A Type IV Pilus Mediates DNA Binding during Natural Transformation in

English version České info

Natural genetic transformation is widely distributed in bacteria and generally occurs during a genetically programmed differentiated state called competence. This process promotes genome plasticity and adaptability in Gram-negative and Gram-positive bacteria. Transformation requires the binding and internalization of exogenous DNA, the mechanisms of which are unclear. Here, we report the discovery of a transformation pilus at the surface of competent Streptococcus pneumoniae cells. This Type IV-like pilus, which is primarily composed of the ComGC pilin, is required for transformation. We provide evidence that it directly binds DNA and propose that the transformation pilus is the primary DNA receptor on the bacterial cell during transformation in S. pneumoniae. Being a central component of the transformation apparatus, the transformation pilus enables S. pneumoniae, a major Gram-positive human pathogen, to acquire resistance to antibiotics and to escape vaccines through the binding and incorporation of new genetic material.

Vyšlo v časopise: A Type IV Pilus Mediates DNA Binding during Natural Transformation in. PLoS Pathog 9(6): e32767. doi:10.1371/journal.ppat.1003473
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003473

Souhrn

Zdroje

1. GriffithF (1928) The Significance of Pneumococcal Types. The Journal of hygiene 27: 113–159.

2. JohnsborgO, EldholmV, HavarsteinLS (2007) Natural genetic transformation: prevalence, mechanisms and function. Research in microbiology 158: 767–778.

3. PopaO, DaganT (2011) Trends and barriers to lateral gene transfer in prokaryotes. Current opinion in microbiology 14: 615–623.

4. HillerNL, AhmedA, PowellE, MartinDP, EutseyR, et al. (2010) Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS pathogens 6: e1001108.

5. HavarsteinLS, CoomaraswamyG, MorrisonDA (1995) An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proceedings of the National Academy of Sciences of the United States of America 92: 11140–11144.

6. PrudhommeM, AttaiechL, SanchezG, MartinB, ClaverysJP (2006) Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313: 89–92.

7. ChenI, DubnauD (2004) DNA uptake during bacterial transformation. Nature reviews Microbiology 2: 241–249.

8. ClaverysJP, MartinB, PolardP (2009) The genetic transformation machinery: composition, localization, and mechanism. FEMS microbiology reviews 33: 643–656.

9. ChenI, ProvvediR, DubnauD (2006) A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. The Journal of biological chemistry 281: 21720–21727.

10. DagkessamanskaiaA, MoscosoM, HenardV, GuiralS, OverwegK, et al. (2004) Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Molecular microbiology 51: 1071–1086.

11. PetersonSN, SungCK, ClineR, DesaiBV, SnesrudEC, et al. (2004) Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Molecular microbiology 51: 1051–1070.

12. KaufensteinM, van der LaanM, GraumannPL (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.

13. BergeM, MoscosoM, PrudhommeM, MartinB, ClaverysJP (2002) Uptake of transforming DNA in Gram-positive bacteria: a view from Streptococcus pneumoniae. Molecular microbiology 45: 411–421.

14. BrileyKJr, Dorsey-OrestoA, PrepiakP, DiasMJ, MannJM, et al. (2011) The secretion ATPase ComGA is required for the binding and transport of transforming DNA. Molecular microbiology 81: 818–830.

15. ChungYS, DubnauD (1998) All seven comG open reading frames are required for DNA binding during transformation of competent Bacillus subtilis. Journal of bacteriology 180: 41–45.

16. NunnD, BergmanS, LoryS (1990) Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. Journal of bacteriology 172: 2911–2919.

17. MartinB, GranadelC, CampoN, HenardV, PrudhommeM, et al. (2010) Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Molecular microbiology 75: 1513–1528.

18. Chamot-RookeJ, MikatyG, MalosseC, SoyerM, DumontA, et al. (2011) Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331: 778–782.

19. StromMS, NunnDN, LoryS (1993) A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proceedings of the National Academy of Sciences of the United States of America 90: 2404–2408.

