Antonie van Leeuwenhoek

, Volume 91, Issue 4, pp 417–422 | Cite as

Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen

  • Delphine Paillard
  • Nest McKain
  • Lal C. Chaudhary
  • Nicola D. Walker
  • Florian Pizette
  • Ingrid Koppova
  • Neil R. McEwan
  • Jan Kopečný
  • Philip E. Vercoe
  • Petra Louis
  • R. John Wallace
Short Communication

Abstract

The Butyrivibrio group comprises Butyrivibrio fibrisolvens and related Gram-positive bacteria isolated mainly from the rumen of cattle and sheep. The aim of this study was to investigate phenotypic characteristics that discriminate between different phylotypes. The phylogenetic position, derived from 16S rDNA sequence data, of 45 isolates from different species and different countries was compared with their fermentation products, mechanism of butyrate formation, lipid metabolism and sensitivity to growth inhibition by linoleic acid (LA). Three clear sub-groups were evident, both phylogenetically and metabolically. Group VA1 typified most Butyrivibrio and Pseudobutyrivibrio isolates, while Groups VA2 and SA comprised Butyrivibrio hungatei and Clostridium proteoclasticum, respectively. All produced butyrate but strains of group VA1 had a butyrate kinase activity <40 U (mg protein)−1, while strains in groups VA2 and SA all exhibited activities >600 U (mg protein)−1. The butyrate kinase gene was present in all VA2 and SA bacteria tested but not in strains of group VA1, all of which were positive for the butyryl-CoA CoA-transferase gene. None of the bacteria tested possessed both genes. Lipase activity, measured by tributyrin hydrolysis, was high in group VA2 and SA strains and low in Group VA1 strains. Only the SA group formed stearic acid from LA. Linoleate isomerase activity, on the other hand, did not correspond with phylogenetic position. Group VA1 bacteria all grew in the presence of 200 μg LA ml−1, while members of Groups VA2 and SA were inhibited by lower concentrations, some as low as 5 μg ml−1. This information provides strong links between phenotypic and phylogenetic properties of this group of clostridial cluster XIVa Gram-positive bacteria.

