1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Mobile DNA in the Pathogenic

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    593.23 Kb
  • XML
    155.15 Kb
  • HTML
    162.78 Kb
  • Authors: Kyle P. Obergfell1, H. Steven Seifert2
  • Editors: Martin Gellert3, Nancy Craig4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Northwestern University Feinberg School of Medicine, Department of Microbiology and Immunology, Chicago, IL 60611; 2: Northwestern University Feinberg School of Medicine, Department of Microbiology and Immunology, Chicago, IL 60611; 3: National Institutes of Health, Bethesda, MD; 4: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
  • Received 03 April 2014 Accepted 09 April 2014 Published 29 January 2015
  • H. Steven Seifert, h-seifert@northwestern.edu
image of Mobile DNA in the Pathogenic <span class="jp-italic">Neisseria</span>
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Mobile DNA in the Pathogenic , Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/1/MDNA3-0015-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/1/MDNA3-0015-2014-2.gif
  • Abstract:

    The genus contains two pathogenic species of prominant public health concern: and . These pathogens display a notable ability to undergo frequent programmed recombination events. The recombination-mediated pathways of transformation and pilin antigenic variation in the are well-studied systems that are critical for pathogenesis. Here we will detail the conserved and unique aspects of transformation and antigenic variation in the . Transformation will be followed from initial DNA binding through recombination into the genome with consideration to the factors necessary at each step. Additional focus is paid to the unique type IV secretion system that mediates donation of transforming DNA in the pathogenic . The pilin antigenic variation system uses programmed recombinations to alter a major surface determinant, which allows immune avoidance and promotes infection. We discuss the - and - acting factors which facilitate pilin antigenic variation and present the current understanding of the mechanisms involved in the process.

  • Citation: Obergfell K, Seifert H. 2015. Mobile DNA in the Pathogenic . Microbiol Spectrum 3(1):MDNA3-0015-2014. doi:10.1128/microbiolspec.MDNA3-0015-2014.

