Development and use of an efficient system for random mariner transposon mutagenesis to identify novel genetic determinants of biofilm formation in the core Enterococcus faecalis genome

Applied and Environmental Microbiology

Volumn 74, Issue 11, 2008, Pages 3377-3386

  Kristich, Christopher J ^a,b   Nguyen, Vy T ^a   Le, Thinh ^a   Barnes, Aaron M T ^a   Grindle, Suzanne ^a   Dunny, Gary M ^a,c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c MMC196 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILTERS; CHROMOSOMES; COMPUTER NETWORKS; GENES; INFORMATION SYSTEMS; MUTAGENESIS;

AMERICAN SOCIETY; BIO FILMS; BIOFILM FORMATIONS; COMPLEMENTATION ANALYSIS; COMPREHENSIVE ANALYSIS; ENTEROCOCCUS FAECALIS; FUNCTIONAL GENOMIC ANALYSIS; GASTROINTESTINAL TRACT (GIT); GENERAL (CO); GENETIC ANALYSES; GENETIC ELEMENTS; GRAM-POSITIVE COMMENSAL BACTERIUM; IMPROVED SYSTEM; INSERTION MUTANTS; MARINER TRANSPOSON; SINGLE COPY; TRANSPOSABLE ELEMENTS; TRANSPOSON MUTAGENESIS; TRANSPOSON SYSTEM; WILD-TYPE (WT);

BIOFILMS;

BACTERIUM; BIOFILM; CHROMOSOME; GENETIC ANALYSIS; GENOME; MUTATION; PATHOGEN;

ARTICLE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIUM MUTANT; BIOFILM; CHROMOSOME; ENTEROCOCCUS FAECALIS; FUNCTIONAL GENOMICS; GENE IDENTIFICATION; GENE INSERTION; GENETIC COMPLEMENTATION; GENETIC SCREENING; MUTAGENESIS; NONHUMAN; TRANSPOSON; WILD TYPE;

BIOFILMS; CHROMOSOMES, BACTERIAL; DNA TRANSPOSABLE ELEMENTS; ENTEROCOCCUS FAECALIS; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; GENOME; MICROSCOPY, ELECTRON, SCANNING; MUTAGENESIS, INSERTIONAL;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; POSIBACTERIA;

EID: 44949129965     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02665-07     Document Type: Article

References (55)

