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Concerted Spatio-Temporal Dynamics of Imported DNA and ComE DNA Uptake Protein during Gonococcal Transformation
Bacterial transformation is the import and inheritable integration of external DNA. As such, it is believed to be a major evolutionary force. A key step is the import of DNA through the outer membrane. Here, we have characterized the spatio-temporal dynamics of DNA during import and residence in the periplasm of the Gram-negative pathogen Neisseria gonorrhoeae. We found that the periplasm can serve as a reservoir for imported DNA that can fill within five minutes by importing DNA from the environment. The amount of imported DNA roughly corresponds to the size of a phage genome. The periplasmic DNA-binding protein ComE is homogeneously distributed in the periplasm in the absence of extracellular DNA. It relocates rapidly to imported DNA when external DNA is added to competent gonococci. As ComE governs the carrying capacity of the periplasm, we propose that it might condense DNA, thus linking DNA uptake to its compaction. Although the import through the outer membrane was localized all around the cell contour, the major part of the imported DNA relocated to the septum at the center of diplococci. Our findings strongly support the idea that the periplasm masses DNA independently of transport through the inner membrane.
Vyšlo v časopise: Concerted Spatio-Temporal Dynamics of Imported DNA and ComE DNA Uptake Protein during Gonococcal Transformation. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004043
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004043Souhrn
Bacterial transformation is the import and inheritable integration of external DNA. As such, it is believed to be a major evolutionary force. A key step is the import of DNA through the outer membrane. Here, we have characterized the spatio-temporal dynamics of DNA during import and residence in the periplasm of the Gram-negative pathogen Neisseria gonorrhoeae. We found that the periplasm can serve as a reservoir for imported DNA that can fill within five minutes by importing DNA from the environment. The amount of imported DNA roughly corresponds to the size of a phage genome. The periplasmic DNA-binding protein ComE is homogeneously distributed in the periplasm in the absence of extracellular DNA. It relocates rapidly to imported DNA when external DNA is added to competent gonococci. As ComE governs the carrying capacity of the periplasm, we propose that it might condense DNA, thus linking DNA uptake to its compaction. Although the import through the outer membrane was localized all around the cell contour, the major part of the imported DNA relocated to the septum at the center of diplococci. Our findings strongly support the idea that the periplasm masses DNA independently of transport through the inner membrane.
Zdroje
1. ChenI, DubnauD (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2 : 241–249.
2. BaltrusDA (2013) Exploring the costs of horizontal gene transfer. Trends in ecology & evolution 28 : 489–495.
3. FryeSA, NilsenM, TonjumT, AmburOH (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. KidaneD, AyoraS, SweasyJB, GraumannPL, AlonsoJC (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. LaurenceauR, Pehau-ArnaudetG, BaconnaisS, GaultJ, MalosseC, et al. (2013) A type IV pilus mediates DNA binding during natural transformation in Streptococcus pneumoniae. PLoS pathogens 9: e1003473.
7. AasFE, WolfgangM, FryeS, DunhamS, LovoldC, 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. LongCD, TobiasonDM, LazioMP, KlineKA, SeifertHS (2003) Low-level pilin expression allows for substantial DNA transformation competence in Neisseria gonorrhoeae. Infection and immunity 71 : 6279–6291.
9. Winther-LarsenHC, WolfgangMC, van PuttenJP, RoosN, AasFE, 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. SalomonssonE, ForsbergA, RoosN, HolzC, MaierB, 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. AasFE, LovoldC, KoomeyM (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. GoodmanSD, ScoccaJJ (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. 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.
14. DrakeSL, KoomeyM (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. AssalkhouR, BalasinghamS, CollinsRF, FryeSA, DavidsenT, et al. (2007) The outer membrane secretin PilQ from Neisseria meningitidis binds DNA. Microbiology 153 : 1593–1603.
16. ChenI, GotschlichEC (2001) ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J Bacteriol 183 : 3160–3168.
17. FaciusD, FusseneggerM, MeyerTF (1996) Sequential action of factors involved in natural competence for transformation of Neisseria gonorrhoeae. FEMS Microbiol Lett 137 : 159–164.
