Home LiteratureArticle Details
PMID: 12620853 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The genes coding for enterocin EJ97 production by Enterococcus faecalis EJ97 are located on a conjugative plasmid.

Applied and environmental microbiology ·Vol. 69 ·No. 3 ·2003-03-00 ·Pages 1633-41

Sánchez-Hidalgo M, Maqueda M, Gálvez A, Abriouel H, Valdivia E, Martínez-Bueno M

Abstract

Enterococcus faecalis EJ97 produces a cationic bacteriocin (enterocin EJ97) of low molecular mass (5,327.7 Da). The complete amino acid sequence of enterocin EJ97 was elucidated after automated microsequencing of oligopeptides generated by endoproteinase GluC digestion and cyanogen bromide treatment. Transfer of the 60-kb conjugative plasmid pEJ97 from the bacteriocinogenic strain E. faecalis EJ97 to E. faecalis OG1X conferred bacteriocin production and resistance on the recipient. The genetic determinants of enterocin EJ97 were located in an 11.3-kb EcoRI-BglII DNA fragment of pEJ97. This region was cloned and sequenced. It contains the ej97A structural gene plus three open reading frames (ORFs) (ej97B, ej97C, and ej97D) and three putative ORFs transcribed in the opposite direction (orfA, orfB, and orfC). The gene ej97A translated as a 44-amino-acid residue mature protein lacking a leader peptide with no homology to other bacteriocins described so far. The product of ej97B (Ej97B) shows strong homology in its C-terminal domain to the superfamily of bacterial ATP-binding cassette transporters. The products of ej97C (Ej97C) and ej97D (Ej97D) could be proteins with 71 and 64 residues, respectively, of unknown functions and with no significant similarity to known proteins. There are two additional ORFs (ORF1 and ORF6) flanking the ej97 module, which have been identified as a transposon-like structure (tnp). ORF1 shows similarities to transposase of the Lactococcus lactis element ISS1 and is up to 50% identical to IS1216. This is flanked by two 18-bp inverted repeats (IRs) that are almost identical to those of ISS1 and IS1216. ORF6 (resEJ97) shows strong homology to the resolvase of plasmid pAM373 and up to 40 to 50% homology with the recombinase of several multiresistant plasmids and transposons from Staphylococcus aureus and E. faecalis. These data suggest that EJ97 could represent a new class of bacteriocins with a novel secretion mechanism and that the whole structure could be a composite transposon. Furthermore, two additional gene clusters were found: one cluster is probably related to the region responsible for the replication of plasmid pEJ97, and the second cluster is related to the sex pheromone response. These regions showed a high homology to the corresponding regions of the conjugative plasmids pAM373, pPD1, and pAD1 of E. faecalis, suggesting that they have a common origin.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/genetics,metabolism Bacteriocins/biosynthesis,genetics Base Sequence Conjugation, Genetic Enterococcus faecalis/genetics,metabolism Molecular Sequence Data Multigene Family Open Reading Frames/genetics Plasmids/genetics Sequence Analysis, DNA Transformation, Bacterial
Chemicals
Bacterial Proteins Bacteriocins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Sánchez-Hidalgo Marina
Departamento de Microbiología, Facultad de Ciencias, Universidad de Granada, Fuentenueva s/n, 18071-Granada, Spain.
Maqueda Mercedes
Gálvez Antonio
Abriouel Hikmate
Valdivia Eva
Martínez-Bueno Manuel
References (56)
56 references, click to expand
  1. Bacteriocins: safe, natural antimicrobials for food preservation.
    Int J Food Microbiol. 2001 Dec 4;71(1):1-20 PMID: 11764886
  2. The gene encoding the low-affinity penicillin-binding protein 3r in Enterococcus hirae S185R is borne on a plasmid carrying other antibiotic resistance determinants.
    Antimicrob Agents Chemother. 1998 Mar;42(3):534-9 PMID: 9517928
  3. Determination of the gene sequence and the molecular structure of the enterococcal peptide antibiotic AS-48.
    J Bacteriol. 1994 Oct;176(20):6334-9 PMID: 7929005
  4. Identification of a new insertion element, similar to gram-negative IS26, on the lactose plasmid of Streptococcus lactis ML3.
    J Bacteriol. 1987 Dec;169(12):5481-8 PMID: 2824436
  5. Distribution of the IS elements ISS1 and IS904 in lactococci.
    FEMS Microbiol Lett. 1991 May 15;64(2-3):311-7 PMID: 1653170
  6. Characterization of a mosaic ISS1 element and evidence for the recent horizontal transfer of two different types of ISS1 between Streptococcus thermophilus and Lactococcus lactis.
    Gene. 1996 Oct 31;178(1-2):15-23 PMID: 8921885
  7. IS257 from Staphylococcus aureus: member of an insertion sequence superfamily prevalent among gram-positive and gram-negative bacteria.