Key Concept Ranking

Type IV Secretion Systems
0.4234951
0.4234951

References

1. Virji M. 2009. Pathogenic Neisseriae: surface modulation, pathogenesis and infection control. Nat Rev Microbiol 7:274–286. [PubMed][CrossRef]
2. Johnston C, Martin B, Fichant G, Polard P, Claverys JP. 2014. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol 12:181–196. [PubMed][CrossRef]
3. Sparling PF. 1966. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J Bacteriol 92:1364–1371. [PubMed]
4. Biswas GD, Sox T, Blackman E, Sparling PF. 1977. Factors affecting genetic transformation of Neisseria gonorrhoeae. J Bacteriol 129:983–992. [PubMed]
5. Koomey M. 1998. Competence for natural transformation in Neisseria gonorrhoeae: a model system for studies of horizontal gene transfer. APMIS Suppl 84:56–61. [PubMed][CrossRef]
6. Sox TE, Mohammed W, Blackman E, Biswas G, Sparling PF. 1978. Conjugative plasmids in Neisseria gonorrhoeae. J Bacteriol 134:278–286. [PubMed]
7. Chen I, Dubnau D. 2004. DNA uptake during bacterial transformation. Nat Rev Microbiol 2:241–249. [PubMed][CrossRef]
8. Smith JM, Smith NH, O'Rourke M, Spratt BG. 1993. How clonal are bacteria? Proc Natl Acad Sci U S A 90:4384–4388. [PubMed][CrossRef]
9. Martin IM, Ison CA. 2003. Detection of mixed infection of Neisseria gonorrhoeae. Sex Transm Infect 79:56–58. [CrossRef]
10. Lynn F, Hobbs MM, Zenilman JM, Behets FM, Van Damme K, Rasamindrakotroka A, Bash MC. 2005. Genetic typing of the porin protein of Neisseria gonorrhoeae from clinical noncultured samples for strain characterization and identification of mixed gonococcal infections. J Clin Microbiol 43:368–375. [PubMed][CrossRef]
11. Gibbs CP, Meyer TF. 1996. Genome plasticity in Neisseria gonorrhoeae. FEMS Microbiol Lett 145:173–179. [PubMed][CrossRef]
12. Hobbs MM, Seiler A, Achtman M, Cannon JG. 1994. Microevolution within a clonal population of pathogenic bacteria: recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis. Mol Microbiol 12:171–180. [PubMed][CrossRef]
13. Snyder LA, Davies JK, Saunders NJ. 2004. Microarray genomotyping of key experimental strains of Neisseria gonorrhoeae reveals gene complement diversity and five new neisserial genes associated with Minimal Mobile Elements. BMC Genomics 5:23. [PubMed][CrossRef]
14. Buckee CO, Jolley KA, Recker M, Penman B, Kriz P, Gupta S, Maiden MC. 2008. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proc Natl Acad Sci U S A 105:15082–15087. [PubMed][CrossRef]
15. Goire N, Lahra MM, Chen M, Donovan B, Fairley CK, Guy R, Kaldor J, Regan D, Ward J, Nissen MD, Sloots TP, Whiley DM. 2014. Molecular approaches to enhance surveillance of gonococcal antimicrobial resistance. Nat Rev Microbiol 12:223–229. [PubMed][CrossRef]
16. Kirkcaldy RD, Ballard RC, Dowell D. 2011. Gonococcal resistance: are cephalosporins next? Curr Infect Dis Rep 13:196–204. [PubMed][CrossRef]
17. Lewis DA. 2010. The Gonococcus fights back: is this time a knock out? Sex Trans Inf 86:415–421. [PubMed][CrossRef]
18. Prevention CfDCa. 2013. Antibiotic resistance threats in the United States, 2013. CDC, Atlanta.
19. Craig L, Pique ME, Tainer JA. 2004. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363–378. [PubMed][CrossRef]
20. Merz AJ, So M, Sheetz MP. 2000. Pilus retraction powers bacterial twitching motility. Nature 407(6800):98–102. [PubMed][CrossRef]
21. Swanson J. 1973. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J Exp Med 137:571–589. [PubMed][CrossRef]
22. Dietrich M, Bartfeld S, Munke R, Lange C, Ogilvie LA, Friedrich A, Meyer TF. 2011. Activation of NF-kappaB by Neisseria gonorrhoeae is associated with microcolony formation and type IV pilus retraction. Cell Microbiol 13:1168–1182. [PubMed][CrossRef]
23. Freitag NE, Seifert HS, Koomey M. 1995. Characterization of the pilF-pilD pilus-assembly locus of Neisseria gonorrhoeae. Mol Microbiol 16:575–586. [PubMed][CrossRef]
24. Long CD, Tobiason DM, Lazio MP, Kline KA, Seifert HS. 2003. Low-level pilin expression allows for substantial DNA transformation competence in Neisseria gonorrhoeae. Infect Immun 71:6279–6291. [PubMed][CrossRef]
25. Drake SL, 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. [PubMed][CrossRef]
26. Tonjum T, Freitag NE, Namork E, Koomey M. 1995. Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol Microbiol 95:451–464. [PubMed][CrossRef]
27. Wolfgang M, Lauer P, Park HS, Brossay L, Hebert J, Koomey M. 1998. pilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29:321–330. [PubMed][CrossRef]
