1887

Abstract

is commonly found in the environment and in association with various bovine body sites and is a major cause of bovine mastitis. Moreover, is known to produce a variety of bacteriocin-like inhibitory substances, antimicrobial agents that generally inhibit closely related bacterial species. In this respect, strain 42 has previously been shown to produce a novel nisin variant named nisin U. This paper reports that, in addition to nisin U, strain 42 produces a second bacteriocin that induces the lysis of metabolically active, susceptible target bacteria and which has therefore been named uberolysin. Isolation of the native active antimicrobial agent revealed that uberolysin is a 7048 Da peptide that is refractory to sequence analysis by Edman degradation. Transposon mutagenesis was used to generate a uberolysin-negative mutant of 42 and sequencing of DNA flanking the insertion site revealed, in addition to the structural gene (), several open reading frames likely to be involved in post-translational modification, transport and producer self-protection (immunity), and possibly in regulation of the biosynthetic gene cluster. In addition, a pair of direct repeats that may be involved in bacteriocin acquisition were identified; indeed, could be identified in 18 % of tested strains. Enzymic hydrolysis of uberolysin was used to confirm that does indeed encode the precursor of uberolysin, that an unusually short leader sequence of only six amino acids is cleaved during processing of the mature peptide and that uberolysin is post-translationally covalently modified to form a head-to-tail monocycle. Thus, uberolysin is a unique cyclic bacteriocin, belonging to the same family of bacteriocins as enterocin AS-48 and circularin A.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/005967-0
2007-05-01
2020-04-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/5/1619.html?itemId=/content/journal/micro/10.1099/mic.0.2006/005967-0&mimeType=html&fmt=ahah

References

  1. Abriouel H., Lucas R., Ben Omar N., Valdivia E., Maqueda M., Martinez-Canamero M., Galvez A.. 2005; Enterocin AS-48RJ: a variant of enterocin AS-48 chromosomally encoded by Enterococcus faecium RJ16 isolated from food. Syst Appl Microbiol28:383–397[CrossRef]
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schaffer 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 Res25:3389–3402[CrossRef]
    [Google Scholar]
  3. Berry C., O'Neil S., Ben-Dov E., Jones A. F., Murphy L., Quail M. A., Holden M. T. G., Harris D., Zaritsky A., Parkhill J.. 2002; Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol68:5082–5095[CrossRef]
    [Google Scholar]
  4. Blowey R., Edmondson P.. 1995; Mastitis Control in Dairy Herds: an Illustrated and Practical Guide Ipswich, UK: Farming Press Books;
    [Google Scholar]
  5. Buddle B. M., Tagg J. R., Ralston M. J.. 1988; Use of an inhibitor typing scheme to study the epidemiology of Streptococcus uberis mastitis. N Z Vet J36:115–119[CrossRef]
    [Google Scholar]
  6. Cornett J. B., Redman B. E., Shockman G. D.. 1978; Autolytic defective mutant of Streptococcus faecalis. J Bacteriol133:631–640
    [Google Scholar]
  7. Cotter P. D., Hill C., Ross R. P.. 2005; Bacteriocins: developing innate immunity for food. Nat Rev Microbiol3:777–788[CrossRef]
    [Google Scholar]
  8. Craik D. J., Daly N. L., Saska I., Trabi M., Rosengren K. J.. 2003; Structures of naturally occurring circular proteins from bacteria. J Bacteriol185:4011–4021[CrossRef]
    [Google Scholar]
  9. Cullen G. A.. 1966; The ecology of Streptococcus uberis. Br Vet J122:333–339
    [Google Scholar]
  10. Cullen G. A.. 1969; Streptococcus uberis : a review. Vet Bull39:155–165
    [Google Scholar]
  11. de Greeff A., Buys H., Smith H. E., van Alphen L.. 2002; Response regulator important in pathogenesis of Streptococcus suis serotype 2. Microb Pathog33:185–192[CrossRef]
    [Google Scholar]