18. FusseneggerM, KahrsAF, FaciusD, MeyerTF (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. FaciusD, MeyerTF (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. KidaneD, GraumannPL (2005) Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 122 : 73–84.
21. AttaiechL, OlivierA, Mortier-BarriereI, SouletAL, GranadelC, 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. ChausseeMS, HillSA (1998) Formation of single-stranded DNA during DNA transformation of Neisseria gonorrhoeae. Journal of bacteriology 180 : 5117–5122.
23. MaierB, ChenI, DubnauD, SheetzMP (2004) DNA transport into Bacillus subtilis requires proton motive force to generate large molecular forces. Nat Struct Mol Biol 11 : 643–649.
24. StinglK, MullerS, Scheidgen-KleyboldtG, ClausenM, MaierB (2010) Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc Natl Acad Sci U S A 107 : 1184–1189.
25. AllemandJF, MaierB, SmithDE (2012) Molecular motors for DNA translocation in prokaryotes. Current opinion in biotechnology 23 : 503–509.
26. AllemandJF, MaierB (2009) Bacterial translocation motors investigated by single molecule techniques. FEMS Microbiol Rev 33 : 593–610.
27. KrugerNJ, StinglK (2011) Two steps away from novelty–principles of bacterial DNA uptake. Molecular microbiology 80 : 860–867.
28. HahnJ, MaierB, HaijemaBJ, SheetzM, DubnauD (2005) Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 122 : 59–71.
29. 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.
30. KramerN, HahnJ, DubnauD (2007) Multiple interactions among the competence proteins of Bacillus subtilis. Mol Microbiol 65 : 454–464.
31. ProvvediR, DubnauD (1999) ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Molecular microbiology 31 : 271–280.
32. BergeMJ, KamgoueA, MartinB, PolardP, CampoN, et al. (2013) Midcell Recruitment of the DNA Uptake and Virulence Nuclease, EndA, for Pneumococcal Transformation. PLoS pathogens 9: e1003596.
33. MaierB, RadlerJO (2000) DNA on fluid membranes: A model polymer in two dimensions. Macromolecules 33 : 7185–7194.
34. HwangH, KimH, MyongS (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. SuckowG, SeitzP, BlokeschM (2011) Quorum sensing contributes to natural transformation of Vibrio cholerae in a species-specific manner. Journal of bacteriology 193 : 4914–4924.
36. SeitzP, ModarresHP, BorgeaudS, BulushevRD, SteinbockLJ, RadenovicA, Dal PeraroM, BlokeschM (2014) ComEA is essential for the transfer of external DNA into the periplasm of naturally transformable Vibrio cholerae. PLoS genetics 10: e1004066.
37. BerryJL, PhelanMM, CollinsRF, AdomaviciusT, TonjumT, et al. (2012) Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS pathogens 8: e1002923.
38. HolzC, OpitzD, GreuneL, KurreR, KoomeyM, et al. (2010) Multiple pilus motors cooperate for persistent bacterial movement in two dimensions. Physical review letters 104 : 178104.
39. SeitzP, BlokeschM (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. KahnME, BaranyF, SmithHO (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. BaroukiR, SmithHO (1985) Reexamination of phenotypic defects in rec-1 and rec-2 mutants of Haemophilus influenzae Rd. Journal of bacteriology 163 : 629–634.
42. LangE, HaugenK, FleckensteinB, HombersetH, FryeSA, et al. (2009) Identification of neisserial DNA binding components. Microbiology 155 : 852–862.
43. SteichenCT, ChoC, ShaoJQ, ApicellaMA (2011) The Neisseria gonorrhoeae biofilm matrix contains DNA, and an endogenous nuclease controls its incorporation. Infection and immunity 79 : 1504–1511.
44. Winther-LarsenHC, HeggeFT, WolfgangM, HayesSF, van PuttenJP, 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. WolfgangM, van PuttenJP, HayesSF, DorwardD, KoomeyM (2000) Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. Embo J 19 : 6408–6418.
46. AasFE, Winther-LarsenHC, WolfgangM, FryeS, LovoldC, 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.
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