An inhibitor of DNA binding and uptake events dictates the proficiency of genetic transformation in Neisseria gonorrhoeae: Mechanism of action and links to Type IV pilus expression

Molecular Microbiology

Volumn 46, Issue 5, 2002, Pages 1441-1450

  Aas, Finn Erik ^a,b,c   Løvold, Cecilia ^a,d   Koomey, Michael ^a,b,c  

^a UNIVERSITY OF OSLO   (Norway)

^b Institute of Pharmacy   (Norway)

^c Ctr for Molec Biol and Neurosci   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA; DNA BINDING PROTEIN; PILIN; PROTEIN COMP; PROTEIN TFP; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; COMP PROTEIN, BACILLUS SUBTILIS; MEMBRANE PROTEIN; PILV PROTEIN, BACTERIA; TRANSFERASE;

ANIMAL CELL; ARTICLE; BACTERIUM PILUS; BIOGENESIS; CELL SPECIFICITY; COMP GENE; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; DNA STRUCTURE; GENE ISOLATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC TRANSFORMATION; GONORRHEA; GRAM NEGATIVE BACTERIUM; INTERSPECIFIC HYBRIDIZATION; INTRASPECIFIC VARIATION; MOLECULAR INTERACTION; NEISSERIA GONORRHOEAE; NONHUMAN; PILE GENE; PILT GENE; PILV GENE; PRIORITY JOURNAL; PROKARYOTE; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SHEAR FLOW; SPECIES IDENTIFICATION; STRAIN IDENTIFICATION; AMINO ACID SEQUENCE; BACTERIUM TRANSFORMATION; CHEMISTRY; DRUG ANTAGONISM; FIMBRIA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; NEISSERIA; NEISSERIA GONORRHOEAE; PROKARYOTA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA, BACTERIAL; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; TRANSFERASES; TRANSFORMATION, BACTERIAL;

EID: 0042072799     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03265.x     Document Type: Article

References (31)

1. Aas, F.E., Wolfgang, M., Frye, S., Dunham, S., Løvold, C., and Koomey, M. (2002) Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to Type IV pilus expression. Mol Microbiol. 46: 749-760.
2. Chen, I., and Gotschlich, E.C. (2001) ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J Bacteriol 183: 3160-3168.
3. Danner, D.B., Deich, R.A., Sisco, K.L., and Smith, H.O. (1980) An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 11: 311-318.
4. Drake, S.L., and Koomey, M. (1995) The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol Microbiol 18: 975-986.
5. Dubnau, D. (1999) DNA uptake in bacteria. Annu Rev Microbiol 53: 217-244.
6. Elkins, C., Thomas, C.E., Seifert, H.S., and Spading, P.F. (1991) Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J Bacteriol 173: 3911-3913.
7. Freitag, N., Seifert, H.S., and Koomey, M. (1995) Characterization of the pilF - pilD pilus assembly locus of Neisseria gonorrhoeae. Mol Microbiol 16: 575-586.
8. Graupner, S., and Wackernagel, W. (2001) Pseudomonas stutzeri has two closely related pilA genes (type IV pilus structural proteins) with opposite influences on natural genetic transformation. J Bacteriol 183: 2359-2366.
9. Gunn, J.S., and Stein, D.C. (1996) Use of a non-selective transformation technique to construct a multiply restriction/modification-deficient mutant of Neisseria gonorrhoeae. Mol Gen Genet 251: 509-517.
10. Kong, L., Siranosian, K.J., Grossman, A.D., and Dubnau, D. (1993) Sequence and properties of mecA, a negative regulator of genetic competence in Bacillus subtilis. Mol Microbiol 9: 365-373.
11. Koomey, M., and Falkow, S. (1987) Cloning of the recA gene of Neisseria gonorrhoeae and construction of gonococcal RecA- mutants. J Bacteriol 169: 790-795.
12. Lacks, S.A., and Greenberg, B. (2001) Constitutive competence for genetic transformation in Streptococcus pneumoniae caused by mutation of a transmembrane histidine kinase. Mol Microbiol 42: 1035-1045.
13. Ma, C., and Redfield, R.J. (2000) Point mutations in a peptidoglycan biosynthesis gene cause competence induction in Haemophilus influenzae. J Bacteriol 182: 3323-3330.
14. Martin, B., Prudhomme, M., Alloing, G., Granadel, C., and Claverys, J.P. (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol Microbiol 38: 867-878.
15. Mattick, J.S. (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56: 289-314.
16. Park, H.S., Wolfgang, M., and Koomey, M. (2002) Modification of type IV pilus-associated epithelial cell adherence and multicellular behaviour by the PilU protein of Neisseria gonorrhoeae. Infect Immun 70: 3891-3903.
17. Rudel, T., Facius, D., Barten, R., Scheuerpflug, I., Nonnenmacher, E., and Meyer, T.F. (1995) Role of pili and the phase-variable PilC protein in natural competence for transformation of Neisseria gonorrhoeae. Proc Natl Acad Sci USA 92: 7986-7990.
18. Rudel, T., Facius, D., Barten, R., Scheuerpflug, I., Nonnenmacher, E., and Meyer, T.F. (1995) Role of pili and the phase-variable PilC protein in natural competence for transformation of Neisseria gonorrhoeae. Proc Natl Acad Sci USA 92: 7986-7990.
19. Seifert, H.S., Ajioka, R.S., Paruchuri, D., Heffron, F., and So, M. (1990) Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J Bacteriol 172: 40-46.
20. Sikorski, J., Teschner, N., and Wackernagel, W. (2002) Highly different levels of natural transformation are associated with genomic subgroups within a local population of Pseudomonas stutzeri from soil. Appl Environ Microbiol 68: 865-873.
21. Smith, J.M., Smith, N.H., O'Rourke, M., and Spratt, B.G. (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90: 4384-4388.
22. Stein, D.C., Danaher, R.J., and Cook, T.M. (1991) Characterization of a gyrB mutation responsible for low-level nalidixic acid resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 35: 622-626.
23. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
24. Tønjum, T., Freitag, N.E., Normark, E., and Koomey, M. (1995) Identification and characterization of pilG, a highly conserved pilus assembly gene in pathogenic Neisseria. Mol Microbiol 16: 451-464.
25. Turgay, K., Hahn, J., Burghoorn, J., and Dubnau, D. (1998) Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J 17: 6730-6738.
26. Ween, O., Teigen, S., Gaustad, P., Kilian, M., and Havarstein, L.S. (2002) Competence without a competence pheromone in a natural isolate of Streptococcus infantis. J Bacteriol 184: 3426-3432.
27. Winther-Larsen, H.C., Hegge, F.T., Wolfgang, M., Hayes, S.F., van Putten, J.P., and Koomey, M. (2001) Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 98: 15276-15281.
28. Wolfgang, M., Lauer, P., Park, H.S., Brossay, L., Hebert, J., and Koomey, M. (1998a) PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29: 321-330.
29. Wolfgang, M., Park, H.S., Hayes, S.F., van Putten, J.P., and Koomey, M. (1998b) Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc Natl Acad Sci USA 95: 14973-14978.
30. Wolfgang, M., van Putten, J.P.M., Hayes, S.F., and Koomey, M. (1999) The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol Microbiol 31: 1345-1357.
31. Wolfgang, M., van Putten, J.P.M., Hayes, S.F., Dorward, D., and Koomey, M. (2000) Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 19: 6408-6418.