  12. Diaz M., Valdivia E., Martinez-Bueno M., Fernandez M., Soler-Gonzalez A. S., Ramirez-Rodrigo H., Maqueda M.. 2003; Characterization of a new operon, as-48EFGH, from the as-48 gene cluster involved in immunity to enterocin AS-48. Appl Environ Microbiol69:1229–1236[CrossRef]
    [Google Scholar]
  13. Diep D. B., Nes I. F.. 2002; Ribosomally synthesized antibacterial peptides in Gram positive bacteria. Curr Drug Targets3:107–122[CrossRef]
    [Google Scholar]
  14. Folli C., Ramazzina I., Arcidiaco P., Stoppini M., Berni R.. 2003; Purification of bacteriocin AS-48 from an Enterococcus faecium strain and analysis of the gene cluster involved in its production. FEMS Microbiol Lett221:143–149[CrossRef]
    [Google Scholar]
  15. Galvez A., Maqueda M., Valdivia E., Quesada A., Montoya E.. 1986; Characterization and partial purification of a broad spectrum antibiotic AS-48 produced by Streptococcus faecalis. Can J Microbiol32:765–771[CrossRef]
    [Google Scholar]
  16. Galvez A., Valdivia E., Martinez-Bueno M., Maqueda M.. 1990; Induction of autolysis in Enterococcus faecalis S-47 by peptide AS-48. J Appl Bacteriol69:406–413[CrossRef]
    [Google Scholar]
  17. Hancock L., Perego M.. 2002; Two-component signal transduction in Enterococcus faecalis. J Bacteriol184:5819–5825[CrossRef]
    [Google Scholar]
  18. Haydel S. E., Clark-Curtiss J. E.. 2004; Global expression analysis of two-component system regulator genes during Mycobacterium tuberculosis growth in human macrophages. FEMS Microbiol Lett236:341–347[CrossRef]
    [Google Scholar]
  19. Heng N. C. K., Tagg J. R.. 2006; What's in a name? Class distinction for bacteriocins. Nat Rev Microbiol4: available online athttp://www.nature.com/nrmicro/journal/v4/n2/full/nrmicro1273-c1.html
    [Google Scholar]
  20. Hickey R. M., Twomey D. P., Ross R. P., Hill C.. 2003; Potential of the enterocin regulatory system to control expression of heterologous genes in Enterococcus. J Appl Microbiol95:390–397[CrossRef]
    [Google Scholar]
  21. Hutchings M. I., Hoskisson P. A., Chandra G., Buttner M. J.. 2004; Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2. Microbiology150:2795–2806[CrossRef]
    [Google Scholar]
  22. Jack R., Bierbaum G., Sahl H.-G.. 1998; Lantibiotics and Related Peptides Heidelberg: Springer;
    [Google Scholar]
  23. Jayarao B. M., Oliver S. P., Tagg J. R., Matthews K. R.. 1991; Genotypic and phenotypic analysis of Streptococcus uberis isolated from bovine mammary secretions. Epidemiol Infect107:543–555[CrossRef]
    [Google Scholar]
  24. Joosten H. M., Nunez M., Devreese B., Van Beeumen J., Marugg J. D.. 1996; Purification and characterization of enterocin 4, a bacteriocin produced by Enterococcus faecalis INIA 4. Appl Environ Microbiol62:4220–4223
    [Google Scholar]
  25. Joosten H. M., Rodriguez E., Nunez M.. 1997; PCR detection of sequences similar to the AS-48 structural gene in bacteriocin-producing enterococci. Lett Appl Microbiol24:40–42[CrossRef]
    [Google Scholar]
  26. Kabuki T., Saito T., Kawai Y., Uemura J., Itoh T.. 1997; Production, purification and characterization of reutericin 6, a bacteriocin with lytic activity produced by Lactobacillus reuteri LA6. Int J Food Microbiol34:145–156[CrossRef]
    [Google Scholar]
  27. Kalmokoff M. L., Teather R. M.. 1997; Isolation and characterization of a bacteriocin (Butyrivibriocin AR10) from the ruminal anaerobe Butyrivibrio fibrisolvens AR10: evidence in support of the widespread occurrence of bacteriocin-like activity among ruminal isolates of B. fibrisolvens. Appl Environ Microbiol63:394–402
    [Google Scholar]
  28. Kalmokoff M. L., Cyr T. D., Hefford M. A., Whitford M. F., Teather R. M.. 2003; Butyrivibriocin AR10, a new cyclic bacteriocin produced by the ruminal anaerobe Butyrivibrio fibrisolvens AR10: characterization of the gene and peptide. Can J Microbiol49:763–773[CrossRef]
    [Google Scholar]
  29. Kawai Y., Saito T., Kitazawa H., Itoh T.. 1998a; Gassericin A; an uncommon cyclic bacteriocin produced by Lactobacillus gasseri LA39 linked at N- and C-terminal ends. Biosci Biotechnol Biochem62:2438–2440[CrossRef]