    Gene. 1989;76(2):195-205 PMID: 2546857
  8. Developing applications for lactococcal bacteriocins.
    Antonie Van Leeuwenhoek. 1999 Jul-Nov;76(1-4):337-46 PMID: 10532388
  9. The bacterial ParA-ParB partitioning proteins.
    J Biotechnol. 2001 Sep 13;91(1):1-34 PMID: 11522360
  10. Cloning and characterization of a region of the Enterococcus faecalis conjugative plasmid, pCF10, encoding a sex pheromone-binding function.
    J Bacteriol. 1993 Aug;175(16):5253-9 PMID: 8349565
  11. In vivo genetic systems in lactic acid bacteria.
    FEMS Microbiol Rev. 1990 Sep;7(1-2):43-60 PMID: 2176796
  12. Ribosomally synthesized antibacterial peptides in Gram positive bacteria.
    Curr Drug Targets. 2002 Apr;3(2):107-22 PMID: 11958295
  13. Biochemical and genetic characterization of the two-peptide bacteriocin enterocin 1071 produced by Enterococcus faecalis FAIR-E 309.
    Appl Environ Microbiol. 2002 May;68(5):2550-4 PMID: 11976133
  14. Antilisterial activity of peptide AS-48 and study of changes induced in the cell envelope properties of an AS-48-adapted strain of Listeria monocytogenes.
    Appl Environ Microbiol. 1999 Feb;65(2):618-25 PMID: 9925591
  15. Characterization of a region of the Enterococcus faecalis plasmid pAM beta 1 which enhances the segregational stability of pAM beta 1-derived cloning vectors in Bacillus subtilis.
    Plasmid. 1991 Nov;26(3):209-21 PMID: 1661428
  16. Molecular mechanism of peptide-specific pheromone signaling in Enterococcus faecalis: functions of pheromone receptor TraA and pheromone-binding protein TraC encoded by plasmid pPD1.
    J Bacteriol. 1998 Feb;180(3):449-56 PMID: 9457843
  17. Regulation of the pAD1 sex pheromone response of Enterococcus faecalis by direct interaction between the cAD1 peptide mating signal and the negatively regulating, DNA-binding TraA protein.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6430-5 PMID: 9600983
  18. Analysis of the gene cluster involved in production and immunity of the peptide antibiotic AS-48 in Enterococcus faecalis.
    Mol Microbiol. 1998 Jan;27(2):347-58 PMID: 9484890
  19. Enterococci from foods.
    FEMS Microbiol Rev. 2002 Jun;26(2):163-71 PMID: 12069881
  20. Enterococcus faecalis conjugative plasmid pAM373: complete nucleotide sequence and genetic analyses of sex pheromone response.
    Mol Microbiol. 2000 Sep;37(6):1327-41 PMID: 10998166
  21. Inhibition of bacterial growth, enterotoxin production, and spore outgrowth in strains of Bacillus cereus by bacteriocin AS-48.
    Appl Environ Microbiol. 2002 Mar;68(3):1473-7 PMID: 11872505
  22. Characterization of insertion sequence IS946, an Iso-ISS1 element, isolated from the conjugative lactococcal plasmid pTR2030.
    J Bacteriol. 1990 Aug;172(8):4151-60 PMID: 2165471
  23. Characterization of the lacticin 481 operon: the Lactococcus lactis genes lctF, lctE, and lctG encode a putative ABC transporter involved in bacteriocin immunity.
    Appl Environ Microbiol. 1997 Nov;63(11):4252-60 PMID: 9361411
  24. Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster.
    Appl Environ Microbiol. 2000 Jun;66(6):2565-71 PMID: 10831439
  25. Complete nucleotide sequence of pSK41: evolution of staphylococcal conjugative multiresistance plasmids.
    J Bacteriol. 1998 Sep;180(17):4350-9 PMID: 9721269
  26. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403.
    Genome Res. 2001 May;11(5):731-53 PMID: 11337471
  27. Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins.
    J Bacteriol. 1998 Apr;180(8):1988-94 PMID: 9555877
  28. Characterization of a plasmid involved with cointegrate formation and lactose metabolism in Lactococcus lactis subsp. lactis OZS1.
    Arch Microbiol. 1990;154(6):560-5 PMID: 2177590
  29. Simple and rapid method for isolating large plasmid DNA from lactic streptococci.
    Appl Environ Microbiol. 1983 Sep;46(3):549-52 PMID: 6416164
  30. Cloning and genetic analysis of the UV resistance determinant (uvr) encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pAD1.
