Concerted Spatio-Temporal Dynamics of Imported DNA and ComE DNA Uptake Protein during Gonococcal Transformation

PLoS Pathogens

Volumn 10, Issue 4, 2014, Pages

  Gangel, Heike ^a   Hepp, Christof ^a   Müller, Stephanie ^a   Oldewurtel, Enno R ^a   Aas, Finn Erik ^b   Koomey, Michael ^b   Maier, Berenike ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; GENOMIC DNA; PROTEIN COME; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; COME PROTEIN, NEISSERIA GONORRHOEAE;

ARTICLE; BACTERIUM COLONY; BACTERIUM TRANSFORMATION; CYTOPLASM; FLUORESCENCE; FLUORESCENCE MICROSCOPY; GENE DOSAGE; GENETIC TRANSFORMATION; GONORRHEA; MOLECULAR DYNAMICS; NEISSERIA GONORRHOEAE; NEISSERIA SICCA; NICK END LABELING; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; ACTIVE TRANSPORT; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; DNA, BACTERIAL; DNA-BINDING PROTEINS; NEISSERIA GONORRHOEAE; PERIPLASM; TRANSFORMATION, BACTERIAL;

EID: 84901378420     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004043     Document Type: Article

References (46)

1. Chen I, Dubnau D, (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2: 241-249.
2. Baltrus DA, (2013) Exploring the costs of horizontal gene transfer. Trends in ecology & evolution 28: 489-495.
3. Frye SA, Nilsen M, Tonjum T, Ambur OH, (2013) Dialects of the DNA uptake sequence in Neisseriaceae. PLoS genetics 9: e1003458.
4. Maier B (2012) Competence and transformation. In: Graumann PL, editor. Bacillus, Cellular and molecular biology. Norfolk: Caister Academic Press.
5. Kidane D, Ayora S, Sweasy JB, Graumann PL, Alonso JC, (2012) The cell pole: the site of cross talk between the DNA uptake and genetic recombination machinery. Critical reviews in biochemistry and molecular biology 47: 531-555.
6. Laurenceau R, Pehau-Arnaudet G, Baconnais S, Gault J, Malosse C, et al. (2013) A type IV pilus mediates DNA binding during natural transformation in Streptococcus pneumoniae. PLoS pathogens 9: e1003473.
7. Aas FE, Wolfgang M, Frye S, Dunham S, Lovold C, et al. (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.
8. Long CD, Tobiason DM, Lazio MP, Kline KA, Seifert HS, (2003) Low-level pilin expression allows for substantial DNA transformation competence in Neisseria gonorrhoeae. Infection and immunity 71: 6279-6291.
9. Winther-Larsen HC, Wolfgang MC, van Putten JP, Roos N, Aas FE, et al. (2007) Pseudomonas aeruginosa Type IV pilus expression in Neisseria gonorrhoeae: effects of pilin subunit composition on function and organelle dynamics. Journal of bacteriology 189: 6676-6685.
10. Salomonsson E, Forsberg A, Roos N, Holz C, Maier B, et al. (2009) Functional analyses of pilin-like proteins from Francisella tularensis: complementation of type IV pilus phenotypes in Neisseria gonorrhoeae. Microbiology 155: 2546-2559.
11. Aas FE, Lovold C, Koomey M, (2002) 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. Mol Microbiol 46: 1441-1450.
12. Goodman SD, Scocca JJ, (1988) Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc Natl Acad Sci U S A 85: 6982-6986.
13. Cehovin A, Simpson PJ, McDowell MA, Brown DR, Noschese R, et al. (2013) Specific DNA recognition mediated by a type IV pilin. Proceedings of the National Academy of Sciences of the United States of America 110: 3065-3070.
14. Drake SL, Koomey M, (1995) The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Molecular microbiology 18: 975-986.
15. Assalkhou R, Balasingham S, Collins RF, Frye SA, Davidsen T, et al. (2007) The outer membrane secretin PilQ from Neisseria meningitidis binds DNA. Microbiology 153: 1593-1603.
16. Chen I, Gotschlich EC, (2001) ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J Bacteriol 183: 3160-3168.
17. Facius D, Fussenegger M, Meyer TF, (1996) Sequential action of factors involved in natural competence for transformation of Neisseria gonorrhoeae. FEMS Microbiol Lett 137: 159-164.
18. Fussenegger M, Kahrs AF, Facius D, Meyer TF, (1996) Tetrapac (tpc), a novel genotype of Neisseria gonorrhoeae affecting epithelial cell invasion, natural transformation competence and cell separation. Molecular microbiology 19: 1357-1372.
19. Facius D, Meyer TF, (1993) A novel determinant (comA) essential for natural transformation competence in Neisseria gonorrhoeae and the effect of a comA defect on pilin variation. Mol Microbiol 10: 699-712.
20. Kidane D, Graumann PL, (2005) Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 122: 73-84.
