, Hugenholtz P (2008) CRISPR—a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181–186

    Article  CAS  PubMed  Google Scholar 

  31. Ueki A, Akasaka H, Satoh A, Suzuki D, Ueki K (2007) Prevotella paludivivens sp. nov., a novel strictly anaerobic, Gram-negative, hemicellulose-decomposing bacterium isolated from plant residue and rice roots in irrigated rice-field soil. Int J Syst Evol Microbiol 57:1803–1809

    Article  PubMed  Google Scholar 

  32. Van Gylswyk NO (1990) Enumeration and presumptive identification of some functional-groups of bacteria in the rumen of dairy-cows fed grass silage-based diets. Fems Microbiol Ecol 73:243–253

    Article  Google Scholar 

  33. Whitford MF, Forster RJ, Beard CE, Gong J, Teather RM (1998) Phylogenetic analysis of rumen bacteria by comparative sequence analysis of cloned 16S rRNA genes. Anaerobe 4:153–163

    Article  CAS  PubMed  Google Scholar 

  34. 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

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The North American Consortium for Genomics of Fibrolytic Ruminal Bacteria includes I. K. O. Cann, R. I. Mackie, and B. A. White (University of Illinois), C. W. Forsberg (University of Guelph), E. Mongodin and S. Daugherty (University of Maryland), J. B. Russell and D. B. Wilson (Cornell University), W. C. Nelson (UCLA), Karen E. Nelson (JCVI) and Mark Morrison (The Ohio State University). The Consortium was supported by the Initiative for Future Agriculture and Food Systems, Grant no. 2000-52100-9618 and Grant No 2001-52100-11330, from the USDA Cooperative State Research, Education, and Extension Service's National Research Initiative Competitive Grants Program. We also gratefully acknowledge the support from Tanja Davidson and Granger Sutton at the JCVI for their recent assistance with the Fibrumba database and webpage curation. We also thank Jonathan Badger for the use of his tree-building scripts.

Author information

Author notes

  1. Mark Morrison

    Present address: CSIRO Livestock Industries, Queensland Bioscience Precinct, 306 Carmody Road, St Lucia, QLD, Australia, 4069

Authors and Affiliations

  1. Department of Human Genomic Medicine, The J. Craig Venter Institute (JCVI), 9704 Medical Center Drive, Rockville, MD, 20850, USA

    Janaki Purushe, Derrick E. Fouts & Karen E. Nelson

  2. The MAPLE Research Initiative, Department of Animal Sciences, The Ohio State University, Columbus, OH, 43210, USA

    Mark Morrison

  3. Departments of Animal Sciences and Pathobiology, University of Illinois, 1207 W. Gregory Drive, Urbana, IL, 61801, USA

    Bryan A. White & Roderick I. Mackie

  4. Architecture et Fonction des Macromolécules Biologiques, UMR6098, CNRS and Universités of Aix-Marseille I and II, 13288, Marseille, France

    Pedro M. Coutinho & Bernard Henrissat

Authors
  1. Janaki Purushe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Derrick E. Fouts
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark Morrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bryan A. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roderick I. Mackie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pedro M. Coutinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bernard Henrissat
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Karen E. Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

the North American Consortium for Rumen Bacteria

Corresponding author

Correspondence to Karen E. Nelson.

Additional information

Janaki Purushe and Derrick E. Fouts contributed equal work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Purushe, J., Fouts, D.E., Morrison, M. et al. Comparative Genome Analysis of Prevotella ruminicola and Prevotella bryantii: Insights into Their Environmental Niche. Microb Ecol 60, 721–729 (2010). https://doi.org/10.1007/s00248-010-9692-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9692-8

Keywords

Search

Navigation