1887

Abstract

Most Gram-positive bacteria inhabiting the gastrointestinal tract are capable of hydrolysing bile salts. Bile salt hydrolysis is thought to play an important role in various biological processes in the host. Therefore, correct annotation of bacterial bile salt hydrolases (Bsh) in public databases (EC 3.5.1.24) is of importance, especially for lactobacilli, which are considered to play a major role in bile salt hydrolysis . In the present study, all enzymes listed in public databases that belong to the Bsh family and the closely related penicillin V acylase (Pva; EC 3.5.1.11) family were compared with the sequences annotated as Bsh in WCFS1, as an example. In Gram-positive bacteria, a clear distinction was made between the two families using sequence alignment, phylogenetic clustering, and protein homology modelling. Biochemical and structural data on experimentally verified Bsh and Pva enzymes were used for validation of function prediction. Hidden Markov models were constructed from the sequence alignments to enable a more accurate prediction of Bsh-encoding genes, and their distinction from those encoding members of the Pva family. Many Pva-related sequences appeared to be annotated incorrectly as Bsh in public databases. This refinement in the annotation of Bsh family members influences the prediction of the function of -like genes in species of the genus , and it is discussed in detail.

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2008-08-01
2019-11-18
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References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  2. Begley, M., Sleator, R. D., Gahan, C. G. & Hill, C. ( 2005; ). Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect Immun 73, 894–904.[CrossRef]
    [Google Scholar]
  3. Begley, M., Hill, C. & Gahan, C. G. ( 2006; ). Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72, 1729–1738.[CrossRef]
    [Google Scholar]
  4. Bongaerts, G. P., Severijnen, R. S., Tangerman, A., Verrips, A. & Tolboom, J. J. ( 2000; ). Bile acid deconjugation by lactobacilli and its effects in patients with a short small bowel. J Gastroenterol 35, 801–804.[CrossRef]
    [Google Scholar]
  5. Christiaens, H., Leer, R. J., Pouwels, P. H. & Verstraete, W. ( 1992; ). Cloning and expression of a conjugated bile acid hydrolase gene from Lactobacillus plantarum by using a direct plate assay. Appl Environ Microbiol 58, 3792–3798.
    [Google Scholar]
  6. Coleman, J. P. & Hudson, L. L. ( 1995; ). Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens. Appl Environ Microbiol 61, 2514–2520.
    [Google Scholar]
  7. Dashkevicz, M. P. & Feighner, S. D. ( 1989; ). Development of a differential medium for bile salt hydrolase-active Lactobacillus spp. Appl Environ Microbiol 55, 11–16.
    [Google Scholar]
  8. De Smet, I., Van Hoorde, L., Vande Woestyne, M., Christiaens, H. & Verstraete, W. ( 1995; ). Significance of bile salt hydrolytic activities of lactobacilli. J Appl Bacteriol 79, 292–301.[CrossRef]
    [Google Scholar]
  9. Durbin, R., Eddy, S. R., Krogh, A. & Mitchison, G. ( 1998; ). Biological Sequence Analysis: Probablistic Models of Proteins and Nucleic Acids. Cambridge: Cambridge University Press.
  10. Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P. & Cossart, P. ( 2002; ). Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol Microbiol 45, 1095–1106.[CrossRef]
    [Google Scholar]
  11. Edgar, R. C. ( 2004; ). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.[CrossRef]
    [Google Scholar]