Keywords

Biohydrogenation Linoleic acid Rumen 

Abbreviations

CLA

conjugated linoleic acid

LA

linoleic acid

References

  1. Attwood GT, Reilly K, Patel BKC (1996) Clostridium proteoclasticum sp. nov., a novel proteolytic bacterium from the bovine rumen. Int J Syst Bacteriol 46:53–758Google Scholar
  2. Charrier C, Duncan GJ, Reid MD, Rucklidge GJ, Henderson D, Young P, Russell VJ, Aminov RI, Flint HJ, Louis P (2006) A novel class of CoA-transferase involved in short-chain fatty acid metabolism in butyrate-producing human colonic bacteria. Microbiology 152:179–185PubMedCrossRefGoogle Scholar
  3. Cheng K-J, Costerton JW (1977) Ultrastructure of Butyrivibrio fibrisolvens - a Gram-positive bacterium? J Bacteriol 129:1506–1512PubMedGoogle Scholar
  4. Diez-Gonzalez F, Bond DR, Jennings E, Russell JB (1999) Alternative schemes of butyrate production in Butyrivibrio fibrisolvens and their relationship to acetate utilization, lactate production, and phylogeny. Arch Microbiol 171:324–330PubMedCrossRefGoogle Scholar
  5. 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 308:1635–1638PubMedCrossRefGoogle Scholar
  6. Forster RJ, Teather RM, Gong J (1996) 16S rDNA analysis of Butyrivibrio fibrisolvens–phylogenetic position and relation to butyrate-producing anaerobic bacteria from the rumen of white-tailed deer. Lett Appl Microbiol 23:218–222PubMedGoogle Scholar
  7. Fukuda S, Furuya H, Suzuki Y, Asanuma N, Hino T (2005) A new strain of Butyrivibrio fibrisolvens that has high ability to isomerise linoleic acid to conjugated linoleic acid. J Gen Appl Microbiol 51:105–113PubMedCrossRefGoogle Scholar
  8. Hazlewood GP, Orpin CG, Greenwood Y, Black ME (1983) Isolation of proteolytic rumen bacteria by use of selective medium containing leaf fraction 1 protein (ribulose bis phosphate carboxylase). Appl Environ Microbiol 45:1780–1784PubMedGoogle Scholar
  9. Hespell RB (1992) The genera Butyrivibrio, Lachnospira, and Roseburia. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The Prokaryotes. Second edition, Springer-Verlag New York Inc, pp 2022–2033Google Scholar
  10. Hespell RB, Wolf R, Bothast RJ (1987) Fermentation of xylans by Butyrivibrio fibrisolvens and other ruminal bacteria. Appl Environ Microbiol 53:2849–2853PubMedGoogle Scholar
  11. Hobson PN (1969) Rumen bacteria. In: Norris JR, Ribbons DW (eds) Methods in Microbiology, vol 3B. Academic Press, London, pp. 133–139Google Scholar
  12. Kepler CR, Tove SB (1967) Biohydrogenation of unsaturated fatty acids. 3. Purification and properties of a linoleate △-12-cis,△-11-trans-isomerase from Butyrivibrio fibrisolvens. J Biol Chem 242:5686–5692PubMedGoogle Scholar
  13. Kopečný J, Zorec M, Mrázek J, Kobayashi Y, Marinšek-Logar R (2003) Butyrivibrio hungatei sp. nov. and Pseudobutyrivibrio xylanivorans sp. nov., butyrate-producing bacteria from the rumen. Int J Syst Evol Microbiol 53:201–209PubMedCrossRefGoogle Scholar
  14. Louis P, Duncan SH, McCrae SI, Millar J, Jackson MS, Flint HJ (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186:2099–2106PubMedCrossRefGoogle Scholar
  15. Moore WEC, Johnson JL, Holdeman LV (1976) Emendation of Bacteroidaceae and Butyrivibrio and description of Desulfomonas gen. nov. and ten new species in the genera Desulfomonas, Butyrivibrio, Eubacterium, Clostridium, and Ruminococcus. Int J Syst Bacteriol 26:238–252Google Scholar
  16. Polan CE, McNeill JJ, Tove SB (1964) Biohydrogenation of unsaturated fatty acids by rumen bacteria. J Bacteriol 88:1056–1064PubMedGoogle Scholar
  17. Richardson AJ, Calder AG, Stewart CS, Smith A (1989) Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol 9:5–8Google Scholar
  18. Rose AH (1955) Measurement of acetate kinase activity. Meth Enzymol 1:591–595CrossRefGoogle Scholar
  19. Rumney CJ, Duncan SH, Henderson C, Stewart CS (1995) Isolation and characteristics of a wheatbran-degrading Butyrivibrio from human faeces. Lett Appl Microbiol 20:232–236PubMedGoogle Scholar
  20. Smeltzer MS, Hart ME, Iandolo JJ (1992) Quantitative spectrophotometric assay for staphylococcal lipase. Appl Environ Microbiol 58:2815–2819PubMedGoogle Scholar
  21. Stewart CS, Flint HJ, Bryant MP (1997) The rumen bacteria. In: Hobson PN, Stewart CS (eds) The rumen microbial ecosystem. Chapman and Hall, London, pp 10–72Google Scholar
  22. Strydom E, Mackie RI, Woods DR (1986) Detection and characterization of extracellular proteases in Butyrivibrio fibrisolvens H17c. Appl Microbiol Biot 24:214–217CrossRefGoogle Scholar
  23. van der Toorn JJTK, van Gylswyk NO (1985) Xylan-digesting bacteria from the rumen of sheep fed maize straw diets. J Gen Microbiol 131:2601–2607Google Scholar
  24. van de Vossenberg JL, Joblin KN (2003) Biohydrogenation of C18 unsaturated fatty acids to stearic acid by a strain of Butyrivibrio hungatei from the bovine rumen. Lett Appl Microbiol 37:424–428PubMedCrossRefGoogle Scholar
  25. van Gylswyk NO, Hippe H, Rainey FA (1996) Pseudobutyrivibrio ruminis gen. nov., sp. nov., a butyrate-producing bacterium from the rumen that closely resembles Butyrivibrio fibrisolvens in phenotype. Int J Syst Bacteriol 46:559–563CrossRefGoogle Scholar
  26. Wallace RJ, Brammall ML (1985) The role of different species of rumen bacteria in the hydrolysis of protein in the rumen. J Gen Microbiol 131:821–832Google Scholar
  27. Wallace RJ, Chaudhary LC, McKain N, McEwan NR, Richardson AJ, Vercoe PE, Walker ND, Paillard D (2006) Clostridium proteoclasticum: a ruminal bacterium that forms stearic acid from linoleic acid. FEMS Microbiol Lett (in press)Google Scholar
  28. Wasowska I, Maia M, Niedźwiedzka KM, Czauderna M, Ramalho-Ribeiro JMC, Devillard E, Shingfield KJ, Wallace RJ (2006) Influence of fish oil on ruminal biohydrogenation of C18 unsaturated fatty acids. Brit J Nutr 95:1199–1211PubMedCrossRefGoogle Scholar
  29. Wedekind KJ, Mansfield HR, Montgomery L (1988) Enumeration and isolation of cellulolytic and hemicellulolytic bacteria from human feces. Appl Environ Microbiol 54:1530–1535PubMedGoogle Scholar
  30. Willems A, Amatmarco M, Collins MD (1996) Phylogenetic analysis of Butyrivibrio strains reveals 3 distinct groups of species within the Clostridium subphylum of the Gram-positive bacteria. Int J Syst Bacteriol 46:195–199PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Delphine Paillard
    • 1
  • Nest McKain
    • 1
  • Lal C. Chaudhary
    • 1
    • 2
  • Nicola D. Walker
    • 1
    • 3
  • Florian Pizette
    • 1
  • Ingrid Koppova
    • 4
  • Neil R. McEwan
    • 1
    • 5
  • Jan Kopečný
    • 4
  • Philip E. Vercoe
    • 6
  • Petra Louis
    • 1
  • R. John Wallace
    • 1
  1. 1.Rowett Research InstituteBucksburnUK
  2. 2.Centre of Advanced Studies in Animal NutritionIndian Veterinary Research InstituteIzatnagarIndia
  3. 3.Unité de Microbiologie INRA de Clermont-Ferrand-TheixSt-Genès ChampanelleFrance
  4. 4.Institute of Animal Physiology & GeneticsPrague 4Czech Republic
  5. 5.Institute of Rural ScienceUniversity of WalesAberystwythUK
  6. 6.Animal Science GroupUniversity of Western AustraliaCrawleyAustralia

Personalised recommendations