1887

Abstract

4185 was previously shown to produce at least two bacteriocins. One of them is encoded by pRJ101. To detect the bacteriocin-encoding gene cluster, an ~9160 kb region of pRJ101 was sequenced. analyses identified 10 genes (, , , , , , , , and ) that might be involved in the production of a novel cyclic bacteriocin named aureocyclicin 4185. The organization of these genes was quite similar to that of the gene cluster responsible for carnocyclin A production and immunity. Four putative proteins encoded by these genes (AclT, AclC, AclD and AclA) also exhibited similarity to proteins encoded by cyclic bacteriocin gene clusters. Mutants derived from insertion of Tn into , , and were affected in bacteriocin production and growth. AclX is a 205 aa putative protein not encoded by the gene clusters of other cyclic bacteriocins. AclX exhibits 50 % similarity to a permease and has five putative membrane-spanning domains. Transcription analyses suggested that is part of the aureocyclicin 4185 gene cluster, encoding a protein required for bacteriocin production. The gene is the structural gene of aureocyclicin 4185, which shows 65 % similarity to garvicin ML. AclA is proposed to be cleaved off, generating a mature peptide with a predicted of 5607 Da (60 aa). By homology modelling, AclA presents four α-helices, like carnocyclin A. AclA could not be found at detectable levels in the culture supernatant of a strain carrying only pRJ101. To our knowledge, this is the first report of a cyclic bacteriocin gene cluster in the genus .

Funding
This study was supported by the:
  • CNPq
  • FAPERJ
  • CAPES
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.075689-0
2014-05-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/5/917.html?itemId=/content/journal/micro/10.1099/mic.0.075689-0&mimeType=html&fmt=ahah

