Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits - PubMed (original) (raw)
Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits
Janet M Manson et al. Proc Natl Acad Sci U S A. 2010.
Abstract
The Enterococcus faecalis pathogenicity island (PAI) encodes known virulence traits and >100 additional genes with unknown roles in enterococcal biology. Phage-related integration and excision genes, and direct repeats flanking the island, suggest it moves as an integrative conjugative element (ICE). However, transfer was observed not to require these genes. Transfer only occurred from donors possessing a pheromone responsive-type of conjugative plasmid, and was invariably accompanied by transfer of flanking donor chromosome sequences. Deletion of plasmid transfer functions, including the cis-acting origin of transfer (oriT), abolished movement. In addition to demonstrating PAI movement by a mechanism involving plasmid integration, we observed transfer of a selectable marker placed virtually anywhere on the chromosome. Transfer of this selectable marker was observed to be accompanied by chromosome-chromosome transfer of vancomycin resistance, MLST markers, and capsule genes as well. Plasmid mobilization therefore appears to be a major mechanism for horizontal gene transfer in the evolution of antibiotic resistant E. faecalis strains capable of causing human infection.
Conflict of interest statement
The authors declare no conflict of interest.
Figures
Fig. 1.
E. faecalis pathogenicity island showing tetracycline resistance marker integration within the int gene (orf EF0479), the choline bile salt hydrolase cbh gene (orf EF0521), or distal orf EF0592 encoding a surface protein of unknown function. The location and direction of primer pairs (
Table S1
) used to amplify the left and right PAI junctions are indicated.
Fig. 2.
SfiI macrorestriction patterns of E. faecalis PAI transconjugants. Lane 1, lambda DNA ladder standard; lane 2, recipient strain OG1RF; lanes 3–14, transconjugant strains TC1, TC2, TC7, TC4, TC6, TC8, TC9, TC10, TC3, TC12, TC5, and TC11, respectively; lane 15, donor strain V583. PFGE pattern groupings are indicated below the gel. Plasmid pTEF2, 57.7 kb in size and present in 3 of the 12 transconjugants, is indicated by arrows.
Fig. 3.
Rate of transfer of tetracycline resistance from various points in the V583 chromosome. The relative location of tetracycline resistance marker insertions within the chromosome are indicated on the horizontal axis with scale shown above. Large regions of acquired/mobile DNA that occur naturally in the V583 donor chromosome are identified by small boxes along the lower horizontal axis (putative phage shown in light gray; other mobile elements such as the pathogenicity island, black).
Similar articles
- Intra- and interspecies genomic transfer of the Enterococcus faecalis pathogenicity island.
Laverde Gomez JA, Hendrickx AP, Willems RJ, Top J, Sava I, Huebner J, Witte W, Werner G. Laverde Gomez JA, et al. PLoS One. 2011 Apr 29;6(4):e16720. doi: 10.1371/journal.pone.0016720. PLoS One. 2011. PMID: 21559082 Free PMC article. - Horizontal transfer of virulence genes encoded on the Enterococcus faecalis pathogenicity island.
Coburn PS, Baghdayan AS, Dolan GT, Shankar N. Coburn PS, et al. Mol Microbiol. 2007 Jan;63(2):530-44. doi: 10.1111/j.1365-2958.2006.05520.x. Epub 2006 Dec 5. Mol Microbiol. 2007. PMID: 17163979 - Plasmid-Assisted Horizontal Transfer of a Large lsa(E)-Carrying Genomic Island in Enterococcus faecalis.
Shan X, Li XS, Schwarz S, Chen Y, Xu C, Du XD. Shan X, et al. Microbiol Spectr. 2022 Aug 31;10(4):e0015422. doi: 10.1128/spectrum.00154-22. Epub 2022 Jul 6. Microbiol Spectr. 2022. PMID: 35863017 Free PMC article. - Horizontal gene transfer and the genomics of enterococcal antibiotic resistance.