28. Biswas GD, Lacks SA, Sparling PF. 1989. Transformation-deficient mutants of piliated Neisseria gonorrhoeae. J Bacteriol 171:657–664. [PubMed]
29. Aas FE, Wolfgang M, Frye S, Dunham S, Lovold C, 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. [PubMed][CrossRef]
30. Berry JL, Cehovin A, McDowell MA, Lea SM, Pelicic V. 2013. Functional analysis of the interdependence between DNA uptake sequence and its cognate ComP receptor during natural transformation in Neisseria species. PLoS Genet 9:19. [PubMed][CrossRef]
31. Chen I, Dubnau D. 2003. DNA transport during transformation. Front Biosci 8:s544–556. [PubMed][CrossRef]
32. Haas R, Schwarz H, Meyer TF. 1987. Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae. Proc Natl Acad Sci U S A 84:9079–9083. [PubMed][CrossRef]
33. Gibbs CP, Reimann BY, Schultz E, Kaufmann A, Haas R, Meyer TF. 1989. Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms. Nature 338(6217):651–652. [PubMed][CrossRef]
34. Long CD, Madraswala RN, Seifert HS. 1998. Comparisons between colony phase variation of Neisseria gonorrhoeae FA1090 and pilus, pilin, and S-pilin expression. Infect Immun 66(5):1918–1927. [PubMed]
35. Collins RF, Davidsen L, Derrick JP, Ford RC, Tonjum T. 2001. Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J Bacteriol 183(13):3825–3832. [PubMed][CrossRef]
36. Hamilton HL, Dillard JP. 2006. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 59:376–385. [PubMed][CrossRef]
37. 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. [PubMed][CrossRef]
38. Burton B, Dubnau D. 2010. Membrane-associated DNA transport machines. Cold Spring Harbor Persp Biol 2:a000406. [PubMed][CrossRef]
39. Chen I, Gotschlich EC. 2001. ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J Bacteriol 183:3160–3168. [PubMed][CrossRef]
40. Seitz P, Pezeshgi Modarres H, 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 in Naturally Transformable Vibrio cholerae Cells. PLoS Genet 10(1):2. [PubMed][CrossRef]
41. Salman H, Zbaida D, Rabin Y, Chatenay D, Elbaum M. 2001. Kinetics and mechanism of DNA uptake into the cell nucleus. Proc Natl Acad Sci U S A 98(13):7247–7252. [PubMed][CrossRef]
42. 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. [PubMed][CrossRef]
43. Elkins C, Thomas CE, Seifert HS, Sparling PF. 1991. Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J Bacteriol 173:3911–3913. [PubMed]
44. Ambur OH, Frye SA, Tonjum T. 2007. New functional identity for the DNA uptake sequence in transformation and its presence in transcriptional terminators. J Bacteriol 189:2077–2085. [PubMed][CrossRef]
45. Smith HO, Gwinn ML, Salzberg SL. 1999. DNA uptake signal sequences in naturally transformable bacteria. Res Microbiol 150:603–616. [PubMed][CrossRef]
46. Davidsen T, Rodland EA, Lagesen K, Seeberg E, Rognes T, Tonjum T. 2004. Biased distribution of DNA uptake sequences towards genome maintenance genes. Nucleic Acids Res 32:1050–1058. [PubMed][CrossRef]
47. Treangen TJ, Ambur OH, Tonjum T, Rocha EP. 2008. The impact of the neisserial DNA uptake sequences on genome evolution and stability. Genome Biol 9:2008–2009. [PubMed][CrossRef]
48. Duffin PM, Seifert HS. 2010. DNA uptake sequence-mediated enhancement of transformation in Neisseria gonorrhoeae is strain dependent. J Bacteriol 192:4436–4444. [PubMed][CrossRef]
49. Duffin PM, Seifert HS. 2012. Genetic transformation of Neisseria gonorrhoeae shows a strand preference. FEMS Microbiol Lett 334:44–48. [PubMed][CrossRef]
50. Mathis LS, Scocca JJ. 1984. On the role of pili in transformation of Neisseria gonorrhoeae. J Gen Microbiol 130:3165–3173. [PubMed]
51. Dorward DW, Garon CF. 1989. DNA-binding proteins in cells and membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171:4196–4201. [PubMed]
52. Wolfgang M, van Putten JP, Hayes SF, 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. [PubMed][CrossRef]
53. 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. [PubMed][CrossRef]
54. Cehovin A, Simpson PJ, McDowell MA, Brown DR, Noschese R, Pallett M, Brady J, Baldwin GS, Lea SM, Matthews SJ, Pelicic V. 2013. Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci U S A 110:3065–3070. [PubMed][CrossRef]
55. Assalkhou R, Balasingham S, Collins RF, Frye SA, Davidsen T, Benam AV, Bjoras M, Derrick JP, Tonjum T. 2007. The outer membrane secretin PilQ from Neisseria meningitidis binds DNA. Microbiology 153:1593–1603. [PubMed][CrossRef]