References

  1. Bastos M. C. F., Bonaldo M. C., Penido E. G. ( 1980). Constitutive erythromycin resistance plasmid in Staphylococcus aureus. J Gen Microbiol 121:513–516[PubMed]
    [Google Scholar]
  2. Bastos M. C. F., Ceotto H., Coelho M. L. V., Nascimento J. S. ( 2009). Staphylococcal antimicrobial peptides: relevant properties and potential biotechnological applications. Curr Pharm Biotechnol 10:38–61 [View Article][PubMed]
    [Google Scholar]
  3. Bastos M. C. F., Coutinho B. G., Coelho M. L. V. ( 2010). Lysostaphin: a staphylococcal bacteriolysin with potential clinical applications. Pharmaceuticals (Ott) 3:1139–1161 [View Article]
    [Google Scholar]
  4. Bierbaum G., Sahl H.-G. ( 2009). Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 10:2–18 [View Article][PubMed]
    [Google Scholar]
  5. Borrero J., Brede D. A., Skaugen M., Diep D. B., Herranz C., Nes I. F., Cintas L. M., Hernández P. E. ( 2011). Characterization of garvicin ML, a novel circular bacteriocin produced by Lactococcus garvieae DCC43, isolated from mallard ducks (Anas platyrhynchos). Appl Environ Microbiol 77:369–373 [View Article][PubMed]
    [Google Scholar]
  6. Bullock W. O., Fernandez J. M., Short J. M. ( 1987). XL1-Blue: a high efficiency plasmid transformation recA Escherichia coli strain with beta-galactosidase selection. Biotechniques 5:376–378
    [Google Scholar]
  7. Ceotto H., Nascimento J. S., Brito M. A. V. P., Bastos M. C. F. ( 2009). Bacteriocin production by Staphylococcus aureus involved in bovine mastitis in Brazil. Res Microbiol 160:592–599 [View Article][PubMed]
    [Google Scholar]
  8. Ceotto H., Brede D., Salehian Z., Nascimento J. S., Fagundes P. C., Nes I. F., Bastos M. C. F. ( 2010). Aureocins 4185, bacteriocins produced by Staphylococcus aureus 4185: potential application in food preservation. Foodborne Pathog Dis 7:1255–1262 [View Article][PubMed]
    [Google Scholar]
  9. Coelho M. L. V., Ceotto H., Madureira D. J., Nes I. F., Bastos M. C. F. ( 2009). Mobilization functions of the bacteriocinogenic plasmid pRJ6 of Staphylococcus aureus. J Microbiol 47:327–336 [View Article][PubMed]
    [Google Scholar]
  10. Daly K. M., Upton M., Sandiford S. K., Draper L. A., Wescombe P. A., Jack R. W., O’Connor P. M., Rossney A., Götz F. & other authors ( 2010). Production of the Bsa lantibiotic by community-acquired Staphylococcus aureus strains. J Bacteriol 192:1131–1142 [View Article][PubMed]
    [Google Scholar]
  11. Davidson A. L., Maloney P. C. ( 2007). ABC transporters: how small machines do a big job. Trends Microbiol 15:448–455 [View Article][PubMed]
    [Google Scholar]
  12. Diaz M., Valdivia E., Martínez-Bueno M., Fernández M., Soler-González A. S., Ramírez-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 Microbiol 69:1229–1236 [View Article][PubMed]
    [Google Scholar]
  13. Giambiagi-Marval M., Mafra M. A., Penido E. G. C., Bastos M. C. F. ( 1990). Distinct groups of plasmids correlated with bacteriocin production in Staphylococcus aureus. J Gen Microbiol 136:1591–1599 [View Article][PubMed]
    [Google Scholar]
  14. Guex N., Peitsch M. C. ( 1997). swiss-model and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723 [View Article][PubMed]
    [Google Scholar]
  15. Heng N. C. K., Wescombe P. A., Burton J. P., Jack R. W., Tagg J. R. ( 2007). The diversity of bacteriocins in Gram-positive bacteria. Bacteriocins: Ecology and Evolution45–92 Riley M. A., Chavan M. A. New York: Springer; [View Article]
    [Google Scholar]
  16. 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 Microbiol 49:763–773 [View Article][PubMed]
    [Google Scholar]
  17. Kawai Y., Saito T., Suzuki M., Itoh T. ( 1998). Sequence analysis by cloning of the structural gene of gassericin A, a hydrophobic bacteriocin produced by Lactobacillus gasseri LA39. Biosci Biotechnol Biochem 62:887–892 [View Article][PubMed]
    [Google Scholar]
  18. Kawai Y., Kusnadi J., Kemperman R., Kok J., Ito Y., Endo M., Arakawa K., Uchida H., Nishimura J. & other authors ( 2009). DNA sequencing and homologous expression of a small peptide conferring immunity to gassericin A, a circular bacteriocin produced by Lactobacillus gasseri LA39. Appl Environ Microbiol 75:1324–1330 [View Article][PubMed]
    [Google Scholar]
  19. Kemperman R., Jonker M., Nauta A., Kuipers O. P., Kok J. ( 2003). Functional analysis of the gene cluster involved in production of the bacteriocin circularin A by Clostridium beijerinckii ATCC 25752. Appl Environ Microbiol 69:5839–5848 [View Article][PubMed]
    [Google Scholar]
  20. Kreiswirth B. N., Löfdahl S., Betley M. J., O’Reilly M., Schlievert P. M., Bergdoll M. S., Novick R. P. ( 1983). The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709–712 [View Article][PubMed]
    [Google Scholar]
  21. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M. ( 1993). procheck: a program to check the stereochemical quality of protein structures. J Appl Cryst 26:283–291 [View Article]
    [Google Scholar]
  22. Maqueda M., Sánchez-Hidalgo M., Fernández M., Montalbán-López M., Valdivia E., Martínez-Bueno M. ( 2008). Genetic features of circular bacteriocins produced by Gram-positive bacteria. FEMS Microbiol Rev 32:2–22 [View Article][PubMed]
    [Google Scholar]
  23. Martin-Visscher L. A., van Belkum M. J., Garneau-Tsodikova S., Whittal R. M., Zheng J., McMullen L. M., Vederas J. C. ( 2008). Isolation and characterization of carnocyclin A, a novel circular bacteriocin produced by Carnobacterium maltaromaticum UAL307. Appl Environ Microbiol 74:4756–4763 [View Article][PubMed]