  12. Elkins, C. A. & Savage, D. C. ( 1998; ). Identification of genes encoding conjugated bile salt hydrolase and transport in Lactobacillus johnsonii 100–100. J Bacteriol 180, 4344–4349.
    [Google Scholar]
  13. Kim, G. B., Miyamoto, C. M., Meighen, E. A. & Lee, B. H. ( 2004; ). Cloning and characterization of the bile salt hydrolase genes (bsh) from Bifidobacterium bifidum strains. Appl Environ Microbiol 70, 5603–5612.[CrossRef]
    [Google Scholar]
  14. Kirby, L. C., Klein, R. A. & Coleman, J. P. ( 1995; ). Continuous spectrophotometric assay of conjugated bile acid hydrolase. Lipids 30, 863–867.[CrossRef]
    [Google Scholar]
  15. Kleerebezem, M., Boekhorst, J., van Kranenburg, R., Molenaar, D., Kuipers, O. P., Leer, R., Tarchini, R., Peters, S. A., Sandbrink, H. M. & other authors ( 2003; ). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100, 1990–1995.[CrossRef]
    [Google Scholar]
  16. Klinkspoor, J. H., Mok, K. S., Van Klinken, B. J., Tytgat, G. N., Lee, S. P. & Groen, A. K. ( 1999; ). Mucin secretion by the human colon cell line LS174T is regulated by bile salts. Glycobiology 9, 13–19.[CrossRef]
    [Google Scholar]
  17. Kumar, R. S., Brannigan, J. A., Prabhune, A. A., Pundle, A. V., Dodson, G. G., Dodson, E. J. & Suresh, C. G. ( 2006; ). Structural and functional analysis of a conjugated bile salt hydrolase from Bifidobacterium longum reveals an evolutionary relationship with penicillin V acylase. J Biol Chem 281, 32516–32525.[CrossRef]
    [Google Scholar]
  18. Lambert, J. M., Bongers, R. S. & Kleerebezem, M. ( 2007; ). Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillus plantarum. Appl Environ Microbiol 73, 1126–1135.[CrossRef]
    [Google Scholar]
  19. Lambert, J. M., Bongers, R. S., De Vos, W. M. & Kleerebezem, M. ( 2008; ). Functional analysis of four bile salt hydrolase and penicillin acylase family members in Lactobacillus plantarum WCFS1. Appl Environ Microbiol in press
    [Google Scholar]
  20. Leer, R. J., Christiaens, H., Verstraete, W., Peters, L., Posno, M. & Pouwels, P. H. ( 1993; ). Gene disruption in Lactobacillus plantarum strain 80 by site-specific recombination: isolation of a mutant strain deficient in conjugated bile salt hydrolase activity. Mol Gen Genet 239, 269–272.
    [Google Scholar]
  21. Marchler-Bauer, A., Anderson, J. B., Cherukuri, P. F., DeWeese-Scott, C., Geer, L. Y., Gwadz, M., He, S., Hurwitz, D. I., Jackson, J. D. & other authors ( 2005; ). CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 33, D192–D196.[CrossRef]
    [Google Scholar]
  22. Olsson, A. & Uhlen, M. ( 1986; ). Sequencing and heterologous expression of the gene encoding penicillin V amidase from Bacillus sphaericus. Gene 45, 175–181.[CrossRef]
    [Google Scholar]
  23. Overbeek, R., Larsen, N., Walunas, T., D'Souza, M., Pusch, G., Selkov, E., Jr, Liolios, K., Joukov, V., Kaznadzev, D. & other authors ( 2003; ). The ERGO genome analysis and discovery system. Nucleic Acids Res 31, 164–171.[CrossRef]
    [Google Scholar]
  24. Pereira, D. I. & Gibson, G. R. ( 2002; ). Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Crit Rev Biochem Mol Biol 37, 259–281.[CrossRef]
    [Google Scholar]
  25. Pereira, D. I., McCartney, A. L. & Gibson, G. R. ( 2003; ). An in vitro study of the probiotic potential of a bile-salt-hydrolyzing Lactobacillus fermentum strain, and determination of its cholesterol-lowering properties. Appl Environ Microbiol 69, 4743–4752.[CrossRef]
    [Google Scholar]
  26. Rathinaswamy, P., Pundle, A. V., Prabhune, A. A., Sivaraman, H., Brannigan, J. A., Dodson, G. G. & Suresh, C. G. ( 2005; ). Cloning, purification, crystallization and preliminary structural studies of penicillin V acylase from Bacillus subtilis. Acta Crystallogr Sect F Struct Biol Cryst Commun 61, 680–683.[CrossRef]
