1887

Abstract

Bile salt hydrolases (BSHs) are gut microbial enzymes that play a significant role in the bile acid modification pathway. Penicillin V acylases (PVAs) are enzymes produced by environmental microbes, having a possible role in pathogenesis or scavenging of phenolic compounds in their microbial habitats. The correct annotation of such physiologically and industrially important enzymes is thus vital. The current methods relying solely on sequence homology do not always provide accurate annotations for these two members of the cholylglycine hydrolase (CGH) family as BSH/PVA enzymes. Here, we present an improved method [binding site similarity (BSS)-based scoring system] for the correct annotation of the CGH family members as BSH/PVA enzymes, which along with the phylogenetic information incorporates the substrate specificity as well as the binding site information. The BSS scoring system was developed through the analysis of the binding sites and binding modes of the available BSH/PVA structures with substrates glycocholic acid and penicillin V. The 198 sequences in the dataset were then annotated accurately using BSS scores as BSH/PVA enzymes. The dataset presented contained sequences from Gram-positive bacteria, Gram-negative bacteria and archaea. The clustering obtained for the dataset using the method described above showed a clear distinction in annotation of Gram-positive bacteria and Gram-negative bacteria. Based on this clustering and a detailed analysis of the sequences of the CGH family in the dataset, we could infer that the CGH genes might have evolved in accordance with the hypothesis stating the evolution of diderms and archaea from the monoderms.