56. Lang E, Haugen K, Fleckenstein B, Homberset H, Frye SA, Ambur OH, Tonjum T. 2009. Identification of neisserial DNA binding components. Microbiology 155:852–862. [PubMed][CrossRef]
57. Benam AV, Lang E, Alfsnes K, Fleckenstein B, Rowe AD, Hovland E, Ambur OH, Frye SA, Tonjum T. 2011. Structure-function relationships of the competence lipoprotein ComL and SSB in meningococcal transformation. Microbiology 157:1329–1342. [PubMed][CrossRef]
58. Frye SA, Nilsen M, Tonjum T, Ambur OH. 2013. Dialects of the DNA uptake sequence in Neisseriaceae. PLoS Genet 9:18. [PubMed][CrossRef]
59. Berry JL, Cehovin A, McDowell MA, Lea SM, Pelicic V. 2013. Functional Analysis of the Interdependence between DNA Uptake Sequence and Its Cognate ComP Receptor during Natural Transformation in Neisseria Species. PLoS Genet 9:e1004014. [PubMed][CrossRef]
60. Fussenegger M, Facius D, Meier J, Meyer TF. 1996. A novel peptidoglycan-linked lipoprotein (ComL) that functions in natural transformation competence of Neisseria gonorrhoeae. Mol Microbiol 19:1095–1105. [PubMed][CrossRef]
61. 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. Mol Microbiol 19:1357–1372. [PubMed][CrossRef]
62. Chaussee MS, Hill SA. 1998. Formation of single-stranded DNA during DNA transformation of Neisseria gonorrhoeae. J Bacteriol 180:5117–5122. [PubMed]
63. Draskovic I, Dubnau D. 2005. Biogenesis of a putative channel protein, ComEC, required for DNA uptake: membrane topology, oligomerization and formation of disulphide bonds. Mol Microbiol 55:881–896. [PubMed][CrossRef]
64. Sox TE, Mohammed W, Sparling PF. 1979. Transformation-derived Neisseria gonorrhoeae plasmids with altered structure and function. J Bacteriol 138:510–518. [PubMed]
65. Stein DC, Gunn JS, Radlinska M, Piekarowicz A. 1995. Restriction and modification systems of Neisseria gonorrhoeae. Gene 157:19–22. [PubMed][CrossRef]
66. Eisenstein BI, Sox T, Biswas G, Blackman E, Sparling PF. 1977. Conjugal transfer of the gonococcal penicillinase plasmid. Science 195:998–1000. [PubMed][CrossRef]
67. Zhang Y, Heidrich N, Ampattu BJ, Gunderson CW, Seifert HS, Schoen C, Vogel J, Sontheimer EJ. 2013. Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol Cell 50:488–503. [PubMed][CrossRef]
68. Barrangou R. 2013. CRISPR-Cas systems and RNA-guided interference. Wiley Interdiscip Rev RNA 4:267–278. [PubMed][CrossRef]
69. Koomey JM, Falkow S. 1987. Cloning of the recA gene of Neisseria gonorrhoeae and construction of gonococcal recA mutants. J Bacteriol 169:790–795. [PubMed]
70. Chen Z, Yang H, Pavletich NP. 2008. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453(7194):489–494. [PubMed][CrossRef]
71. Gruenig MC, Stohl EA, Chitteni-Pattu S, Seifert HS, Cox MM. 2010. Less is more: Neisseria gonorrhoeae RecX protein stimulates recombination by inhibiting RecA. J Biol Chem 285:37188–37197. [PubMed][CrossRef]
72. Mehr IJ, Seifert HS. 1998. Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol Microbiol 30:697–710. [PubMed][CrossRef]
73. Stohl EA, Seifert HS. 2001. The recX gene potentiates homologous recombination in Neisseria gonorrhoeae. Mol Microbiol 40:1301–1310. [PubMed][CrossRef]
74. Dillingham MS, Kowalczykowski SC. 2008. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol Mol Biol Rev 72:642–671. [PubMed][CrossRef]
75. Kline KA, Seifert HS. 2005. Mutation of the priA gene of Neisseria gonorrhoeae affects DNA transformation and DNA repair. J Bacteriol 187:5347–5355. [PubMed][CrossRef]
76. Marians KJ. 2000. PriA-directed replication fork restart in Escherichia coli. Trends Biochem Sci 25:185–189. [PubMed][CrossRef]
77. Mell JC, Redfield RJ. 2014. Natural competence and the evolution of DNA uptake specificity. J Bacteriol 31:31. [PubMed][CrossRef]
78. Lewis K. 2000. Programmed death in bacteria. Microbiol Mol Biol Rev 64:503–514. [PubMed][CrossRef]
79. Dillard JP, Seifert HS. 2001. A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 41:263–277. [CrossRef]
80. Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT, Dillard JP. 2005. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55:1704–1721. [PubMed][CrossRef]
81. Snyder LA, Jarvis SA, Saunders NJ. 2005. Complete and variant forms of the ‘gonococcal genetic island’ in Neisseria meningitidis. Microbiology 151:4005–4013. [PubMed][CrossRef]
82. Woodhams KL, Benet ZL, Blonsky SE, Hackett KT, Dillard JP. 2012. Prevalence and detailed mapping of the gonococcal genetic island in Neisseria meningitidis. J Bacteriol 194:2275–2285. [PubMed][CrossRef]
83. Dominguez NM, Hackett KT, Dillard JP. 2011. XerCD-mediated site-specific recombination leads to loss of the 57-kilobase gonococcal genetic island. J Bacteriol 193:377–388. [PubMed][CrossRef]
84. Salgado-Pabón W, Jain S, Turner N, Van Der Does C, Dillard JP. 2007. A novel relaxase homologue is involved in chromosomal DNA processing for type IV secretion in Neisseria gonorrhoeae. Mol Microbiol 66:930–947. [PubMed][CrossRef]
85. Ramsey ME, Woodhams KL, Dillard JP. 2011. The Gonococcal Genetic Island and Type IV Secretion in the Pathogenic Neisseria. Front Microbiol 2(61):00061. [PubMed][CrossRef]
86. Bhatty M, Laverde Gomez JA, Christie PJ. 2013. The expanding bacterial type IV secretion lexicon. Res Microbiol 164:620–639. [PubMed][CrossRef]
87. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 2009. Structure of the outer membrane complex of a type IV secretion system. Nature 462(7276):1011–1015. [PubMed][CrossRef]
88. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323(5911):266–268. [PubMed][CrossRef]
89. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat Rev Microbiol 7:703–714. [PubMed][CrossRef]
90. Kohler PL, Chan YA, Hackett KT, Turner N, Hamilton HL, Cloud-Hansen KA, Dillard JP. 2013. Mating pair formation homologue TraG is a variable membrane protein essential for contact-independent type IV secretion of chromosomal DNA by Neisseria gonorrhoeae. J Bacteriol 195:1666–1679. [PubMed][CrossRef]
91. Chan YA, Hackett KT, Dillard JP. 2012. The lytic transglycosylases of Neisseria gonorrhoeae. Microb Drug Resist 18:271–279. [PubMed][CrossRef]
92. Leonard TA, Moller-Jensen J, Lowe J. 2005. Towards understanding the molecular basis of bacterial DNA segregation. Philos Trans R Soc Lond B Biol Sci 360(1455):523–535. [PubMed][CrossRef]
93. Grinter NJ. 1981. Analysis of chromosome mobilization using hybrids between plasmid RP4 and a fragment of bacteriophage lambda carrying IS1. Plasmid 5:267–276. [PubMed][CrossRef]
94. Salgado-Pabon W, Du Y, Hackett KT, Lyons KM, Arvidson CG, Dillard JP. 2010. Increased expression of the type IV secretion system in piliated Neisseria gonorrhoeae variants. J Bacteriol 192:1912–1920. [PubMed][CrossRef]
95. Zola TA, Strange HR, Dominguez NM, Dillard JP, Cornelissen CN. 2010. Type IV secretion machinery promotes ton-independent intracellular survival of Neisseria gonorrhoeae within cervical epithelial cells. Infect Immun 78:2429–2437. [PubMed][CrossRef]
96. Zweig MA, Schork S, Koerdt A, Siewering K, Sternberg C, Thormann K, Albers SV, Molin S, van der Does C. 2013. Secreted single-stranded DNA is involved in the initial phase of biofilm formation by Neisseria gonorrhoeae. Environ Microbiol 3:1462–2920. [PubMed][CrossRef]
97. Takeuchi N, Kaneko K, Koonin EV. 2013. Horizontal Gene Transfer Can Rescue Prokaryotes from Muller's Ratchet: Benefit of DNA from Dead Cells and Population Subdivision. G3 17(113):009845. [PubMed][CrossRef]
98. Baumdicker F, Hess WR, Pfaffelhuber P. 2012. The infinitely many genes model for the distributed genome of bacteria. Genome Biol Evol 4:443–456. [PubMed][CrossRef]
99. Vink C, Rudenko G, Seifert HS. 2012. Microbial antigenic variation mediated by homologous DNA recombination. FEMS Microbiol Rev 36:917–948. [PubMed]
100. van der Woude MW. 2011. Phase variation: how to create and coordinate population diversity. Curr Opin Microbiol 14:205–211. [PubMed][CrossRef]
101. Kline KA, Sechman EV, Skaar EP, Seifert HS. 2003. Recombination, repair and replication in the pathogenic Neisseriae: the 3 R's of molecular genetics of two human-specific bacterial pathogens. Mol Microbiol 50:3–13. [PubMed][CrossRef]
102. Stern A, Brown M, Nickel P, Meyer TF. 1986. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61–71. [PubMed][CrossRef]
103. Danaher RJ, Levin JC, Arking D, Burch CL, Sandlin R, Stein DC. 1995. Genetic basis of Neisseria gonorrhoeae lipooligosaccharide antigenic variation. J Bacteriol 177:7275–7279. [PubMed]
104. Jennings MP, Hood DW, Peak IR, Virji M, Moxon ER. 1995. Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. Mol Microbiol 18:729–740. [PubMed][CrossRef]
105. Bos MP, Hogan D, Belland RJ. 1999. Homologue scanning mutagenesis reveals CD66 receptor residues required for neisserial Opa protein binding. J Exp Med 190:331–340. [PubMed][CrossRef]
106. Gotschlich EC. 1994. Genetic locus for the biosynthesis of the variable portion of Neisseria gonorrhoeae lipooligosaccharide. J Exp Med 180:2181–2190. [PubMed][CrossRef]
107. Meyer TF, Mlawer N, So M. 1982. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell 30:45–52. [PubMed][CrossRef]
108. Hamrick TS, Dempsey JA, Cohen MS, Cannon JG. 2001. Antigenic variation of gonococcal pilin expression in vivo: analysis of the strain FA1090 pilin repertoire and identification of the pilS gene copies recombining with pilE during experimental human infection. Microbiology 147:839–849. [PubMed]
109. Haas R, Meyer TF. 1986. The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44:107–115. [PubMed][CrossRef]
110. Haas R, Veit S, Meyer TF. 1992. Silent pilin genes of Neisseria gonorrhoeae MS11 and the occurrence of related hypervariant sequences among other gonococcal isolates. Mol Microbiol 6:197–208. [PubMed][CrossRef]
111. Segal E, Hagblom P, Seifert HS, So M. 1986. Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc Natl Acad Sci U S A 83:2177–2181. [PubMed][CrossRef]
112. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH, Tainer JA. 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 23:651–662. [PubMed][CrossRef]
113. Forest KT, Bernstein SL, Getzoff ED, So M, Tribbick G, Geysen HMX, Deal CD, Tainer JA. 1996. Assembly and antigenicity of the Neisseria gonorrhoeae pilus mapped with antibodies. Infect Immun 64:644–652. [PubMed]
114. Criss AK, Kline KA, Seifert HS. 2005. The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol 58:510–519. [PubMed][CrossRef]
115. Kellogg DS, Jr., Peacock WL, Jr., Deacon WE, Brown L, Pirkle DI. 1963. Neisseria gonorrhoeae. I. Virulence Genetically Linked to Clonal Variation. J Bacteriol 85:1274–1279. [PubMed]
116. Jonsson AB, Nyberg G, Normark S. 1991. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 10:477–488. [PubMed]
117. Segal E, Billyard E, So M, Storzbach S, Meyer TF. 1985. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 40:293–300. [PubMed][CrossRef]
118. Hagblom P, Segal E, Billyard E, So M. 1985. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315(6015):156–158. [PubMed][CrossRef]
119. Koomey M, Gotschlich EC, Robbins K, Bergstrom S, Swanson J. 1987. Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117:391–398. [PubMed]
120. Jennings MP, Jen FE, Roddam LF, Apicella MA, Edwards JL. 2011. Neisseria gonorrhoeae pilin glycan contributes to CR3 activation during challenge of primary cervical epithelial cells. Cell Microbiol 13:885–896. [PubMed][CrossRef]
121. Marceau M, Forest K, Beretti JL, Tainer J, Nassif X. 1998. Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol 27:705–715. [PubMed][CrossRef]
122. Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, Gault J, Imhaus AF, Martin P, Trellet M, Clary G, Chafey P, Camoin L, Nilges M, Nassif X, Dumenil G. 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331(6018):778–782. [PubMed][CrossRef]
123. Miller F, Phan G, Brissac T, Bouchiat C, Lioux G, Nassif X, Coureuil M. 2014. The Hypervariable Region of Meningococcal Major Pilin PilE Controls the Host Cell Response via Antigenic Variation. mBio 5:01024–13. [PubMed][CrossRef]
124. Mehr IJ, Seifert HS. 1997. Random shuttle mutagenesis: gonococcal mutants deficient in pilin antigenic variation. Mol Microbiol 23:1121–1131. [PubMed][CrossRef]
125. Sechman EV, Rohrer MS, Seifert HS. 2005. A genetic screen identifies genes and sites involved in pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol 57:468–483. [PubMed][CrossRef]
126. Cahoon LA, Seifert HS. 2009. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325(5941):764–767. [PubMed][CrossRef]
127. Stohl EA, Blount L, Seifert HS. 2002. Differential cross-complementation patterns of Escherichia coli and Neisseria gonorrhoeae RecA proteins. Microbiology 148:1821–1831. [PubMed]
128. Stohl EA, Gruenig MC, Cox MM, Seifert HS. 2011. Purification and characterization of the RecA protein from Neisseria gonorrhoeae. PloS one 6:0017101. [PubMed][CrossRef]
129. Stohl EA, Brockman JP, Burkle KL, Morimatsu K, Kowalczykowski SC, Seifert HS. 2003. Escherichia coli RecX inhibits RecA recombinase and coprotease activities in vitro and in vivo. J Biol Chem 278:2278–2285. [PubMed][CrossRef]
130. Mehr IJ, Long CD, Serkin CD, Seifert HS. 2000. A homologue of the recombination-dependent growth gene, rdgC, is involved in gonococcal pilin antigenic variation. Genetics 154:523–532. [PubMed]
131. Drees JC, Chitteni-Pattu S, McCaslin DR, Inman RB, Cox MM. 2006. Inhibition of RecA protein function by the RdgC protein from Escherichia coli. J Biol Chem 281:4708–4717. [PubMed][CrossRef]
132. Hiom K. 2009. DNA Repair: Common Approaches to Fixing Double-Strand Breaks. Curr Biol 19:R523–R525. [PubMed][CrossRef]
133. Skaar EP, Lazio MP, Seifert HS. 2002. Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J Bacteriol 184:919–927. [PubMed][CrossRef]
134. Killoran MP, Kohler PL, Dillard JP, Keck JL. 2009. RecQ DNA helicase HRDC domains are critical determinants in Neisseria gonorrhoeae pilin antigenic variation and DNA repair. Mol Microbiol 71:158–171. [PubMed][CrossRef]
135. Lane HE, Denhardt DT. 1974. The rep mutation. III. Altered structure of the replicating Escherichia coli chromosome. J Bacteriol 120:805–814. [PubMed]
136. Kline KA, Seifert HS. 2005. Role of the Rep helicase gene in homologous recombination in Neisseria gonorrhoeae. J Bacteriol 187:2903–2907. [PubMed][CrossRef]
137. Chaussee MS, Wilson J, Hill SA. 1999. Characterization of the recD gene of Neisseria gonorrhoeae MS11 and the effect of recD inactivation on pilin variation and DNA transformation. Microbiology 145:389–400. [PubMed][CrossRef]
138. Hill SA, Woodward T, Reger A, Baker R, Dinse T. 2007. Role for the RecBCD recombination pathway for pilE gene variation in repair-proficient Neisseria gonorrhoeae. J Bacteriol 189:7983–7990. [PubMed][CrossRef]
139. Helm RA, Seifert HS. 2009. Pilin antigenic variation occurs independently of the RecBCD pathway in Neisseria gonorrhoeae. J Bacteriol 191:5613–5621. [PubMed][CrossRef]
140. Sechman EV, Kline KA, Seifert HS. 2006. Loss of both Holliday junction processing pathways is synthetically lethal in the presence of gonococcal pilin antigenic variation. Mol Microbiol 61:185–193. [PubMed][CrossRef]
141. Wainwright LA, Pritchard KH, Seifert HS. 1994. A conserved DNA sequence is required for efficient gonococcal pilin antigenic variation. Mol Microbiol 13:75–87. [PubMed][CrossRef]
142. Howell-Adams B, Wainwright LA, Seifert HS. 1996. The size and position of heterologous insertions in a silent locus differentially affect pilin recombination in Neisseria gonorrhoeae. Mol Microbiol 22:509–522. [PubMed][CrossRef]
143. Howell-Adams B, Seifert HS. 1999. Insertion mutations in pilE differentially alter gonococcal pilin antigenic variation. J Bacteriol 181:6133–6141. [PubMed]
144. Kuryavyi V, Cahoon LA, Seifert HS, Patel DJ. 2012. RecA-binding pilE G4 sequence essential for pilin antigenic variation forms monomeric and 5′ end-stacked dimeric parallel G-quadruplexes. Structure 20:2090–2102. [PubMed][CrossRef]
145. Cahoon LA, Manthei KA, Rotman E, Keck JL, Seifert HS. 2013. The Neisseria gonorrhoeae RecQ helicase HRDC domains are essential for efficient binding and unwinding of the pilE guanine quartet structure required for pilin Av. J Bacteriol 195:2255–2261. [PubMed][CrossRef]
146. Cahoon LA, Seifert HS. 2013. Transcription of a cis-acting, noncoding, small RNA is required for pilin antigenic variation in Neisseria gonorrhoeae. PLoS Pathog 9(1):e1003074. [PubMed][CrossRef]
147. Seifert HS, Ajioka RS, Marchal C, Sparling PF, So M. 1988. DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae. Nature 336(6197):392–395. [PubMed][CrossRef]
148. Swanson J, Morrison S, Barrera O, Hill S. 1990. Piliation changes in transformation-defective gonococci. J Exp Med 171:2131–2139. [PubMed][CrossRef]
149. Zhang QY, DeRyckere D, Lauer P, Koomey M. 1992. Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc Natl Acad Sci U S A 89:5366–5370. [PubMed][CrossRef]
150. Tobiason DM, Seifert HS. 2006. The obligate human pathogen, Neisseria gonorrhoeae, is polyploid. PLoS Biol 4(6). [PubMed][CrossRef]
151. Stabler RA, Marsden GL, Witney AA, Li Y, Bentley SD, Tang CM, Hinds J. 2005. Identification of pathogen-specific genes through microarray analysis of pathogenic and commensal Neisseria species. Microbiology 151:2907–2922. [PubMed][CrossRef]
152. Seifert HS, Wright CJ, Jerse AE, Cohen MS, Cannon JG. 1994. Multiple gonococcal pilin antigenic variants are produced during experimental human infections. J Clin Invest 93:2744–2749. [PubMed][CrossRef]
153. Kobayashi I. 1992. Mechanisms for gene conversion and homologous recombination: the double-strand break repair model and the successive half crossing-over model. Adv Biophys 28:81–133. [PubMed][CrossRef]
154. Howell-Adams B, Seifert HS. 2000. Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37:1146–1158. [PubMed][CrossRef]
microbiolspec.MDNA3-0015-2014.citations
cm/3/1
content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0015-2014
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0015-2014
2015-01-29
2017-04-29

Abstract:

The genus contains two pathogenic species of prominant public health concern: and . These pathogens display a notable ability to undergo frequent programmed recombination events. The recombination-mediated pathways of transformation and pilin antigenic variation in the are well-studied systems that are critical for pathogenesis. Here we will detail the conserved and unique aspects of transformation and antigenic variation in the . Transformation will be followed from initial DNA binding through recombination into the genome with consideration to the factors necessary at each step. Additional focus is paid to the unique type IV secretion system that mediates donation of transforming DNA in the pathogenic . The pilin antigenic variation system uses programmed recombinations to alter a major surface determinant, which allows immune avoidance and promotes infection. We discuss the - and - acting factors which facilitate pilin antigenic variation and present the current understanding of the mechanisms involved in the process.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/3/1/MDNA3-0015-2014.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0015-2014&mimeType=html&fmt=ahah

Figures

Image of FIGURE 1

Click to view

FIGURE 1

Type IV pilus and DNA uptake. (A) Type IV pilus—the Tfp is a several micron long, 60 Å wide fiber anchored in the inner membrane by PilG that extends through the PilQ secretin pore. Composed mainly of the major pilin PilE (pilin), which is processed by a dedicated protease, PilD. The PilF and PilT NTPases mediate extension and retraction of the pilus through polymerization and depolymerization of the pilin subunits. (B) Competence pseudopilus—hypothesized pseudopilus that could mediate transformation. Uses the type IV pilus complex including the PilQ pore but is not an extended fiber. Possible localization of ComP to the pseudopilus could mediate specific DNA binding. (C) DNA uptake model—retraction of the (pseudo)pilus mediated by PilT brings the initial length of DNA into the periplasm. DNA is then bound by a protein or protein complex possibly containing ComE, which mediates import of the remaining length of DNA into the periplasm. The inner membrane protein ComA facilitates DNA entry into the cytoplasm. doi:10.1128/microbiolspec.MDNA3-0015-2014.f1

Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view

FIGURE 2

Type IV secretion system model. ParA and ParB recruit the chromosomal DNA to the type IV secretion system. TraI relaxase nicks the DNA at the site and the DNA is unwound most likely by the Yea helicase. The resulting single-stranded DNA, possibly still bound by TraI, is then secreted through the type IV secretion complex into the extracellular milieu in a contact-independent manner. The inner membrane complex is predicted to consist of TraG, TraD, and TraC with TraB spanning both the inner and outer membranes to form a channel for the DNA. The transglycosylases AtlA and LtgX create localized breaks in the peptidoglycan to allow the system to assemble. The outer membrane complex consists of TraB, TraK, and TraV. doi:10.1128/microbiolspec.MDNA3-0015-2014.f2

Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view

FIGURE 3

Molecular description of antigenic variation. The and loci have regions of sequence microhomology (grey) and variability (colored). Sequence from a nonexpressed loci copy is transferred into the expression locus with the sequence not changing. Recombination can occur (A) in just a section of the gene resulting in a hybrid, (B) across the entire gene resulting in an entirely new variable region of , or (C) multiple times with different silent copies resulting in a new sequence containing information from different silent copies throughout the variable regions. doi:10.1128/microbiolspec.MDNA3-0015-2014.f3

Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view

FIGURE 4

The guanine quartet (G4). (A) Gene map showing the location of the -associated G4-forming sequence and the sRNA promoter required for antigenic variation at the locus. (B) The sequence upstream of that forms a G4. Mutation of the boxed guanine residues leads to loss of antigenic variation implicating the G4 in antigenic variation. (C) The parallel G4 structure of the G4 as solved by nuclear magnetic resonance analysis. doi:10.1128/microbiolspec.MDNA3-0015-2014.f4

Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5

Click to view

FIGURE 5

Proposed recombination pathways. (A) Unequal crossing-over model—a dsDNA break occurs at the locus and (I) the 5′ ends are resected by RecBCD to leave 3′ overhangs. (II) A single 3′ end mediated by RecA, invades the locus forming a D-loop. (III) The 3′ ends are extended by DNA polymerase using the gene as a template. (IV) Resolution of the double Holliday junctions results in a new sequence without altering the donor sequence. (B) Successive half crossing-over model–recombination begins with a dsDNA break or single-stranded gap in in a region of homology. (I) An RecA and RecOR mediated half crossing-over event occurs linking the and a locus on a sister chromosome. (II) A second half crossing-over event occurs in another region of microhomology downstream of the first event between the hyrbid and the original locus. (III) This recombination event leads to a new sequence at the locus and destruction of the donor chromosome. (C) Hybrid intermediate model—similar to the half crossing-over model, recombination initiates with a double-stranded break or single-stranded gap at and (I) a half crossing-over event with a donor on the same chromosome. (II) This results in a hybrid intermediate and the loss of the donor chromosome. (III) The hybrid intermediate then undergoes two recombination events with the recipient on a different chromosome. The first recombination event would occur in the extensive region of homology upstream of the genes while the second even would use microhomology within the variable regions of the genes. (IV) Resolution of the Holliday junction intermediates leads to a new sequence on the recipient chromosome. doi:10.1128/microbiolspec.MDNA3-0015-2014.f5

Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6

Click to view

FIGURE 6

Proposed antigenic variation initiation pathway. Transcription initiation at the sRNA upstream of melts the DNA allowing the G4 structure to form. An unknown protein likely binds the G4 to stabilize the structure. A single-stranded nick may occur on the strand opposite the G4 due to a stalled replication fork. RecQ could unwind the G4 structure. RecJ resects the 5′ nicked end allowing RecA to mediate recombination, possibly enhanced by binding the G4 structure, with RecOR using regions of homology between and the donor , presumably through a recombination mechanism detailed in Fig. 5 . RecG and RuvABC then process and resolve the recombination intermediate. doi:10.1128/microbiolspec.MDNA3-0015-2014.f6

Source: microbiolspec January 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.MDNA3-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error