1. Ashour, J., and M. K. Hondalus. 2003. Phenotypic mutants of the intracellular actinomycete Rhodococcus equi created by in vivo Himar1 transposon mutagenesis. J. Bacteriol. 185:2644-2652.
2. Bae, T., A. K. Banger, A. Wallace, E. M. Glass, F. Aslund, O. Schneewind, and D. M. Missiakas. 2004. Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc. Natl. Acad. Sci. USA 101:12312-12317.
3. Bae, T., B. Kozlowicz, and G. M. Dunny. 2002. Two targets in pCF10 DNA for PrgX binding: their role in production of Qa and prgX mRNA and in regulation of pheromone-inducible conjugation. J. Mol. Biol. 315:995-1007.
4. Baldassarri, L., R. Cecchini, L. Bertuccini, M. G. Ammendolia, F. Iosi, C. R. Arciola, L. Montanaro, R. Di Rosa, G. Gherardi, G. Dicuonzo, G. Orefici, and R. Creti. 2001. Enterococcus sp. produces slime and survives in rat peritoneal macrophages. Med. Microbiol. Immunol. (Berlin) 190:113-120.
5. Bayles, K. 2007. The biological role of death and lysis in biofilm development. Nat. Rev. Microbiol. 5:721-726.
6. Beloin, C., J. Valle, P. Latour-Lambert, P. Faure, M. Kzreminski, D. Balestrino, J. A. Haagensen, S. Molin, G. Prensier, B. Arbeille, and J. M. Ghigo. 2004. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51:659-674.
7. Bourgogne, A., K. V. Singh, K. A. Fox, K. J. Pflughoeft, B. E. Murray, and D. A. Garsin. 2007. EbpR is important for biofilm formation by activating expression of the endocarditis and biofilm-associated pilus operon (ebpABC) of Enterococcus faecalis OG1RF. J. Bacteriol. 189:6490-6493.
8. Bryan, E. M., T. Bae, M. Kleerebezem, and G. M. Dunny. 2000. Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44:183-190.
9. Clewell, D. B., P. K. Tomich, M. C. Gawron-Burke, A. E. Franke, Y. Yagi, and F. Y. An. 1982. Mapping of Streptococcus faecalis plasmids pAD1 and pAD2 and studies relating to transposition of Tn917. J. Bacteriol. 152:1220-1230.
10. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
11. Donlan, R. M. 2001. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis. 33:1387-1392.
12. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
13. Dubern, J. F., E. L. Lagendijk, B. J. Lugtenberg, and G. V. Bloemberg. 2005. The heat shock genes dnaK, dnaJ, and grpE are involved in regulation of putisolvin biosynthesis in Pseudomonas putida PCL1445. J. Bacteriol. 187: 5967-5976.
14. Dunny, G. M., B. L. Brown, and D. B. Clewell. 1978. Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc. Natl. Acad. Sci. USA 75:3479-3483.
15. Erlandsen, S. L., C. J. Kristich, G. M. Dunny, and C. L. Wells. 2004. High-resolution visualization of the microbial glycocalyx with low-voltage scanning electron microscopy: dependence on cationic dyes. J. Histochem. Cytochem. 52:1427.
16. Foley, I., and P. Gilbert. 1997. In vitro studies of the activity of glycopeptide combinations against Enterococcus faecalis biofilms. J. Antimicrob. Chemother. 40:667-672.
17. Garsin, D. A., J. Urbach, J. C. Huguet-Tapia, J. E. Peters, and F. M. Ausubel. 2004. Construction of an Enterococcus faecalis Tn917-mediated-gene-disruption library offers insight into Tn917 insertion patterns. J. Bacteriol. 186:7280-7289.
18. Gawron-Burke, C., and D. B. Clewell. 1982. A transposon in Streptococcus faecalis with fertility properties. Nature 300:281-284.
19. Hancock, L. E., and M. Perego. 2004. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186:5629-5639.
20. Hava, D. L., and A. Camilli. 2002. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45:1389-1406.
21. Kak, V., and J. W. Chow. 2002. Acquired antibiotic resistances in enterococci, p. 355-383. In M. S. Gilmore, D. B. Clewell, P. Courvalin, G. M. Dunny, B. E. Murray, and L. B. Rice (ed.), The enterococci: pathogenesis, molecular biology, and antibiotic resistance. ASM Press, Washington, DC.
22. Kemp, K. D., K. V. Singh, S. R. Nallapareddy, and B. E. Murray. 2007. Relative contributions of Enterococcus faecalis OG1RF sortase-encoding genes, srtA and bps (srtC), to biofilm formation and a murine model of urinary tract infection. Infect. Immun. 75:5399-5404.
23. Kristich, C. J., J. R. Chandler, and G. M. Dunny. 2007. Development of a host-genotype-independent counterselectable marker and a high-frequency conjugative delivery system and their use in genetic analysis of Enterococcus faecalis. Plasmid 57:131-144.
24. Kristich, C. J., Y. H. Li, D. G. Cvitkovitch, and G. M. Dunny. 2004. Esp-independent biofilm formation by Enterococcus faecalis. J. Bacteriol. 186: 154-163.
25. Kristich, C. J., D. A. Manias, and G. M. Dunny. 2005. Development of a method for markerless genetic exchange in Enterococcus faecalis and its use in construction of a srtA mutant. Appl. Environ. Microbiol. 71:5837-5849.
26. Lampe, D. J., B. J. Akerley, E. J. Rubin, J. J. Mekalanos, and H. M. Robertson. 1999. Hyperactive transposase mutants of the Himar1 mariner transposon. Proc. Natl. Acad. Sci. USA 96:11428-11433.
27. Lampe, D. J., M. E. Churchill, and H. M. Robertson. 1996. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J. 15:5470-5479.
28. Lampe, D. J., T. E. Grant, and H. M. Robertson. 1998. Factors affecting transposition of the Himar1 mariner transposon in vitro. Genetics 149:179-187.