    [Google Scholar]
  24. Martin-Visscher L. A., Gong X., Duszyk M., Vederas J. C. ( 2009). The three-dimensional structure of carnocyclin A reveals that many circular bacteriocins share a common structural motif. J Biol Chem 284:28674–28681 [View Article][PubMed]
    [Google Scholar]
  25. Martínez-Bueno M., Maqueda M., Gálvez 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 Bacteriol 176:6334–6339[PubMed]
    [Google Scholar]
  26. Martínez-Bueno M., Valdivia E., Gálvez 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 Microbiol 27:347–358 [View Article][PubMed]
    [Google Scholar]
  27. Masuda Y., Ono H., Kitagawa H., Ito H., Mu F., Sawa N., Zendo T., Sonomoto K. ( 2011). Identification and characterization of leucocyclicin Q, a novel cyclic bacteriocin produced by Leuconostoc mesenteroides TK41401. Appl Environ Microbiol 77:8164–8170 [View Article][PubMed]
    [Google Scholar]
  28. Nascimento J. S., Abrantes A., Giambiagi-deMarval M., Bastos M. C. F. ( 2004). Growth conditions required for bacteriocin production by strains of Staphylococcus aureus. World J Microbiol Biotechnol 20:941–947 [View Article]
    [Google Scholar]
  29. Nascimento J. S., Coelho M. L. V., Ceotto H., Potter A., Fleming L. R., Salehian Z., Nes I. F., Bastos M. C. F. ( 2012). Genes involved in immunity to and secretion of aureocin A53, an atypical class II bacteriocin produced by Staphylococcus aureus A53. J Bacteriol 194:875–883 [View Article][PubMed]
    [Google Scholar]
  30. Netz D. J. A., Sahl H.-G., Marcelino R., Nascimento J. S., Oliveira S. S., Soares M. B., Bastos M. C. F. ( 2001). Molecular characterisation of aureocin A70, a multi-peptide bacteriocin isolated from Staphylococcus aureus. J Mol Biol 311:939–949 [View Article][PubMed]
    [Google Scholar]
  31. Netz D. J. A., Pohl R., Beck-Sickinger A. G., Selmer T., Pierik A. J., Bastos M. C. F., Sahl H.-G. ( 2002). Biochemical characterisation and genetic analysis of aureocin A53, a new, atypical bacteriocin from Staphylococcus aureus. J Mol Biol 319:745–756 [View Article][PubMed]
    [Google Scholar]
  32. Nissen-Meyer J., Rogne P., Oppegård C., Haugen H. S., Kristiansen P. E. ( 2009). Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by gram-positive bacteria. Curr Pharm Biotechnol 10:19–37 [View Article][PubMed]
    [Google Scholar]
  33. Oliveira S. S., Nascimento J. S., Póvoa D. C., de Araújo S. A., Gamon M. R., Bastos M. C. F. ( 1998). Genetic analysis of the bacteriocin-encoding plasmids pRJ6 and pRJ9 of Staphylococcus aureus by transposon mutagenesis and cloning of genes involved in bacteriocin production. J Appl Microbiol 85:972–984 [View Article][PubMed]
    [Google Scholar]
  34. Perkins J. B., Youngman P. J. ( 1986). Construction and properties of Tn917-lac, a transposon derivative that mediates transcriptional gene fusions in Bacillus subtilis. Proc Natl Acad Sci U S A 83:140–144 [View Article][PubMed]
    [Google Scholar]
  35. Planchon S., Chambon C., Desvaux M., Chafsey I., Leroy S., Talon R., Hébraud M. ( 2007). Proteomic analysis of cell envelope from Staphylococcus xylosus C2a, a coagulase-negative staphylococcus. J Proteome Res 6:3566–3580 [View Article][PubMed]
    [Google Scholar]
  36. Sambrook J., Fritsch E. F., Maniatis T. ( 1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  37. Samyn B., Martinez-Bueno M., Devreese B., Maqueda M., Gálvez A., Valdivia E., Coyette J., Van Beeumen J. ( 1994). The cyclic structure of the enterococcal peptide antibiotic AS-48. FEBS Lett 352:87–90 [View Article][PubMed]
    [Google Scholar]
  38. Sandiford S., Upton M. ( 2012). Identification, characterization, and recombinant expression of epidermicin NI01, a novel unmodified bacteriocin produced by Staphylococcus epidermidis that displays potent activity against staphylococci. Antimicrob Agents Chemother 56:1539–1547 [View Article][PubMed]
    [Google Scholar]
  39. Sawa N., Zendo T., Kiyofuji J., Fujita K., Himeno K., Nakayama J., Sonomoto K. ( 2009). Identification and characterization of lactocyclicin Q, a novel cyclic bacteriocin produced by Lactococcus sp. strain QU 12. Appl Environ Microbiol 75:1552–1558 [View Article][PubMed]
    [Google Scholar]
  40. van Belkum M. J., Vederas J. C. ( 2012). The ABC transporter CclEFGH facilitates the production of the circular bacteriocin carnocyclin A. Probiotics Antimicrob Prot 4:273–278 [View Article]
    [Google Scholar]
  41. van Belkum M. J., Martin-Visscher L. A., Vederas J. C. ( 2010). Cloning and characterization of the gene cluster involved in the production of the circular bacteriocin carnocyclin A. Probiotics Antimicrob Prot 2:218–225 [View Article]
    [Google Scholar]
  42. van Belkum M. J., Martin-Visscher L. A., Vederas J. C. ( 2011). Structure and genetics of circular bacteriocins. Trends Microbiol 19:411–418 [View Article][PubMed]
    [Google Scholar]
  43. Wirawan R. E., Swanson K. M., Kleffmann T., Jack R. W., Tagg J. R. ( 2007). Uberolysin: a novel cyclic bacteriocin produced by Streptococcus uberis. Microbiology 153:1619–1630 [View Article][PubMed]
    [Google Scholar]
  44. Zheng G., Yan L. Z., Vederas J. C., Zuber P. ( 1999). Genes of the sbo-alb locus of Bacillus subtilis are required for production of the antilisterial bacteriocin subtilosin. J Bacteriol 181:7346–7355[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.075689-0
Loading
/content/journal/micro/10.1099/mic.0.075689-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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