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Abstract

Dysgalacticin is a novel bacteriocin produced by subsp. strain W2580 that has a narrow spectrum of antimicrobial activity directed primarily against the principal human streptococcal pathogen . Unlike many previously described bacteriocins of Gram-positive bacteria, dysgalacticin is a heat-labile 21.5 kDa anionic protein that kills its target without inducing lysis. The N-terminal amino acid sequence of dysgalacticin [Asn-Glu-Thr-Asn-Asn-Phe-Ala-Glu-Thr-Gln-Lys-Glu-Ile-Thr-Thr-Asn-(Asn)-Glu-Ala] has no known homologue in publicly available sequence databases. The dysgalacticin structural gene, , is located on the indigenous plasmid pW2580 of strain W2580 and encodes a 220 aa preprotein which is probably exported via a Sec-dependent transport system. Natural variants containing conservative amino acid substitutions were also detected by sequence analyses of elements from strains displaying W2580-like inhibitory profiles. Production of recombinant dysgalacticin by confirmed that this protein is solely responsible for the inhibitory activity exhibited by strain W2580. A combination of secondary structure prediction and reductive alkylation was employed to demonstrate that dysgalacticin has a novel structure containing a disulphide bond essential for its biological activity. Moreover, dysgalacticin displays similarity in predicted secondary structure (but not primary amino acid sequence or inhibitory spectrum) with another plasmid-encoded streptococcal bacteriocin, streptococcin A-M57 from , indicating that dysgalacticin represents a prototype of a new class of antimicrobial proteins.

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2006-07-01
2020-08-08
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References

  1. Altschul S. F, Madden T. L, Zhang J, Zhang Z, Miller W, Lipman D. J, Schäffer A. A. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  2. Balakrishnan M, Simmonds R. S, Carne A, Tagg J. R. 2000; Streptococcus mutans strain N produces a novel low molecular mass non-lantibiotic bacteriocin. FEMS Microbiol Lett183:165–169[CrossRef]
    [Google Scholar]
  3. Bendtsen J. D, Nielsen H, Brunak S, von Heijne G. 2004; Improved prediction of signal peptides – SignalP 3.0. J Mol Biol340:783–795[CrossRef]
    [Google Scholar]
  4. Beukes M, Beirbaum G, Sahl H. G, Hastings J. W. 2000; Purification and partial characterization of a murein hydrolase, millericin B, produced by Streptococcus milleri NMSCC 061. Appl Environ Microbiol66:23–28[CrossRef]
    [Google Scholar]
  5. Cotter P. D, Hill C, Ross R. P. 2005; Bacteriocins: developing innate immunity for food. Nat Rev Microbiol3:777–788[CrossRef]
    [Google Scholar]
  6. Chatterjee C, Paul M, Xie L, van der Donk W. A. 2005; Biosynthesis and mode of action of lantibiotics. Chem Rev105:633–684[CrossRef]
    [Google Scholar]
  7. del Solar G, Giraldo R, Ruiz-Echevarria M. J, Espinosa M, Diaz-Orejas R. 1998; Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev62:434–464
    [Google Scholar]
  8. Eijsink V. G, Axelsson L, Diep D. B, Havarstein L. S, Holo H, Nes I. F. 2002; Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie Van Leeuwenhoek81:639–654[CrossRef]
    [Google Scholar]
  9. Ennahar S, Sashihara T, Sonomoto K, Ishizaki A. 2000; Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol Rev24:85–106[CrossRef]
    [Google Scholar]
  10. Fimland G, Johnsen L, Dalhus B, Nissen-Meyer J. 2005; Pediocin-like antimicrobial peptides (class IIa bacteriocins) and their immunity proteins: biosynthesis, structure, and mode of action. J Pept Sci11:688–696[CrossRef]
    [Google Scholar]
  11. Gillor O, Kirkup B. C, Riley M. A. 2004; Colicins and microcins: the next generation antimicrobials. Adv Appl Microbiol54:129–146
    [Google Scholar]
  12. Hale J. D. F, Heng N. C. K, Jack R. W, Tagg J. R. 2005; Identification of nlmTE , the locus encoding the ABC transport system required for export of nonlantibiotic mutacins in Streptococcus mutans . J Bacteriol187:5036–5039[CrossRef]
    [Google Scholar]
  13. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580[CrossRef]
    [Google Scholar]
  14. Hardie J. M. 1986; Genus Streptococcus Rosenbach 1884, 22[sup]AL[/sup]. In Bergey's Manual of Systematic Bacteriologyvol. 2 pp 1043–1071 Edited by Sneath P. H. A., Mair N. S., Sharpe M. E., Holt J. G.. Baltimore: Williams & Wilkins;