    [Google Scholar]
  30. Kawai Y., Saito T., Suzuki M., Itoh T.. 1998b; Sequence analysis by cloning of the structural gene of gassericin A, a hydrophobic bacteriocin produced by Lactobacillus gasseri LA39. Biosci Biotechnol Biochem62:887–892[CrossRef]
    [Google Scholar]
  31. Kawai Y., Ishii Y., Uemura K., Kitazawa H., Saito T., Itoh T.. 2001; Lactobacillus reuteri LA6 and Lactobacillus gasseri LA39 isolated from the faeces of the same human infant produce identical cyclic bacteriocin. Food Microbiol18:407–415[CrossRef]
    [Google Scholar]
  32. Kawai Y., Arakawa K., Itoh A., Saitoh B., Ishii Y., Nishimura J., Kitazawa H., Itoh T., Saito T.. 2003; Heterologous expression of gassericin A, a bacteriocin produced by Lactobacillus gasseri LA39. Anim Sci J74:45–51[CrossRef]
    [Google Scholar]
  33. Kawai Y., Ishii Y., Arakawa K., Uemura K., Saitoh B., Nishimura J., Kitazawa H., Yamazaki Y., Tateno Y.. & other authors (2004a). Structural and functional differences in two cyclic bacteriocins with the same sequences produced by lactobacilli. Appl Environ Microbiol70:2906–2911[CrossRef]
    [Google Scholar]
  34. Kawai Y., Kemperman R., Kok J., Saito T.. 2004b; The circular bacteriocins gassericin A and circularin A. Curr Protein Pept Sci5:393–398[CrossRef]
    [Google Scholar]
  35. Kawulka K. E., Sprules T., Diaper C. M., Whittal R. M., McKay R. T., Mercier P., Zuber P., Vederas J. C.. 2004; Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to alpha-carbon cross-links: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry43:3385–3395[CrossRef]
    [Google Scholar]
  36. Kemperman R., Jonker M., Nauta A., Kuipers O. P., Kok J.. 2003a; Functional analysis of the gene cluster involved in production of the bacteriocin circularin A by Clostridium beijerinckii ATCC 25752. Appl Environ Microbiol69:5839–5848[CrossRef]
    [Google Scholar]
  37. Kemperman R., Kuipers A., Karsens H., Nauta A., Kuipers O., Kok J.. 2003b; Identification and characterization of two novel clostridial bacteriocins, circularin A and closticin 574. Appl Environ Microbiol69:1589–1597[CrossRef]
    [Google Scholar]
  38. Khan I. U., Hassan A. A., Abdulmawjood A., Lammler C., Wolter W., Zschock M.. 2003; Identification and epidemiological characterization of Streptococcus uberis isolated from bovine mastitis using conventional and molecular methods. J Vet Sci4:213–224
    [Google Scholar]
  39. Klaenhammer T. R.. 1993; Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev12:39–85[CrossRef]
    [Google Scholar]
  40. Klesse N. A.. 2001; Purification and partial characterisation of a novel bacteriocin produced by Streptococcus uberis strain ATCC 27958 MSc thesis University of Otago; Dunedin:
    [Google Scholar]
  41. Knutsen E., Ween O., Håvarstein L. S.. 2004; Two separate quorum-sensing systems upregulate transcription of the same ABC transporter in Streptococcus pneumoniae. J Bacteriol186:3078–3085[CrossRef]
    [Google Scholar]
  42. Leigh J. A.. 1999; Streptococcus uberis : a permanent barrier to the control of bovine mastitis?. Vet J157:225–238[CrossRef]
    [Google Scholar]
  43. Maisnier-Patin S., Forni E., Richard J.. 1996; Purification, partial characterisation and mode of action of enterococcin EFS2, an antilisterial bacteriocin produced by a strain of Enterococcus faecalis isolated from a cheese. Int J Food Microbiol30:255–270[CrossRef]
    [Google Scholar]
  44. Maqueda M., Galvez A., Bueno M. M., Sanchez-Barrena M. J., Gonzalez C., Albert A., Rico M., Valdivia E.. 2004; Peptide AS-48: prototype of a new class of cyclic bacteriocins. Curr Protein Pept Sci5:399–416[CrossRef]
    [Google Scholar]
  45. Martinez-Bueno M., Galvez A., Valdivia E., Maqueda M.. 1990; A transferable plasmid associated with AS-48 production in Enterococcus faecalis. J Bacteriol172:2817–2818
    [Google Scholar]
  46. Martinez-Bueno M., Maqueda M., Galvez A., Samyn B., Van Beeumen J., Coyette J., Valdivia E.. 1994; Determination of the gene sequence and the molecular structure of the enterococcal peptide antibiotic AS-48. J Bacteriol176:6334–6339
    [Google Scholar]
  47. Martinez-Bueno M., Valdivia E., Galvez A., Coyette J., Maqueda M.. 1998; Analysis of the gene cluster involved in production and immunity of the peptide antibiotic AS-48 in Enterococcus faecalis. Mol Microbiol27:347–358[CrossRef]
    [Google Scholar]
  48. Morgan S., Ross R. P., Hill C.. 1995; Bacteriolytic activity caused by the presence of a novel lactococcal plasmid encoding lactococcins A. B, and M. Appl Environ Microbiol61:2995–3001
    [Google Scholar]
  49. Nes I. F., Tagg J. R.. 1996; Novel lantibiotics and their pre-peptides. Antonie van Leeuwenhoek69:89–97[CrossRef]
    [Google Scholar]
  50. Nida K., Cleary P. P.. 1983; Insertional inactivation of streptolysin S expression in Streptococcus pyogenes. J Bacteriol155:1156–1161
    [Google Scholar]
  51. Nobusato A., Uchiyama I., Ohashi S., Kobayashi I.. 2000; Insertion with long target duplication: a mechanism for gene mobility suggested from comparison of two related bacterial genomes. Gene259:99–108[CrossRef]
    [Google Scholar]
  52. Osaki M., Takamatsu D., Shimoji Y., Sekizaki T.. 2002; Characterization of Streptococcus suis genes encoding proteins homologous to sortase of gram-positive bacteria. J Bacteriol184:971–982[CrossRef]
    [Google Scholar]
  53. 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]
  54. Sambrook J., Russell D. W.. 2001; Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  55. Shevchenko A., Jensen O. N., Podtelejnikov A. V., Sagliocco F., Wilm M., Vorm O., Mortensen P., Boucherie H., Mann M.. 1996; Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci U S A93:14440–14445[CrossRef]
    [Google Scholar]
  56. Tagg J. R., Bannister L. V.. 1979; “Fingerprinting” beta-haemolytic streptococci by their production of and sensitivity to bacteriocine-like inhibitors. J Med Microbiol12:397–411[CrossRef]
    [Google Scholar]
  57. Tagg J. R., Vugler L. G.. 1986; An inhibitor typing scheme for Streptococcus uberis. J Dairy Res53:451–456[CrossRef]
    [Google Scholar]
  58. Tagg J. R., Dajani A. S., Wannamaker L. W.. 1976; Bacteriocins of gram-positive bacteria. Bacteriol Rev40:722–756
    [Google Scholar]
  59. Tettelin H., Masignani V., Cieslewicz M. J., Donati C., Medini D., Ward N. L., Angiuoli S. V., Crabtree J., Jones A. L.. other authors 2005; Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae : implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A102:13950–13955[CrossRef]
    [Google Scholar]
  60. Tomita H., Fujimoto S., Tanimoto K., Ike Y.. 1997; Cloning and genetic and sequence analyses of the bacteriocin 21 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pPD1. J Bacteriol179:7843–7855
    [Google Scholar]
  61. Ulijasz A. T., Andes D. R., Glasner J. D., Weisblum B.. 2004; Regulation of iron transport in Streptococcus pneumoniae by RitR, an orphan response regulator. J Bacteriol186:8123–8136[CrossRef]
    [Google Scholar]
  62. 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]
  63. Wirawan R. E., Klesse N. A., Jack R. W., Tagg J. R.. 2006; Molecular and genetic characterization of a novel nisin variant produced by Streptococcus uberis. Appl Environ Microbiol72:1148–1156[CrossRef]
    [Google Scholar]
  64. Xu Q., Stickel S., Roberts R. J., Blaser M. J., Morgan R. D.. 2000; Purification of the novel endonuclease, Hpy188I, and cloning of its restriction-modification genes reveal evidence of its horizontal transfer to the Helicobacter pylori genome. J Biol Chem275:17086–17093[CrossRef]
    [Google Scholar]
  65. Zheng G., Hehn R., Zuber P.. 2000; Mutational analysis of the sbo-alb locus of Bacillus subtilis : identification of genes required for subtilosin production and immunity. J Bacteriol182:3266–3273[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/005967-0
Loading
/content/journal/micro/10.1099/mic.0.2006/005967-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error