Funding
This study was supported by the:
  • Council of Scientific and Industrial Research
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2014-06-01
2021-05-05
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References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. ( 1997). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  2. Avinash V. S., Panigrahi P., Suresh C. G., Pundle A. V., Ramasamy S. ( 2013). Structural modelling of substrate binding and inhibition in penicillin V acylase from Pectobacterium atrosepticum. Biochem Biophys Res Commun 437:538–543 [CrossRef][PubMed]
    [Google Scholar]
  3. Batta A. K., Salen G., Shefer S. ( 1984). Substrate specificity of cholylglycine hydrolase for the hydrolysis of bile acid conjugates. J Biol Chem 259:15035–15039[PubMed]
    [Google Scholar]
  4. Begley M., Hill C., Gahan C. G. ( 2006). Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72:1729–1738 [CrossRef][PubMed]
    [Google Scholar]
  5. Ben-Bassat A., Bauer K., Chang S. Y., Myambo K., Boosman A., Chang S. ( 1987). Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure. J Bacteriol 169:751–757[PubMed]
    [Google Scholar]
  6. Berman H. M., Westbrook J., Feng Z., Gilliland G., Bhat T. N., Weissig H., Shindyalov I. N., Bourne P. E. ( 2000). The Protein Data Bank. Nucleic Acids Res 28:235–242 [CrossRef][PubMed]
    [Google Scholar]
  7. Bokhove M., Nadal Jimenez P., Quax W. J., Dijkstra B. W. ( 2010). The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket. Proc Natl Acad Sci U S A 107:686–691 [CrossRef][PubMed]
    [Google Scholar]
  8. Chandra P. M., Brannigan J. A., Prabhune A., Pundle A., Turkenburg J. P., Dodson G. G., Suresh C. G. ( 2005). Cloning, preparation and preliminary crystallographic studies of penicillin V acylase autoproteolytic processing mutants. Acta Crystallogr Sect F Struct Biol Cryst Commun 61:124–127 [CrossRef][PubMed]
    [Google Scholar]
  9. 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[PubMed]
    [Google Scholar]
  10. Friesner R. A., Murphy R. B., Repasky M. P., Frye L. L., Greenwood J. R., Halgren T. A., Sanschagrin P. C., Mainz D. T. ( 2006). Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein–ligand complexes. J Med Chem 49:6177–6196 [CrossRef][PubMed]
    [Google Scholar]
  11. Gupta R. S. ( 2011). Origin of diderm (Gram-negative) bacteria: antibiotic selection pressure rather than endosymbiosis likely led to the evolution of bacterial cells with two membranes. Antonie van Leeuwenhoek 100:171–182 [CrossRef][PubMed]
    [Google Scholar]
  12. Halgren T. ( 2007). New method for fast and accurate binding-site identification and analysis. Chem Biol Drug Des 69:146–148 [CrossRef][PubMed]
    [Google Scholar]
  13. Haupt V. J., Daminelli S., Schroeder M. ( 2013). Drug promiscuity in PDB: protein binding site similarity is key. PLoS ONE 8:e65894 [CrossRef][PubMed]
    [Google Scholar]
  14. Henikoff S., Henikoff J. G. ( 1992). Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci U S A 89:10915–10919 [CrossRef][PubMed]
    [Google Scholar]
  15. Jones B. V., Begley M., Hill C., Gahan C. G. M., Marchesi J. R. ( 2008). Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci U S A 105:13580–13585 [CrossRef][PubMed]
    [Google Scholar]
  16. Kovacikova G., Lin W., Skorupski K. ( 2003). The virulence activator AphA links quorum sensing to pathogenesis and physiology in Vibrio cholerae by repressing the expression of a penicillin amidase gene on the small chromosome. J Bacteriol 185:4825–4836 [CrossRef][PubMed]
    [Google Scholar]
  17. Krissinel E., Henrick K. ( 2007). Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797 [CrossRef][PubMed]
    [Google Scholar]
  18. 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][PubMed]
    [Google Scholar]
  19. Lambert J. M., Siezen R. J., de Vos W. M., Kleerebezem M. ( 2008). Improved annotation of conjugated bile acid hydrolase superfamily members in Gram-positive bacteria. Microbiology 154:2492–2500 [CrossRef][PubMed]
    [Google Scholar]
  20. Lodola A., Branduardi D., De Vivo M., Capoferri L., Mor M., Piomelli D., Cavalli A. ( 2012). A catalytic mechanism for cysteine N-terminal nucleophile hydrolases, as revealed by free energy simulations. PLoS ONE 7:e32397 [CrossRef][PubMed]
    [Google Scholar]
  21. Marchler-Bauer A., Zheng C., Chitsaz F., Derbyshire M. K., Geer L. Y., Geer R. C., Gonzales N. R., Gwadz M., Hurwitz D. I. & other authors ( 2013). CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41:D1D348–D352 [CrossRef][PubMed]
    [Google Scholar]
  22. Mukherji R., Bhand A., Prabhune A. A. ( 2013). Production of penicillin V acylase from novel soil actinomycete: identification of isolate and optimization of physico-chemical parameters. World J Biol Biol Sci 1:010–020
    [Google Scholar]
  23. Oinonen C., Rouvinen J. ( 2000). Structural comparison of Ntn-hydrolases. Protein Sci 9:2329–2337 [CrossRef][PubMed]
    [Google Scholar]
  24. Olsson A., Uhlén M. ( 1986). Sequencing and heterologous expression of the gene encoding penicillin V amidase from Bacillus sphaericus. Gene 45:175–181 [CrossRef][PubMed]
    [Google Scholar]
  25. Pronk S., Páll S., Schulz R., Larsson P., Bjelkmar P., Apostolov R., Shirts M. R., Smith J. C., Kasson P. M. & other authors ( 2013). gromacs 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29:845–854 [CrossRef][PubMed]
    [Google Scholar]
  26. Punta M., Coggill P. C., Eberhardt R. Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G. & other authors ( 2012). The Pfam protein families database. Nucleic Acids Res 40:D1D290–D301 [CrossRef][PubMed]
    [Google Scholar]
  27. Rathinaswamy P., Gaikwad S. M., Suresh C. G., Prabhune A. A., Brannigan J. A., Dodson G. G., Pundle A. V. ( 2012). Purification and characterization of YxeI, a penicillin acylase from Bacillus subtilis. Int J Biol Macromol 50:25–30 [CrossRef][PubMed]
    [Google Scholar]
  28. Rawlings N. D., Barrett A. J., Bateman A. ( 2012). merops: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40:D1D343–D350 [CrossRef][PubMed]
    [Google Scholar]
  29. Reddy G. S., Prakash J. S., Vairamani M., Prabhakar S., Matsumoto G. I., Shivaji S. ( 2002). Planococcus antarcticus and Planococcus psychrophilus spp. nov. isolated from cyanobacterial mat samples collected from ponds in Antarctica. Extremophiles 6:253–261 [CrossRef][PubMed]
    [Google Scholar]
  30. 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][PubMed]
    [Google Scholar]
  31. Sousa da Silva A. W., Vranken W. F. ( 2012). acpype – AnteChamber PYthon Parser interfacE. BMC Res Notes 5:367 [CrossRef][PubMed]
    [Google Scholar]
  32. Stellwag E. J., Hylemon P. B. ( 1976). Purification and characterization of bile salt hydrolase from Bacteroides fragilis subsp. fragilis. Biochim Biophys Acta 452:165–176 [CrossRef][PubMed]
    [Google Scholar]
  33. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. ( 2011). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  34. 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][PubMed]
    [Google Scholar]
  35. Valas R. E., Bourne P. E. ( 2011). The origin of a derived superkingdom: how a gram-positive bacterium crossed the desert to become an archaeon. Biol Direct 6:16 [CrossRef][PubMed]
    [Google Scholar]
  36. Valle F., Balbás P., Merino E., Bolivar F. ( 1991). The role of penicillin amidases in nature and in industry. Trends Biochem Sci 16:36–40 [CrossRef][PubMed]
    [Google Scholar]
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