29. Le Breton, Y., N. P. Mohapatra, and W. G. Haldenwang. 2006. In vivo random mutagenesis of Bacillus subtilis by use of TnYLB-1, a mariner-based transposon. Appl. Environ. Microbiol. 72:327-333.
30. Leenhouts, K., G. Buist, A. Bolhuis, A. ten Berge, J. Kiel, I. Mierau, M. Dabrowska, G. Venema, and J. Kok. 1996. A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol. Gen. Genet. 253:217-224.
31. Lemos, J. A., Y. Luzardo, and R. A. Burne. 2007. Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans. J. Bacteriol. 189:1582-1588.
32. Liu, Z. M., A. M. Tucker, L. O. Driskell, and D. O. Wood. 2007. mariner- based transposon mutagenesis of Rickettsia prowazekii. Appl. Environ. Microbiol. 73:6644-6649.
33. Maier, T. M., R. Pechous, M. Casey, T. C. Zahrt, and D. W. Frank. 2006. In vivo Himar1-based transposon mutagenesis of Francisella tularensis. Appl. Environ. Microbiol. 72:1878-1885.
34. Marrie, T. J., and J. W. Costerton. 1984. Morphology of bacterial attachment to cardiac pacemaker leads and power packs. J. Clin. Microbiol. 19:911-914.
35. Mohamed, J. A., W. Huang, S. R. Nallapareddy, F. Teng, and B. E. Murray. 2004. Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 72:3658-3663.
36. Mohamed, J. A., F. Teng, S. R. Nallapareddy, and B. E. Murray. 2006. Pleiotrophic effects of 2 Enterococcus faecalis sagA-like genes, salA and salB, which encode proteins that are antigenic during human infection, on biofilm formation and binding to collagen type I and fibronectin. J. Infect. Dis. 193:231-240.
37. Nallapareddy, S. R., K. V. Singh, J. Sillanpaa, D. A. Garsin, M. Hook, S. L. Erlandsen, and B. E. Murray. 2006. Endocarditis and biofilm-associated pili of Enterococcus faecalis. J. Clin. Investig. 116:2799-2807.
38. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
39. Richards, M. J., J. R. Edwards, D. H. Culver, and R. P. Gaynes. 2000. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect. Control Hosp. Epidemiol. 21:510-515.
40. Rubin, E. J., B. J. Akerley, V. N. Novik, D. J. Lampe, R. N. Husson, and J. J. Mekalanos. 1999. In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc. Natl. Acad. Sci. USA 96:1645-1650.
41. Sandoe, J. A., I. R. Witherden, J. H. Cove, J. Heritage, and M. H. Wilcox. 2003. Correlation between enterococcal biofilm formation in vitro and medical-device-related infection potential in vivo. J. Med. Microbiol. 52:547-550.
42. Schaberg, D. R., D. H. Culver, and R. P. Gaynes. 1991. Major trends in the microbial etiology of nosocomial infection. Am. J. Med. 91:72S-75S.
43. Scott, J. R., F. Bringet, D. Marra, G. Van Alstine, and C. K. Rudy. 1994. Conjugative transposition of Tn976: preferred targets and evidence for conjugative transfer of a single strand and for a double-stranded circular intermediate. Mol. Microbiol. 11:1099-1108.
44. Scott, J. R., and G. G. Churchward. 1995. Conjugative transposition. Annu. Rev. Microbiol. 49:367-397.
45. Shankar, N., A. S. Baghdayan, and M. S. Gilmore. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417:746-750.
46. Stewart, P. E., J. Hoff, E. Fischer, J. G. Krum, and P. A. Rosa. 2004. Genome-wide transposon mutagenesis of Borrelia burgdorferi for identification of phenotypic mutants. Appl. Environ. Microbiol. 70:5973-5979.
47. Stoodley, P., K. Sauer, D. G. Davies, and J. W. Costerton. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56:187-209.
48. Tam, C., E. M. Glass, D. M. Anderson, and D. Missiakas. 2006. Transposon mutagenesis of Bacillus anthracis strain Sterne using Bursa aurealis. Plasmid 56:74-77.
49. Tannock, G. W., and G. Cook. 2002. Enterococci as members of the intestinal microflora of humans, p. 101-132. In M. S. Gilmore, D. B. Clewell, P. Courvalin, G. M. Dunny, B. E. Murray, and L. B. Rice (ed.), The enterococci: pathogenesis, molecular biology, and antibiotic resistance. ASM Press, Washington, DC.
50. Tendolkar, P. M., A. S. Baghdayan, and N. Shankar. 2006. Putative surface proteins encoded within a novel transferable locus confer a high-biofilm phenotype to Enterococcus faecalis. J. Bacteriol. 188:2063-2072.
51. Toledo-Arana, A., J. Valle, C. Solano, M. J. Arrizubieta, C. Cucarella, M. Lamata, B. Amorena, J. Leiva, J. R. Penades, and I. Lasa. 2001. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 67:4538-4545.
52. Waters, C. M., M. H. Antiporta, B. E. Murray, and G. M. Dunny. 2003. Role of the Enterococcus faecalis GelE protease in determination of cellular chain length, supernatant pheromone levels, and degradation of fibrin and misfolded surface proteins. J. Bacteriol. 185:3613-3623.
53. Wirth, R., F. An, and D. B. Clewell. 1987. Highly efficient cloning system for Streptococcus faecalis protoplast transformation, shuttle vectors, and applications, p. 25-27. In J. J. Ferretti and R. I. Curtiss (ed.), Streptococcal genetics. ASM Press, Washington, DC.
54. Youderian, P., N. Burke, D. J. White, and P. L. Hartzell. 2003. Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol. Microbiol. 49:555-570.
55. Zhang, J. K., M. A. Pritchett, D. J. Lampe, H. M. Robertson, and W. W. Metcalf. 2000. In vivo transposon mutagenesis of the methanogenic archaeon Methanosarcina acetivorans C2A using a modified version of the insect mariner-family transposable element Himar1. Proc. Natl. Acad. Sci. USA 97:9665-9670.