21. Attaiech L, Olivier A, Mortier-Barriere I, Soulet AL, Granadel C, et al. (2011) Role of the single-stranded DNA-binding protein SsbB in pneumococcal transformation: maintenance of a reservoir for genetic plasticity. PLoS genetics 7: e1002156.
22. Chaussee MS, Hill SA, (1998) Formation of single-stranded DNA during DNA transformation of Neisseria gonorrhoeae. Journal of bacteriology 180: 5117-5122.
23. Maier B, Chen I, Dubnau D, Sheetz MP, (2004) DNA transport into Bacillus subtilis requires proton motive force to generate large molecular forces. Nat Struct Mol Biol 11: 643-649.
24. Stingl K, Muller S, Scheidgen-Kleyboldt G, Clausen M, Maier B, (2010) Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc Natl Acad Sci U S A 107: 1184-1189.
25. Allemand JF, Maier B, Smith DE, (2012) Molecular motors for DNA translocation in prokaryotes. Current opinion in biotechnology 23: 503-509.
26. Allemand JF, Maier B, (2009) Bacterial translocation motors investigated by single molecule techniques. FEMS Microbiol Rev 33: 593-610.
27. Kruger NJ, Stingl K, (2011) Two steps away from novelty-principles of bacterial DNA uptake. Molecular microbiology 80: 860-867.
28. Hahn J, Maier B, Haijema BJ, Sheetz M, Dubnau D, (2005) Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 122: 59-71.
29. Kaufenstein M, van der Laan M, Graumann PL, (2011) The three-layered DNA uptake machinery at the cell pole in competent Bacillus subtilis cells is a stable complex. Journal of bacteriology 193: 1633-1642.
30. Kramer N, Hahn J, Dubnau D, (2007) Multiple interactions among the competence proteins of Bacillus subtilis. Mol Microbiol 65: 454-464.
31. Provvedi R, Dubnau D, (1999) ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Molecular microbiology 31: 271-280.
32. Berge MJ, Kamgoue A, Martin B, Polard P, Campo N, et al. (2013) Midcell Recruitment of the DNA Uptake and Virulence Nuclease, EndA, for Pneumococcal Transformation. PLoS pathogens 9: e1003596.
33. Maier B, Radler JO, (2000) DNA on fluid membranes: A model polymer in two dimensions. Macromolecules 33: 7185-7194.
34. Hwang H, Kim H, Myong S, (2011) Protein induced fluorescence enhancement as a single molecule assay with short distance sensitivity. Proceedings of the National Academy of Sciences of the United States of America 108: 7414-7418.
35. Suckow G, Seitz P, Blokesch M, (2011) Quorum sensing contributes to natural transformation of Vibrio cholerae in a species-specific manner. Journal of bacteriology 193: 4914-4924.
36. Seitz P, Modarres HP, Borgeaud S, Bulushev RD, Steinbock LJ, Radenovic A, Dal Peraro M, Blokesch M, (2014) ComEA is essential for the transfer of external DNA into the periplasm of naturally transformable Vibrio cholerae. PLoS genetics 10: e1004066.
37. Berry JL, Phelan MM, Collins RF, Adomavicius T, Tonjum T, et al. (2012) Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS pathogens 8: e1002923.
38. Holz C, Opitz D, Greune L, Kurre R, Koomey M, et al. (2010) Multiple pilus motors cooperate for persistent bacterial movement in two dimensions. Physical review letters 104: 178104.
39. Seitz P, Blokesch M, (2013) DNA-uptake machinery of naturally competent Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America 110: 17987-17992.
40. Kahn ME, Barany F, Smith HO, (1983) Transformasomes: specialized membranous structures that protect DNA during Haemophilus transformation. Proceedings of the National Academy of Sciences of the United States of America 80: 6927-6931.
41. Barouki R, Smith HO, (1985) Reexamination of phenotypic defects in rec-1 and rec-2 mutants of Haemophilus influenzae Rd. Journal of bacteriology 163: 629-634.
42. Lang E, Haugen K, Fleckenstein B, Homberset H, Frye SA, et al. (2009) Identification of neisserial DNA binding components. Microbiology 155: 852-862.
43. Steichen CT, Cho C, Shao JQ, Apicella MA, (2011) The Neisseria gonorrhoeae biofilm matrix contains DNA, and an endogenous nuclease controls its incorporation. Infection and immunity 79: 1504-1511.
44. Winther-Larsen HC, Hegge FT, Wolfgang M, Hayes SF, van Putten JP, et al. (2001) Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proceedings of the National Academy of Sciences of the United States of America 98: 15276-15281.
45. Wolfgang M, van Putten JP, Hayes SF, Dorward D, Koomey M, (2000) Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. Embo J 19: 6408-6418.
46. Aas FE, Winther-Larsen HC, Wolfgang M, Frye S, Lovold C, et al. (2007) Substitutions in the N-terminal alpha helical spine of Neisseria gonorrhoeae pilin affect Type IV pilus assembly, dynamics and associated functions. Molecular microbiology 63: 69-85.