    [Google Scholar]
  15. Heng N. C. K, Burtenshaw G. A, Jack R. W, Tagg J. R. 2004; Sequence analysis of pDN571, a plasmid encoding novel bacteriocin production in M-type 57 Streptococcus pyogenes . Plasmid52:225–229[CrossRef]
    [Google Scholar]
  16. Hubbard M. J, McHugh N. J. 1996; Mitochondrial ATP synthase F1-beta-subunit is a calcium-binding protein. FEBS Lett391:323–329[CrossRef]
    [Google Scholar]
  17. Jack R. W, Carne A, Metzger J, Stefanovic S, Sahl H. G, Jung G, Tagg J. 1994; Elucidation of the structure of SA-FF22, a lanthionine-containing antibacterial peptide produced by Streptococcus pyogenes strain FF22. Eur J Biochem220:455–462[CrossRef]
    [Google Scholar]
  18. Jack R. W, Tagg J. R, Ray B. 1995; Bacteriocins of gram-positive bacteria. Microbiol Rev59:171–200
    [Google Scholar]
  19. Jack R. W, Wan J, Gordon J, Harmark K, Davidson B. E, Hillier A. J, Wettenhall R. E, Hickey M. W, Coventry M. J. 1996; Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Carnobacterium piscicola JG126. Appl Environ Microbiol62:2897–2903
    [Google Scholar]
  20. Jack R. W, Bierbaum G, Sahl H.-G. 1998; Lantibiotics and Related Peptides Berlin: Springer;
    [Google Scholar]
  21. Joerger M. C, Klaenhammer T. R. 1986; Characterization and purification of helveticin J and evidence for a chromosomally determined bacteriocin produced by Lactobacillus helveticus 481. J Bacteriol167:439–446
    [Google Scholar]
  22. Khan S. A. 2005; Plasmid rolling-circle replication: highlights of two decades of research. Plasmid53:126–136[CrossRef]
    [Google Scholar]
  23. Kirkup B. C, Riley M. A. 2004; Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature428:412–414[CrossRef]
    [Google Scholar]
  24. Kramer M. G, Espinosa M, Misra T. K, Khan S. A. 1998; Lagging strand replication of rolling-circle plasmids: specific recognition of the ssoA -type origins in different gram-positive bacteria. Proc Natl Acad Sci U S A95:10505–10510[CrossRef]
    [Google Scholar]
  25. Lai A. C, Tran S, Simmonds R. S. 2002; Functional characterization of domains found within a lytic enzyme produced by Streptococcus equi subsp. zooepidemicus . FEMS Microbiol Lett215:133–138[CrossRef]
    [Google Scholar]
  26. McGuffin L. J, Bryson K, Jones D. T. 2000; The PSIPRED protein structure prediction server. Bioinformatics16:404–405[CrossRef]
    [Google Scholar]
  27. Moscoso M, Espinosa M, del Solar G. 1995; In vitro recognition of the replication origin of pLS1 and of plasmids of the pLS1 family by the RepB initiator protein. J Bacteriol177:7041–7049
    [Google Scholar]
  28. Navarre W. W, Schneewind O. 1999; Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev63:174–229
    [Google Scholar]
  29. Papagianni M. 2003; Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol Adv21:465–499[CrossRef]
    [Google Scholar]
  30. Paulsen I. T, Banerjei L, Myers G. S.29 other authors 2003; Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis . Science299:2071–2074[CrossRef]
    [Google Scholar]
  31. Pollastri G, Przybylski D, Rost B, Baldi P. 2002; Improving the prediction of protein secondary structure in three and eight classes using recurrent neural networks and profiles. Proteins47:228–235[CrossRef]
    [Google Scholar]
  32. Qi F, Chen P, Caufield P. W. 2001; The group I strain of Streptococcus mutans , UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl Environ Microbiol67:15–21[CrossRef]
    [Google Scholar]
  33. Ragland N, Tagg J. 1990; Applications of bacteriocin-like inhibitory substance (BLIS) typing in a longitudinal study of the oral carriage of beta-haemolytic streptococci by a group of Dunedin schoolchildren. Zentralbl Bakteriol274:100–108[CrossRef]
    [Google Scholar]
  34. Riley M. A, Gordon D. M. 1999; The ecological role of bacteriocins in bacterial competition. Trends Microbiol7:129–133[CrossRef]
    [Google Scholar]
  35. Riley M. A, Wertz J. E. 2002; Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol56:117–137[CrossRef]
    [Google Scholar]
  36. Ross K. F, Ronson C. W, Tagg J. R. 1993; Isolation and characterization of the lantibiotic salivaricin A and its structural gene salA from Streptococcus salivarius 20P3. Appl Environ Microbiol59:2014–2021