    J Bacteriol. 1997 Dec;179(23):7468-75 PMID: 9393713
  31. Purification of sex pheromones specific for pMB1 and pMB2 plasmids of Enterococcus faecalis S-48.
    Can J Microbiol. 1995 Jul;41(7):629-32 PMID: 7641145
  32. Bacteriocins of gram-positive bacteria.
    Microbiol Rev. 1995 Jun;59(2):171-200 PMID: 7603408
  33. Characterisation of sin, a potential recombinase-encoding gene from Staphylococcus aureus.
    Gene. 1994 Apr 8;141(1):109-14 PMID: 8163161
  34. Biosynthesis of bacteriocins in lactic acid bacteria.
    Antonie Van Leeuwenhoek. 1996 Oct;70(2-4):113-28 PMID: 8879403
  35. ABC transporters: bacterial exporters.
    Microbiol Rev. 1993 Dec;57(4):995-1017 PMID: 8302219
  36. Comparison of lantibiotic gene clusters and encoded proteins.
    Antonie Van Leeuwenhoek. 1996 Feb;69(2):171-84 PMID: 8775977
  37. A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31.
    J Bacteriol. 1996 Jun;178(12):3508-16 PMID: 8655548
  38. Nonlantibiotic antibacterial peptides from lactic acid bacteria.
    Nat Prod Rep. 2000 Aug;17(4):323-35 PMID: 11014335
  39. Isolation and characterization of enterocin EJ97, a bacteriocin produced by Enterococcus faecalis EJ97.
    Arch Microbiol. 1998 Dec;171(1):59-65 PMID: 9871020
  40. Cloning and genetic organization of the bacteriocin 31 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pYI17.
    J Bacteriol. 1996 Jun;178(12):3585-93 PMID: 8655558
  41. Characterization of the traC determinant of the Enterococcus faecalis hemolysin-bacteriocin plasmid pAD1: binding of sex pheromone.
    J Bacteriol. 1993 Aug;175(16):5260-4 PMID: 8349566
  42. ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains.
    FEMS Microbiol Rev. 1998 Apr;22(1):1-20 PMID: 9640644
  43. Lactococcin 972, a bacteriocin that inhibits septum formation in lactococci.
    Microbiology. 2000 Apr;146 ( Pt 4):949-55 PMID: 10784053
  44. Class IIa bacteriocins from lactic acid bacteria: antibacterial activity and food preservation.
    J Biosci Bioeng. 1999;87(6):705-16 PMID: 16232543
  45. Bacteriocins: mechanism of membrane insertion and pore formation.
    Antonie Van Leeuwenhoek. 1999 Jul-Nov;76(1-4):185-98 PMID: 10532378
  46. Genetics of bacteriocins produced by lactic acid bacteria.
    FEMS Microbiol Rev. 1993 Sep;12(1-3):39-85 PMID: 8398217
  47. Cloning and characterization of a region of Enterococcus faecalis plasmid pPD1 encoding pheromone inhibitor (ipd), pheromone sensitivity (traC), and pheromone shutdown (traB) genes.
    J Bacteriol. 1995 Oct;177(19):5567-73 PMID: 7559344
  48. Genetic structure of the Enterococcus faecalis plasmid pAD1-encoded cytolytic toxin system and its relationship to lantibiotic determinants.
    J Bacteriol. 1994 Dec;176(23):7335-44 PMID: 7961506
  49. Genes involved in self-protection against the lantibiotic subtilin produced by Bacillus subtilis ATCC 6633.
    Appl Environ Microbiol. 1994 Aug;60(8):2793-801 PMID: 8085823
  50. The specific genes for lantibiotic mutacin II biosynthesis in Streptococcus mutans T8 are clustered and can be transferred en bloc.
    Appl Environ Microbiol. 1999 Mar;65(3):1356-60 PMID: 10049909
  51. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  52. Characterization and cloning of the genes encoding enterocin 1071A and enterocin 1071B, two antimicrobial peptides produced by Enterococcus faecalis BFE 1071.
    Appl Environ Microbiol. 2000 Apr;66(4):1298-304 PMID: 10742203
  53. Biochemical and genetic evidence that Enterococcus faecium L50 produces enterocins L50A and L50B, the sec-dependent enterocin P, and a novel bacteriocin secreted without an N-terminal extension termed enterocin Q.
    J Bacteriol. 2000 Dec;182(23):6806-14 PMID: 11073927
  54. Identification, characterization, and nucleotide sequence of a region of Enterococcus faecalis pheromone-responsive plasmid pAD1 capable of autonomous replication.
    J Bacteriol. 1993 Apr;175(7):1900-9 PMID: 8384618
  55. Class IIa bacteriocins: biosynthesis, structure and activity.
    FEMS Microbiol Rev. 2000 Jan;24(1):85-106 PMID: 10640600
  56. Molecular rearrangement of lactose plasmid DNA associated with high-frequency transfer and cell aggregation in Lactococcus lactis 712.
    Mol Microbiol. 1992 Nov;6(21):3213-23 PMID: 1453959
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
Published
2003-03-00
Pages
1633-41
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC150074
Subset
IM
Databases
GENBANK
AJ490170
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com