    [Google Scholar]
  27. Ridlon, J. M., Kang, D. J. & Hylemon, P. B. ( 2006; ). Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47, 241–259.
    [Google Scholar]
  28. Rossocha, M., Schultz-Heienbrok, R., von Moeller, H., Coleman, J. P. & Saenger, W. ( 2005; ). Conjugated bile acid hydrolase is a tetrameric N-terminal thiol hydrolase with specific recognition of its cholyl but not of its tauryl product. Biochemistry 44, 5739–5748.[CrossRef]
    [Google Scholar]
  29. Shimotoyodome, A., Meguro, S., Hase, T., Tokimitsu, I. & Sakata, T. ( 2000; ). Decreased colonic mucus in rats with loperamide-induced constipation. Comp Biochem Physiol A Mol Integr Physiol 126, 203–212.[CrossRef]
    [Google Scholar]
  30. Suresh, C. G., Pundle, A. V., SivaRaman, H., Rao, K. N., Brannigan, J. A., McVey, C. E., Verma, C. S., Dauter, Z., Dodson, E. J. & Dodson, G. G. ( 1999; ). Penicillin V acylase crystal structure reveals new Ntn-hydrolase family members. Nat Struct Biol 6, 414–416.[CrossRef]
    [Google Scholar]
  31. Tanaka, H., Doesburg, K., Iwasaki, T. & Mierau, I. ( 1999; ). Screening of lactic acid bacteria for bile salt hydrolase activity. J Dairy Sci 82, 2530–2535.[CrossRef]
    [Google Scholar]
  32. Tanaka, H., Hashiba, H., Kok, J. & Mierau, I. ( 2000; ). Bile salt hydrolase of Bifidobacterium longum – biochemical and genetic characterization. Appl Environ Microbiol 66, 2502–2512.[CrossRef]
    [Google Scholar]
  33. Tannock, G. W., Dashkevicz, M. P. & Feighner, S. D. ( 1989; ). Lactobacilli and bile salt hydrolase in the murine intestinal tract. Appl Environ Microbiol 55, 1848–1851.
    [Google Scholar]
  34. Tannock, G. W., Tangerman, A., Van Schaik, A. & McConnell, M. A. ( 1994; ). Deconjugation of bile acids by lactobacilli in the mouse small bowel. Appl Environ Microbiol 60, 3419–3420.
    [Google Scholar]
  35. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  36. van der Heijden, R. T., Snel, B., van Noort, V. & Huynen, M. A. ( 2007; ). Orthology prediction at scalable resolution by phylogenetic tree analysis. BMC Bioinformatics 8, 83 [CrossRef]
    [Google Scholar]
  37. Wijaya, A., Hermann, A., Abriouel, H., Specht, I., Yousif, N. M., Holzapfel, W. H. & Franz, C. M. ( 2004; ). Cloning of the bile salt hydrolase (bsh) gene from Enterococcus faecium FAIR-E 345 and chromosomal location of bsh genes in food enterococci. J Food Prot 67, 2772–2778.
    [Google Scholar]
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(a) CLUSTAL_X alignment of sequences in the Bsh cluster. (b) CLUSTAL_X alignment of sequences in the Pva cluster. For clarity, one representative sequence is shown when sequences of different strains of the same organism are identical or nearly identical. Black arrowheads indicate catalytic residues; grey arrowheads indicate binding-pocket residues.

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Annotation of Gram-positive CBAH superfamily members in the phylogenetic tree.

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HMM motifs for Bshand Pvaare available as text files.

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HMM motifs for Bshand Pvaare available as text files.

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Results of search in sequenced genomes with HMMs for Bsh and Pva, respectively, sorted by the score for either of the HMMs, is available as an Excel file.

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