    [Google Scholar]
  37. Rost B. 1996; phd: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol266:525–539
    [Google Scholar]
  38. Rost B, Yachdav G, Liu J. 2004; The PredictProtein server. Nucleic Acids Res32:W321–W326[CrossRef]
    [Google Scholar]
  39. Sahl H.-G, Bierbaum G. 1998; Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from gram-positive bacteria. Annu Rev Microbiol52:41–79[CrossRef]
    [Google Scholar]
  40. Sambrook J, Russell D. W. 2001; Molecular Cloning: a Laboratory Manual, 3rd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  41. Schnell N, Entian K. D, Schneider U, Gotz F, Zahner H, Kellner R, Jung G. 1988; Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature333:276–278[CrossRef]
    [Google Scholar]
  42. Simmonds R. S, Pearson L, Kennedy R. C, Tagg J. R. 1996; Mode of action of a lysostaphin-like bacteriolytic agent produced by Streptococcus zooepidemicus 4881. Appl Environ Microbiol62:4536–4541
    [Google Scholar]
  43. Simmonds R. S, Simpson W. J, Tagg J. R. 1997; Cloning and sequence analysis of zooA , a Streptococcus zooepidemicus gene encoding a bacteriocin-like inhibitory substance having a domain structure similar to that of lysostaphin. Gene189:255–261[CrossRef]
    [Google Scholar]
  44. Solow B. T, Somkuti G. A. 2000; Comparison of low-molecular-weight heat stress proteins encoded on plasmids in different strains of Streptococcus thermophilus . Curr Microbiol41:177–181[CrossRef]
    [Google Scholar]
  45. Tagg J. R, Bannister L. V. 1979; “Fingerprinting” beta-haemolytic streptococci by their production of and sensitivity to bacteriocin-like inhibitors. J Med Microbiol12:397–411[CrossRef]
    [Google Scholar]
  46. Tagg J. R, Wannamaker L. W. 1976; Genetic basis of streptococcin A-FF22 production. Antimicrob Agents Chemother10:299–306[CrossRef]
    [Google Scholar]
  47. Tagg J. R, Wong H. K. 1983; Inhibitor production by group G streptococci of human and of animal origin. J Med Microbiol16:409–415[CrossRef]
    [Google Scholar]
  48. Takamatsu D, Osaki M, Sekizaki T. 2000; Sequence analysis of a small cryptic plasmid isolated from Streptococcus suis serotype 2. Curr Microbiol40:61–66[CrossRef]
    [Google Scholar]
  49. Tauch A, Bischoff N, Puhler A, Kalinowski J. 2004; Comparative genomics identified two conserved DNA modules in a corynebacterial plasmid family present in clinical isolates of the opportunistic human pathogen Corynebacterium jeikeium . Plasmid52:102–118[CrossRef]
    [Google Scholar]
  50. Tjalsma H, Antelmann H, Jongbloed J. D.11 other authors 2004; Proteomics of protein secretion by Bacillus subtilis : separating the “secrets” of the secretome. Microbiol Mol Biol Rev68:207–233[CrossRef]
    [Google Scholar]
  51. Turgeon N, Moineau S. 2000; Isolation and characterization of a Streptococcus thermophilus plasmid closely related to the pMV158 family. Plasmid45:171–183
    [Google Scholar]
  52. van Roosmalen M. L, Geukens N, Jongbloed J. D, Tjalsma H, Dubois J. Y, Bron S, van Dijl J. M, Anné J. 2004; Type I signal peptidases of Gram-positive bacteria. Biochim Biophys Acta 1694;279–297[CrossRef]
    [Google Scholar]
  53. Vullo A, Frasconi P. 2004; Disulfide connectivity prediction using recursive neural networks and evolutionary information. Bioinformatics20:653–659[CrossRef]
    [Google Scholar]
  54. Wescombe P. A, Tagg J. R. 2003; Purification and characterization of streptin, a type A1 lantibiotic produced by Streptococcus pyogenes . Appl Environ Microbiol69:2737–2747[CrossRef]
    [Google Scholar]
  55. Wilson K. H, Blitchington R. B, Greene R. C. 1990; Amplification of bacterial 16S ribosomal DNA with polymerase chain reaction. J Clin Microbiol28:1942–1946
    [Google Scholar]
  56. Wong H. K. 1981; Inhibition of group A streptococci by bacteriocins MSc thesis University of Otago;
    [Google Scholar]
  57. Wong H. K, Tagg J. R, Hynes W. L. 1981; Bacteriocin-like inhibitors of group A streptococci produced by group F and group G streptococci. Proc Univ Otago Med Sch59:105–106
    [Google Scholar]
  58. Xu F, Pearce L. E, Yu P.-L. 1991; Construction of a family of lactococcal vectors for gene cloning and translational fusions. FEMS Microbiol Lett77:55–60[CrossRef]
    [Google Scholar]
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