20. StromMS, LoryS (1991) Amino acid substitutions in pilin of Pseudomonas aeruginosa. Effect on leader peptide cleavage, amino-terminal methylation, and pilus assembly. The Journal of biological chemistry 266: 1656–1664.

21. BurtonB, DubnauD (2010) Membrane-associated DNA transport machines. Cold Spring Harbor perspectives in biology 2: a000406.

22. DupaigneP, Le BretonC, FabreF, GangloffS, Le CamE, et al. (2008) The Srs2 helicase activity is stimulated by Rad51 filaments on dsDNA: implications for crossover incidence during mitotic recombination. Molecular cell 29: 243–254.

23. MejeanV, ClaverysJP (1993) DNA processing during entry in transformation of Streptococcus pneumoniae. The Journal of biological chemistry 268: 5594–5599.

24. BarocchiMA, RiesJ, ZogajX, HemsleyC, AlbigerB, et al. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proceedings of the National Academy of Sciences of the United States of America 103: 2857–2862.

25. AlloingG, MartinB, GranadelC, ClaverysJP (1998) Development of competence in Streptococcus pneumonaie: pheromone autoinduction and control of quorum sensing by the oligopeptide permease. Molecular microbiology 29: 75–83.

26. PestovaEV, HavarsteinLS, MorrisonDA (1996) Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system. Molecular microbiology 21: 853–862.

27. CamposM, CisnerosDA, NivaskumarM, FranceticO (2013) The type II secretion system - a dynamic fiber assembly nanomachine. Research in microbiology [Epub ahead of print] doi:10.1016/j.resmic.2013.03.013

28. VargaJJ, NguyenV, O'BrienDK, RodgersK, WalkerRA, et al. (2006) Type IV pili-dependent gliding motility in the Gram-positive pathogen Clostridium perfringens and other Clostridia. Molecular microbiology 62: 680–694.

29. ImamS, ChenZ, RoosDS, PohlschroderM (2011) Identification of surprisingly diverse type IV pili, across a broad range of gram-positive bacteria. PloS one 6: e28919.

30. CraigL, PiqueME, TainerJA (2004) Type IV pilus structure and bacterial pathogenicity. Nature reviews Microbiology 2: 363–378.

31. BiswasGD, SoxT, BlackmanE, SparlingPF (1977) Factors affecting genetic transformation of Neisseria gonorrhoeae. Journal of bacteriology 129: 983–992.

32. DoughertyTJ, AsmusA, TomaszA (1979) Specificity of DNA uptake in genetic transformation of gonococci. Biochemical and biophysical research communications 86: 97–104.

33. van SchaikEJ, GiltnerCL, AudetteGF, KeizerDW, BautistaDL, et al. (2005) DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. Journal of bacteriology 187: 1455–1464.

34. LangE, HaugenK, FleckensteinB, HombersetH, FryeSA, et al. (2009) Identification of neisserial DNA binding components. Microbiology 155: 852–862.

35. CehovinA, SimpsonPJ, McDowellMA, BrownDR, NoscheseR, 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.

36. CarbonnelleE, HelaineS, NassifX, PelicicV (2006) A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Molecular microbiology 61: 1510–1522.

37. GeorgiadouM, CastagniniM, KarimovaG, LadantD, PelicicV (2012) Large-scale study of the interactions between proteins involved in type IV pilus biology in Neisseria meningitidis: characterization of a subcomplex involved in pilus assembly. Molecular microbiology 84: 857–873.

38. MerzAJ, SoM, SheetzMP (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98–102.

39. RabinovichL, SigalN, BorovokI, Nir-PazR, HerskovitsAA (2012) Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150: 792–802.

40. MartinB, PrudhommeM, AlloingG, GranadelC, ClaverysJP (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Molecular microbiology 38: 867–878.

41. SauvonnetN, VignonG, PugsleyAP, GounonP (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. The EMBO journal 19: 2221–2228.

42. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature methods 9: 671–675.

43. HansenJK, ForestKT (2006) Type IV pilin structures: insights on shared architecture, fiber assembly, receptor binding and type II secretion. Journal of molecular microbiology and biotechnology 11: 192–207.