Palmer KL, Kos VN, Gilmore MS. Palmer KL, et al. Curr Opin Microbiol. 2010 Oct;13(5):632-9. doi: 10.1016/j.mib.2010.08.004. Epub 2010 Sep 15. Curr Opin Microbiol. 2010. PMID: 20837397 Free PMC article. Review. - Broad-host-range Inc18 plasmids: Occurrence, spread and transfer mechanisms.
Kohler V, Vaishampayan A, Grohmann E. Kohler V, et al. Plasmid. 2018 Sep;99:11-21. doi: 10.1016/j.plasmid.2018.06.001. Epub 2018 Jun 19. Plasmid. 2018. PMID: 29932966 Review.
Cited by
- H-NS is a bacterial transposon capture protein.
Cooper C, Legood S, Wheat RL, Forrest D, Sharma P, Haycocks JRJ, Grainger DC. Cooper C, et al. Nat Commun. 2024 Aug 20;15(1):7137. doi: 10.1038/s41467-024-51407-5. Nat Commun. 2024. PMID: 39164300 Free PMC article. - An enterococcal phage protein inhibits type IV restriction enzymes involved in antiphage defense.
Bullen NP, Johnson CN, Andersen SE, Arya G, Marotta SR, Lee YJ, Weigele PR, Whitney JC, Duerkop BA. Bullen NP, et al. Nat Commun. 2024 Aug 13;15(1):6955. doi: 10.1038/s41467-024-51346-1. Nat Commun. 2024. PMID: 39138193 Free PMC article. - The Impact of Enterococcus spp. in the Immunocompromised Host: A Comprehensive Review.
Sangiorgio G, Calvo M, Migliorisi G, Campanile F, Stefani S. Sangiorgio G, et al. Pathogens. 2024 May 15;13(5):409. doi: 10.3390/pathogens13050409. Pathogens. 2024. PMID: 38787261 Free PMC article. Review. - A metagenomics pipeline reveals insertion sequence-driven evolution of the microbiota.
Kirsch JM, Hryckowian AJ, Duerkop BA. Kirsch JM, et al. Cell Host Microbe. 2024 May 8;32(5):739-754.e4. doi: 10.1016/j.chom.2024.03.005. Epub 2024 Apr 1. Cell Host Microbe. 2024. PMID: 38565143 - Conserved signatures of the canine faecal microbiome are associated with metronidazole treatment and recovery.
Marshall-Jones ZV, Patel KV, Castillo-Fernandez J, Lonsdale ZN, Haydock R, Staunton R, Amos GCA, Watson P. Marshall-Jones ZV, et al. Sci Rep. 2024 Mar 4;14(1):5277. doi: 10.1038/s41598-024-51338-7. Sci Rep. 2024. PMID: 38438389 Free PMC article.
References
- Hunt CP. The emergence of enterococci as a cause of nosocomial infection. Br J Biomed Sci. 1998;55:149–156. - PubMed
- Sood S, Malhotra M, Das BK, Kapil A. Enterococcal infections & antimicrobial resistance. Indian J Med Res. 2008;128:111–121. - PubMed
- Paulsen IT, et al. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science. 2003;299:2071–2074. - PubMed
- Shankar N, Baghdayan AS, Gilmore MS. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature. 2002;417:746–750. - PubMed
- Quintiliani R, Jr, Courvalin P. Conjugal transfer of the vancomycin resistance determinant vanB between enterococci involves the movement of large genetic elements from chromosome to chromosome. FEMS Microbiol Lett. 1994;119:359–363. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- R01AI072360/AI/NIAID NIH HHS/United States
- R01 AI072360/AI/NIAID NIH HHS/United States
- P01 AI083214/AI/NIAID NIH HHS/United States
- R01 AI077782/AI/NIAID NIH HHS/United States
- P01AI083214/AI/NIAID NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources