Publikationsserver der Universitätsbibliothek Marburg

Titel:Role and visualization of the single-stranded and double-stranded DNA in the biofilm of Neisseria gonorrhoeae
Autor:Zweig, Maria
Weitere Beteiligte: Søgaard-Andersen, Lotte (Prof. MD, PhD)
Veröffentlicht:2013
URI:https://archiv.ub.uni-marburg.de/diss/z2013/0373
DOI: https://doi.org/10.17192/z2013.0373
URN: urn:nbn:de:hebis:04-z2013-03739
DDC: Biowissenschaften, Biologie
Titel (trans.):Rolle und Visualisierung von Einzelstrang- und Doppelstrang-DNAs im Biofilm von Neisseria gonorrhoeae
Publikationsdatum:2013-07-04
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
SSB, Neisseria, SSB, Neisseria, GGI, GGI, Biofilm, Biofilm

Summary:
Neisseria gonorrhoeae, the causative agent of the sexually transmitted disease gonorrhoea, is a Gram-negative human-adapted diplococcus. 80% of the clinical N. gonorrhoeae isolates encode an unusual Type IV secretion system (T4SS) within the horizontally acquired region - the Gonococcal Genetic Island (GGI). Next to the Single Stranded DNA binding protein (SSB) encoded on the chromosome, a second SSB, SsbB, is encoded within the GGI. SSBs are highly conserved, essential proteins found in all kingdoms of life. They bind single stranded DNA (ssDNA) with high affinity, have low sequence specificity and are involved in DNA recombination, DNA replication and DNA repair. A second copy of SSBs can be encoded on the chromosome or on a plasmid. These SSBs can be involved in diverse mechanisms like natural competence, plasmid segregation and DNA transport. We analyzed the physiological role of SsbB and characterized its function biochemically. We found that close homologs of SsbB are located within a conserved genetic cluster found in genetic islands of different proteobacteria. This cluster encodes DNA processing enzymes such as the ParA and ParB partitioning proteins, the TopB topoisomerase and four conserved hypothetical proteins. The SsbB homologs found in these clusters form a family separated from other ssDNA binding proteins. Remarkably, in contrast to most other SSBs, SsbB did not complement the Escherichia coli ssb deletion mutant. Purified SsbB formed a stable tetramer. Electrophoretic mobility shift assays, fluorescence titration assays, as well as atomic force microscopy demonstrated that SsbB binds ssDNA specifically with high affinity. SsbB binds single stranded DNA with minimal binding frames of 15 and 70 nucleotides for one or two SsbB tetramersrespectively. The binding mode was independent of increasing Mg2+ or NaCl concentrations. No role of SsbB in ssDNA secretion or DNA uptake could be identified, but SsbB strongly stimulated Topoisomerase I activity. We propose that these novel SsbBs play an unknown role in the maintenance of genetic islands. Remarkably the T4SS of N.gonorrhoeae was shown to secrete ssDNA directly into the medium. Currently nothing is known about the exact function of the secreted DNA. Studies have shown that not only exopolysaccharides but also extracellular DNA (eDNA) can play an important role in the initial establishment of biofilms. The composition and the origin of the eDNA are not completely understood. N. gonorrhoeae biofilms contain large amounts of extracellular DNA which play an important role in biofilm formation. To study the role of ssDNA in biofilm formation, the development of biofilms of N. gonorrhoeae strain MS11 was compared with a MS11 ΔtraB strain, which is impaired in ssDNA secretion and the MS11 ΔtraB::traB complementation strain in which ssDNA secretion is restored. Furthermore, the role of ssDNA in biofilm formation was studied by treating biofilms with Exonuclease I which specifically degrades ssDNA. These experiments demonstrated that the secreted ssDNA strongly stimulated biofilm formation especially during initial attachment. Furthermore, we developed a unique technique to separately detect ssDNA and dsDNA. To visualize ssDNA, SSB proteins, which specifically bind ssDNA with high affinity in a sequence-independent manner, were employed. The highly stable SSB protein from Thermoanaerobacter tengcongensis, and different cysteine mutants within this protein were purified to homogeneity. The different cysteines containing proteins were labelled with environmentally sensitive fluorescent probes. Specific combinations of cysteine mutants and fluorescent probes were selected to obtain proteins that showed a strongly increased fluorescence upon binding of ssDNA. To visualize dsDNA the thermostable double stranded DNA binding protein Sac7d of Sulfolobus acidocadarius was used. Both proteins were applied to visualize single- and double-stranded DNA in biofilms and planktonic cultures. Remarkably, only dsDNA could be detected in N. gonorrhoeae biofilms using this approach. We conclude that ssDNA plays an important role in biofilm formation, but that the amount of ssDNA necessary is much lower than the amount of dsDNA found in mature biofilms.

Bibliographie / References

  1. Swanson J, Kraus SJ, Gotschlich EC (1971) Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med 134: 886-906.
  2. Pachulec E, van der Does C (2010) Conjugative plasmids of Neisseria gonorrhoeae. PLoS One 5: e9962.
  3. Wei TF, Bujalowski W, Lohman TM (1992) Cooperative binding of polyamines induces the Escherichia coli single-strand binding protein-DNA binding mode transitions. Biochemistry 31: 6166-6174.
  4. Li YH, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG (2001) Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183: 897-908.
  5. Lohman TM, Overman LB (1985) Two binding modes in Escherichia coli single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J Biol Chem 260: 3594-3603.
  6. Shokri L, Rouzina I, Williams MC (2009) Interaction of bacteriophage T4 and T7 single-stranded DNA-binding proteins with DNA. Phys Biol 6: 025002.
  7. Raghunathan S, Kozlov AG, Lohman TM, Waksman G (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat Struct Biol 7: 648-652.
  8. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, et al. (2009) Structure of a type IV secretion system core complex. Science 323: 266-268.
  9. Spence JM, Wright L, Clark VL (2008) Laboratory maintenance of Neisseria gonorrhoeae. Curr Protoc Microbiol Chapter 4: Unit 4A 1.
  10. Grandoso G, Avila P, Cayon A, Hernando MA, Llosa M, et al. (2000) Two active-site tyrosyl residues of protein TrwC act sequentially at the origin of transfer during plasmid R388 conjugation. J Mol Biol 295: 1163-1172.
  11. Hedgethorne K, Webb MR (2012) Fluorescent SSB as a reagentless biosensor for single-stranded DNA. Methods Mol Biol 922: 219-233.
  12. Pohlner J, Halter R, Meyer TF (1987) Neisseria gonorrhoeae IgA protease. Secretion and implications for pathogenesis. Antonie Van Leeuwenhoek 53: 479-484.
  13. Golub EI, Low KB (1986) Derepression of single-stranded DNA-binding protein genes on plasmids derepressed for conjugation, and complementation of an E. coli ssb-mutation by these genes. Mol Gen Genet 204: 410-416.
  14. Olszewski M, Mickiewicz M, Kur J (2008) Two highly thermostable paralogous single-stranded DNA- binding proteins from Thermoanaerobacter tengcongensis. Arch Microbiol 190: 79-87.
  15. van der Meer JR, Ravatn R, Sentchilo V (2001) The clc element of Pseudomonas sp. strain B13 and other mobile degradative elements employing phage-like integrases. Arch Microbiol 175: 79-85.
  16. Jan HC, Lee YL, Huang CY (2011) Characterization of a single-stranded DNA-binding protein from Pseudomonas aeruginosa PAO1. Protein J 30: 20-26.
  17. Bowie JU, Sauer RT (1990) TraY proteins of F and related episomes are members of the Arc and Mnt repressor family. J Mol Biol 211: 5-6.
  18. Moncalian G, de la Cruz F (2004) DNA binding properties of protein TrwA, a possible structural variant of the Arc repressor superfamily. Biochim Biophys Acta 1701: 15-23.
  19. Redfield RJ, Cameron AD, Qian Q, Hinds J, Ali TR, et al. (2005) A novel CRP-dependent regulon controls expression of competence genes in Haemophilus influenzae. J Mol Biol 347: 735-747.
  20. Gelvin SB (2010) Finding a way to the nucleus. Curr Opin Microbiol 13: 53-58.
  21. Bochkarev A, Bochkareva E (2004) From RPA to BRCA2: lessons from single-stranded DNA binding by the OB-fold. Curr Opin Struct Biol 14: 36-42.
  22. Seifert HS, Ajioka R, So M (1988) Alternative model for Neisseria gonorrhoeae pilin variation. Vaccine 6: 107-109.
  23. Smeets LC, Kusters JG (2002) Natural transformation in Helicobacter pylori: DNA transport in an unexpected way. Trends Microbiol 10: 159-162; discussion 162.
  24. Frederico LA, Kunkel TA, Shaw BR (1993) Cytosine deamination in mismatched base pairs. Biochemistry 32: 6523-6530.
  25. Wang BY, Chi B, Kuramitsu HK (2002) Genetic exchange between Treponema denticola and Streptococcus gordonii in biofilms. Oral Microbiol Immunol 17: 108-112.
  26. Merz AJ, Enns CA, So M (1999) Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol Microbiol 32: 1316-1332.
  27. 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.
  28. Robbins JB, Murphy MC, White BA, Mackie RI, Ha T, et al. (2004) Functional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivorans and their effects on DNA synthesis by DNA polymerase BI. J Biol Chem 279: 6315-6326.
  29. Grove DE, Bryant FR (2006) Effect of Mg2+ on the DNA binding modes of the Streptococcus pneumoniae SsbA and SsbB proteins. J Biol Chem 281: 2087-2094.
  30. Hobbs MD, Sakai A, Cox MM (2007) SSB protein limits RecOR binding onto single-stranded DNA. J Biol Chem 282: 11058-11067.
  31. Steichen CT, Shao JQ, Ketterer MR, Apicella MA (2008) Gonococcal cervicitis: a role for biofilm in pathogenesis. J Infect Dis 198: 1856-1861.
  32. Potter AJ, Kidd SP, Edwards JL, Falsetta ML, Apicella MA, et al. (2009) Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells. J Infect Dis 199: 227-235.
  33. Despalins A, Marsit S, Oberto J (2011) Absynte: a web tool to analyze the evolution of orthologous archaeal and bacterial gene clusters. Bioinformatics 27: 2905-2906.
  34. McGee ZA, Stephens DS, Hoffman LH, Schlech WF, 3rd, Horn RG (1983) Mechanisms of mucosal invasion by pathogenic Neisseria. Rev Infect Dis 5 Suppl 4: S708-714.
  35. Wadsworth RI, White MF (2001) Identification and properties of the crenarchaeal single-stranded DNA binding protein from Sulfolobus solfataricus. Nucleic Acids Res 29: 914-920.
  36. Davidsen T, Rodland EA, Lagesen K, Seeberg E, Rognes T, et al. (2004) Biased distribution of DNA uptake sequences towards genome maintenance genes. Nucleic Acids Res 32: 1050-1058.
  37. Yakovchuk P, Protozanova E, Frank-Kamenetskii MD (2006) Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res 34: 564-574.
  38. Hamon L, Pastre D, Dupaigne P, Le Breton C, Le Cam E, et al. (2007) High-resolution AFM imaging of single-stranded DNA-binding (SSB) protein--DNA complexes. Nucleic Acids Res 35: e58. References 118
  39. Virji M, Everson JS, Lambden PR (1982) Effect of anti-pilus antisera on virulence of variants of Neisseria gonorrhoeae for cultured epithelial cells. J Gen Microbiol 128: 1095-1100.
  40. Chapman SJ, Perkins HR (1983) Peptidoglycan-degrading enzymes in ether-treated cells of Neisseria gonorrhoeae. J Gen Microbiol 129: 877-883.
  41. Virji M, Heckels JE (1984) The role of common and type-specific pilus antigenic domains in adhesion and virulence of gonococci for human epithelial cells. J Gen Microbiol 130: 1089-1095.
  42. de Vries J, Wackernagel W (1994) Cloning and sequencing of the Proteus mirabilis gene for a single- stranded DNA-binding protein (SSB) and complementation of Escherichia coli ssb point and deletion mutations. Microbiology 140 ( Pt 4): 889-895.
  43. Philipova D, Mullen JR, Maniar HS, Lu J, Gu C, et al. (1996) A hierarchy of SSB protomers in replication protein A. Genes Dev 10: 2222-2233.
  44. Griffith JD, Harris LD, Register J, 3rd (1984) Visualization of SSB-ssDNA complexes active in the assembly of stable RecA-DNA filaments. Cold Spring Harb Symp Quant Biol 49: 553-559.
  45. Savvides SN, Raghunathan S, Futterer K, Kozlov AG, Lohman TM, et al. (2004) The C-terminal domain of full-length E. coli SSB is disordered even when bound to DNA. Protein Sci 13: 1942-1947.
  46. Hamilton HL, Dillard JP (2006) Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 59: 376-385.
  47. Lappann M, Haagensen JA, Claus H, Vogel U, Molin S (2006) Meningococcal biofilm formation: structure, development and phenotypes in a standardized continuous flow system. Mol Microbiol 62: 1292-1309.
  48. Ragonese H, Haisch D, Villareal E, Choi JH, Matson SW (2007) The F plasmid-encoded TraM protein stimulates relaxosome-mediated cleavage at oriT through an interaction with TraI. Mol Microbiol 63: 1173-1184.
  49. Mulcahy H, Charron-Mazenod L, Lewenza S (2010) Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ Microbiol 12: 1621-1629.
  50. Bockelmann U, Janke A, Kuhn R, Neu TR, Wecke J, et al. (2006) Bacterial extracellular DNA forming a defined network-like structure. FEMS Microbiol Lett 262: 31-38.
  51. Fernandez-Lopez R, Garcillan-Barcia MP, Revilla C, Lazaro M, Vielva L, et al. (2006) Dynamics of the IncW genetic backbone imply general trends in conjugative plasmid evolution. FEMS Microbiol Rev 30: 942-966.
  52. Pestryakov PE, Lavrik OI (2008) Mechanisms of single-stranded DNA-binding protein functioning in cellular DNA metabolism. Biochemistry (Mosc) 73: 1388-1404.
  53. Annear DI, Wild B (1982) Growth of Neisseria gonorrhoeae in brain heart infusion. J Clin Pathol 35: 119.
  54. Carney FE, Jr., Taylor-Robinson D (1973) Growth and effect of Neisseria gonorrhoeae in organ cultures. Br J Vener Dis 49: 435-440.
  55. Dillingham MS, Tibbles KL, Hunter JL, Bell JC, Kowalczykowski SC, et al. (2008) Fluorescent single- stranded DNA binding protein as a probe for sensitive, real-time assays of helicase activity. Biophys J 95: 3330-3339.
  56. Morse SA, Bartenstein L (1974) Factors affecting autolysis of Neisseria gonorrhoeae. Proc Soc Exp Biol Med 145: 1418-1421.
  57. Fuxman Bass JI, Russo DM, Gabelloni ML, Geffner JR, Giordano M, et al. (2010) Extracellular DNA: a major proinflammatory component of Pseudomonas aeruginosa biofilms. J Immunol 184: 6386- 6395.
  58. Seubert A, Hiestand R, de la Cruz F, Dehio C (2003) A bacterial conjugation machinery recruited for pathogenesis. Mol Microbiol 49: 1253-1266.
  59. Snyder LA, Jarvis SA, Saunders NJ (2005) Complete and variant forms of the 'gonococcal genetic island' in Neisseria meningitidis. Microbiology 151: 4005-4013.
  60. Larbig KD, Christmann A, Johann A, Klockgether J, Hartsch T, et al. (2002) Gene islands integrated into tRNA(Gly) genes confer genome diversity on a Pseudomonas aeruginosa clone. J Bacteriol 184: 6665-6680.
  61. Kerr ID, Wadsworth RI, Blankenfeldt W, Staines AG, White MF, et al. (2001) Overexpression, purification, crystallization and data collection of a single-stranded DNA-binding protein from Sulfolobus solfataricus. Acta Crystallogr D Biol Crystallogr 57: 1290-1292.
  62. Seib KL, Wu HJ, Srikhanta YN, Edwards JL, Falsetta ML, et al. (2007) Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol Microbiol 63: 54-68.
  63. Francia MV, Varsaki A, Garcillan-Barcia MP, Latorre A, Drainas C, et al. (2004) A classification scheme for mobilization regions of bacterial plasmids. FEMS Microbiol Rev 28: 79-100.
  64. Garcillan-Barcia MP, Francia MV, de la Cruz F (2009) The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33: 657-687.
  65. Smillie C, Garcillan-Barcia MP, Francia MV, Rocha EP, de la Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74: 434-452.
  66. Varsaki A, Moncalian G, Garcillan-Barcia Mdel P, Drainas C, de la Cruz F (2009) Analysis of ColE1 MbeC unveils an extended ribbon-helix-helix family of nicking accessory proteins. J Bacteriol 191: 1446-1455.
  67. Arechaga I, Pena A, Zunzunegui S, del Carmen Fernandez-Alonso M, Rivas G, et al. (2008) ATPase activity and oligomeric state of TrwK, the VirB4 homologue of the plasmid R388 type IV secretion system. J Bacteriol 190: 5472-5479.
  68. Llosa M, Gomis-Ruth FX, Coll M, de la Cruz Fd F (2002) Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 45: 1-8.
  69. Llosa M, Roy C, Dehio C (2009) Bacterial type IV secretion systems in human disease. Mol Microbiol 73: 141-151.
  70. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
  71. Guglielmini J, Quintais L, Garcillan-Barcia MP, de la Cruz F, Rocha EP (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7: e1002222.
  72. Schroder G, Lanka E (2005) The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid 54: 1-25.
  73. Donlan RM (2000) Role of biofilms in antimicrobial resistance. ASAIO J 46: S47-52.
  74. Seifert HS (1992) Molecular mechanisms of antigenic variation in Neisseria gonorrhoeae. Mol Cell Biol Hum Dis Ser 1: 1-22.
  75. Wade JJ, Graver MA (2007) A fully defined, clear and protein-free liquid medium permitting dense growth of Neisseria gonorrhoeae from very low inocula. FEMS Microbiol Lett 273: 35-37.
  76. Dillard JP, Seifert HS (1997) A peptidoglycan hydrolase similar to bacteriophage endolysins acts as an autolysin in Neisseria gonorrhoeae. Mol Microbiol 25: 893-901.
  77. Fischer W (2011) Assembly and molecular mode of action of the Helicobacter pylori Cag type IV secretion apparatus. FEBS J 278: 1203-1212.
  78. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
  79. Christie PJ, Vogel JP (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8: 354-360.
  80. Suck D (1997) Common fold, common function, common origin? Nat Struct Biol 4: 161-165.
  81. Pansegrau W, Ziegelin G, Lanka E (1990) Covalent association of the traI gene product of plasmid RP4 with the 5'-terminal nucleotide at the relaxation nick site. J Biol Chem 265: 10637-10644.
  82. Ferretti JJ, Dyer DW, Roe BA (1997) Data available. Nature 386: 320.
  83. Gubish ER, Jr., Chen KC, Buchanan TM (1982) Detection of a gonococcal endo-beta-N-acetyl-D- glucosaminidase and its peptidoglycan cleavage site. J Bacteriol 151: 172-176.
  84. Grove DE, Willcox S, Griffith JD, Bryant FR (2005) Differential single-stranded DNA binding properties of the paralogous SsbA and SsbB proteins from Streptococcus pneumoniae. J Biol Chem 280: 11067-11073.
  85. Potter AJ, Kidd SP, Edwards JL, Falsetta ML, Apicella MA, et al. (2009) Esterase D is essential for protection of Neisseria gonorrhoeae against nitrosative stress and for bacterial growth during interaction with cervical epithelial cells. J Infect Dis 200: 273-278.
  86. Lawley TD, Klimke WA, Gubbins MJ, Frost LS (2003) F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 224: 1-15.
  87. Dabrowski S, Olszewski M, Piatek R, Brillowska-Dabrowska A, Konopa G, et al. (2002) Identification and characterization of single-stranded-DNA-binding proteins from Thermus thermophilus and Thermus aquaticus -new arrangement of binding domains. Microbiology 148: 3307-3315.
  88. Bujalowski W, Lohman TM (1989) Negative co-operativity in Escherichia coli single strand binding protein-oligonucleotide interactions. I. Evidence and a quantitative model. J Mol Biol 207: 249- 268.
  89. 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.
  90. Hagen TA, Cornelissen CN (2006) Neisseria gonorrhoeae requires expression of TonB and the putative transporter TdfF to replicate within cervical epithelial cells. Mol Microbiol 62: 1144- 1157.
  91. Chedin F, Seitz EM, Kowalczykowski SC (1998) Novel homologs of replication protein A in archaea: implications for the evolution of ssDNA-binding proteins. Trends Biochem Sci 23: 273-277.
  92. Citovsky V, Zupan J, Warnick D, Zambryski P (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256: 1802-1805.
  93. Murzin AG (1993) OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J 12: 861-867.
  94. McGee ZA, Gorby GL, Wyrick PB, Hodinka R, Hoffman LH (1988) Parasite-directed endocytosis. Rev Infect Dis 10 Suppl 2: S311-316.
  95. Hacker J, Kaper JB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679.
  96. Merrill BM, Williams KR, Chase JW, Konigsberg WH (1984) Photochemical cross-linking of the Escherichia coli single-stranded DNA-binding protein to oligodeoxynucleotides. Identification of phenylalanine 60 as the site of cross-linking. J Biol Chem 259: 10850-10856.
  97. Wold MS, Kelly T (1988) Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc Natl Acad Sci U S A 85: 2523-2527.
  98. Smith H, Parsons NJ, Cole JA (1995) Sialylation of neisserial lipopolysaccharide: a major influence on pathogenicity. Microb Pathog 19: 365-377.
  99. Benam AV, Lang E, Alfsnes K, Fleckenstein B, Rowe AD, et al. (2011) Structure-function relationships of the competence lipoprotein ComL and SSB in meningococcal transformation. Microbiology 157: 1329-1342.
  100. Brock TD, Brock KM, Belly RT, Weiss RL (1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 84: 54-68.
  101. Cha TA, Alberts BM (1989) The bacteriophage T4 DNA replication fork. Only DNA helicase is required for leading strand DNA synthesis by the DNA polymerase holoenzyme. J Biol Chem 264: 12220- 12225.
  102. Cannon JG, Sparling PF (1984) The genetics of the gonococcus. Annu Rev Microbiol 38: 111-133.
  103. Wu Z, Xu L, Tu Y, Chen R, Yu Y, et al. (2011) The relationship between the symptoms of female gonococcal infections and serum progesterone level and the genotypes of Neisseria gonorrhoeae multi-antigen sequence type (NG-MAST) in Wuhan, China. Eur J Clin Microbiol Infect Dis 30: 113-116.
  104. Schwarz G, Watanabe F (1983) Thermodynamics and kinetics of co-operative protein-nucleic acid binding. I. General aspects of analysis of data. J Mol Biol 163: 467-484.
  105. Porter RD, Black S (1991) The single-stranded-DNA-binding protein encoded by the Escherichia coli F factor can complement a deletion of the chromosomal ssb gene. J Bacteriol 173: 2720-2723.
  106. Bycroft M, Hubbard TJ, Proctor M, Freund SM, Murzin AG (1997) The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88: 235-242.
  107. Falsetta ML, Bair TB, Ku SC, Vanden Hoven RN, Steichen CT, et al. (2009) Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms. Infect Immun 77: 3522-3532.
  108. Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2: 114-122.
  109. Sundberg C, Meek L, Carroll K, Das A, Ream W (1996) VirE1 protein mediates export of the single- stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J Bacteriol 178: 1207-1212.
  110. Guglielmini J, de la Cruz F, Rocha EP (2013) Evolution of Conjugation and Type IV Secretion Systems. Mol Biol Evol 30: 315-331.
  111. Hendrickx L, Hausner M, Wuertz S (2003) Natural genetic transformation in monoculture Acinetobacter sp. strain BD413 biofilms. Appl Environ Microbiol 69: 1721-1727.
  112. Richards JJ, Melander C (2009) Controlling bacterial biofilms. Chembiochem 10: 2287-2294.
  113. O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
  114. 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.
  115. Gerbase AC, Rowley JT, Mertens TE (1998) Global epidemiology of sexually transmitted diseases. Lancet 351 Suppl 3: 2-4.
  116. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, et al. (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59: 1114-1128.
  117. Lappann M, Claus H, van Alen T, Harmsen M, Elias J, et al. (2010) A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol Microbiol 75: 1355-1371.
  118. Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, et al. (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153: 2083-2092.
  119. Szczepankowska AK, Prestel E, Mariadassou M, Bardowski JK, Bidnenko E (2011) Phylogenetic and complementation analysis of a single-stranded DNA binding protein family from lactococcal phages indicates a non-bacterial origin. PLoS One 6: e26942.
  120. McAfee JG, Edmondson SP, Zegar I, Shriver JW (1996) Equilibrium DNA binding of Sac7d protein from the hyperthermophile Sulfolobus acidocaldarius: fluorescence and circular dichroism studies. Biochemistry 35: 4034-4045.
  121. Sikder D, Unniraman S, Bhaduri T, Nagaraja V (2001) Functional cooperation between topoisomerase I and single strand DNA-binding protein. J Mol Biol 306: 669-679.
  122. Acharya N, Varshney U (2002) Biochemical properties of single-stranded DNA-binding protein from Mycobacterium smegmatis, a fast-growing mycobacterium and its physical and functional interaction with uracil DNA glycosylases. J Mol Biol 318: 1251-1264.
  123. Purnapatre K, Varshney U (1999) Cloning, over-expression and biochemical characterization of the single-stranded DNA binding protein from Mycobacterium tuberculosis. Eur J Biochem 264: 591- 598.
  124. Wold MS (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66: 61-92.
  125. Lohman TM, Ferrari ME (1994) Escherichia coli single-stranded DNA-binding protein: multiple DNA- binding modes and cooperativities. Annu Rev Biochem 63: 527-570.
  126. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
  127. Finkel SE, Kolter R (2001) DNA as a nutrient: novel role for bacterial competence gene homologs. J Bacteriol 183: 6288-6293.
  128. Greiner LL, Edwards JL, Shao J, Rabinak C, Entz D, et al. (2005) Biofilm Formation by Neisseria gonorrhoeae. Infect Immun 73: 1964-1970.
  129. Steinberger RE, Holden PA (2005) Extracellular DNA in single-and multiple-species unsaturated biofilms. Appl Environ Microbiol 71: 5404-5410.
  130. Lynch EC, Blake MS, Gotschlich EC, Mauro A (1984) Studies of Porins: Spontaneously Transferred from Whole Cells and Reconstituted from Purified Proteins of Neisseria gonorrhoeae and Neisseria meningitidis. Biophys J 45: 104-107.
  131. Theobald DL, Mitton-Fry RM, Wuttke DS (2003) Nucleic acid recognition by OB-fold proteins. Annu Rev Biophys Biomol Struct 32: 115-133.
  132. Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67: 277-301, table of contents.
  133. Kerr ID, Wadsworth RI, Cubeddu L, Blankenfeldt W, Naismith JH, et al. (2003) Insights into ssDNA recognition by the OB fold from a structural and thermodynamic study of Sulfolobus SSB protein. EMBO J 22: 2561-2570.
  134. Krause S, Barcena M, Pansegrau W, Lurz R, Carazo JM, et al. (2000) Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc Natl Acad Sci U S A 97: 3067- 3072.
  135. Moscoso M, Garcia E, Lopez R (2006) Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 188: 7785-7795.
  136. Bos MP, Grunert F, Belland RJ (1997) Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect Immun 65: 2353-2361.
  137. Kerle KK, Mascola JR, Miller TA (1992) Disseminated gonococcal infection. Am Fam Physician 45: 209- 214.
  138. Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, et al. (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A 104: 8113-8118.
  139. Jurcisek JA, Bakaletz LO (2007) Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 189: 3868-3875.
  140. Kohler PL, Hamilton HL, Cloud-Hansen K, Dillard JP (2007) AtlA functions as a peptidoglycan lytic transglycosylase in the Neisseria gonorrhoeae type IV secretion system. J Bacteriol 189: 5421- 5428.
  141. Johnson AP, Clark JB, Osborn MF, Taylor-Robinson D (1980) A comparison of the association of Neisseria gonorrhoeae with human and guinea-pig genital mucosa maintained in organ culture. Br J Exp Pathol 61: 521-527.
  142. Howland CJ, Rees CE, Barth PT, Wilkins BM (1989) The ssb gene of plasmid ColIb-P9. J Bacteriol 171: 2466-2473.
  143. Kado CI, Liu ST (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145: 1365-1373.
  144. Golub EI, Low KB (1985) Conjugative plasmids of enteric bacteria from many different incompatibility groups have similar genes for single-stranded DNA-binding proteins. J Bacteriol 162: 235-241.
  145. Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74: 470-476.
  146. Grange W, Duckely M, Husale S, Jacob S, Engel A, et al. (2008) VirE2: a unique ssDNA-compacting molecular machine. PLoS Biol 6: e44.
  147. Elmros T, Burman LG, Bloom GD (1976) Autolysis of Neisseria gonorrhoeae. J Bacteriol 126: 969-976.
  148. Biswas GD, Sox T, Blackman E, Sparling PF (1977) Factors affecting genetic transformation of Neisseria gonorrhoeae. J Bacteriol 129: 983-992.
  149. Lim KH, Jones CE, vanden Hoven RN, Edwards JL, Falsetta ML, et al. (2008) Metal binding specificity of the MntABC permease of Neisseria gonorrhoeae and its influence on bacterial growth and interaction with cervical epithelial cells. Infect Immun 76: 3569-3576.
  150. Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190: 5690-5698.
  151. Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4: e1000213. References 119
  152. Salgado-Pabon 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.
  153. Vilain S, Pretorius JM, Theron J, Brozel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75: 2861-2868.
  154. Juhas M, Crook DW, Hood DW (2008) Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 10: 2377-2386.
  155. Izano EA, Shah SM, Kaplan JB (2009) Intercellular adhesion and biocide resistance in nontypeable Haemophilus influenzae biofilms. Microb Pathog 46: 207-213.
  156. Short HB, Clark VL, Kellogg DS, Jr., Young FE (1982) Anaerobic survival of clinical isolates and laboratory strains of Neisseria gonorrhoea: use in transfer and storage. J Clin Microbiol 15: 915- 919.
  157. Carnoy C, Roten CA (2009) The dif/Xer recombination systems in proteobacteria. PLoS One 4: e6531.
  158. Sparling PF (1966) Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J Bacteriol 92: 1364-1371.
  159. Alvarez-Martinez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
  160. 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.
  161. Harmsen M, Lappann M, Knochel S, Molin S (2010) Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 76: 2271-2279.
  162. Falsetta ML, McEwan AG, Jennings MP, Apicella MA (2010) Anaerobic metabolism occurs in the substratum of gonococcal biofilms and may be sustained in part by nitric oxide. Infect Immun 78: 2320-2328.
  163. Das T, Sharma PK, Busscher HJ, van der Mei HC, Krom BP (2010) Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microbiol 76: 3405-3408.
  164. 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.
  165. Higashi DL, Zhang GH, Biais N, Myers LR, Weyand NJ, et al. (2009) Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex. Microbiology 155: 4084- 4092.
  166. Koerdt A, Godeke J, Berger J, Thormann KM, Albers SV (2010) Crenarchaeal biofilm formation under extreme conditions. PLoS One 5: e14104.
  167. Jain S, Moscicka KB, Bos MP, Pachulec E, Stuart MC, et al. Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria. PLoS One 6: e16624.
  168. Conover MS, Mishra M, Deora R (2011) Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS One 6: e16861.
  169. Schelert J, Dixit V, Hoang V, Simbahan J, Drozda M, et al. (2004) Occurrence and characterization of mercury resistance in the hyperthermophilic archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186: 427-437.
  170. Steichen CT, Cho C, Shao JQ, Apicella MA (2011) The Neisseria gonorrhoeae biofilm matrix contains DNA, and an endogenous nuclease controls its incorporation. Infect Immun 79: 1504-1511.
  171. Ramsey ME, Woodhams KL, Dillard JP (2011) The Gonococcal Genetic Island and Type IV Secretion in the Pathogenic Neisseria. Front Microbiol 2: 61.
  172. Jain S, Kahnt J, van der Does C (2011) Processing and maturation of the pilin of the type IV secretion system encoded within the gonococcal genetic island. J Biol Chem 286: 43601-43610.
  173. Jain S, Zweig M, Peeters E, Siewering K, Hackett KT, et al. (2012) Characterization of the single stranded DNA binding protein SsbB encoded in the Gonoccocal Genetic Island. PLoS One 7: e35285.
  174. 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.
  175. Lindner C, Nijland R, van Hartskamp M, Bron S, Hamoen LW, et al. (2004) Differential expression of two paralogous genes of Bacillus subtilis encoding single-stranded DNA binding protein. J Bacteriol 186: 1097-1105.
  176. Virji M, Everson JS (1981) Comparative virulence of opacity variants of Neisseria gonorrhoeae strain P9. Infect Immun 31: 965-970.
  177. Stephens DS (1989) Gonococcal and meningococcal pathogenesis as defined by human cell, cell culture, and organ culture assays. Clin Microbiol Rev 2 Suppl: S104-111.
  178. Atmakuri K, Cascales E, Christie PJ (2004) Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54: 1199- 1211.
  179. Fronzes R, Christie PJ, Waksman G (2009) The structural biology of type IV secretion systems. Nat Rev Microbiol 7: 703-714.
  180. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E (2005) Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59: 451-485.
  181. van Putten JP (1993) Phase variation of lipopolysaccharide directs interconversion of invasive and immuno-resistant phenotypes of Neisseria gonorrhoeae. EMBO J 12: 4043-4051.
  182. McGee ZA, Johnson AP, Taylor-Robinson D (1976) Human fallopian tubes in organ culture: preparation, maintenance, and quantitation of damage by pathogenic microorganisms. Infect Immun 13: 608-618.
  183. Fairman MP, Stillman B (1988) Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J 7: 1211-1218.
  184. Umezu K, Chi NW, Kolodner RD (1993) Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc Natl Acad Sci U S A 90: 3875-3879.
  185. Smith JM, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci U S A 90: 4384-4388.
  186. Kim YT, Richardson CC (1993) Bacteriophage T7 gene 2.5 protein: an essential protein for DNA replication. Proc Natl Acad Sci U S A 90: 10173-10177.
  187. Edwards JL, Apicella MA (2004) The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin Microbiol Rev 17: 965-981, table of contents.
  188. Hamilton HL, Schwartz KJ, Dillard JP (2001) Insertion-duplication mutagenesis of neisseria: use in characterization of DNA transfer genes in the gonococcal genetic island. J Bacteriol 183: 4718- 4726.
  189. Chrysogelos S, Griffith J (1982) Escherichia coli single-strand binding protein organizes single- stranded DNA in nucleosome-like units. Proc Natl Acad Sci U S A 79: 5803-5807.
  190. Pansegrau W, Schroder W, Lanka E (1993) Relaxase (TraI) of IncP alpha plasmid RP4 catalyzes a site- specific cleaving-joining reaction of single-stranded DNA. Proc Natl Acad Sci U S A 90: 2925- 2929.
  191. Heilmann C, Hussain M, Peters G, Gotz F (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24: 1013- 1024.
  192. Lohman TM, Overman LB, Datta S (1986) Salt-dependent changes in the DNA binding co-operativity of Escherichia coli single strand binding protein. J Mol Biol 187: 603-615.
  193. Miroux B, Walker JE (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260: 289- 298.
  194. Olszewski M, Grot A, Wojciechowski M, Nowak M, Mickiewicz M, et al. (2010) Characterization of exceptionally thermostable single-stranded DNA-binding proteins from Thermotoga maritima and Thermotoga neapolitana. BMC Microbiol 10: 260.
  195. Hall-Stoodley L, Nistico L, Sambanthamoorthy K, Dice B, Nguyen D, et al. (2008) Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol 8: 173.


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