The DNA-Uptake Process of Naturally Competent Vibrio cholerae

Trends in Microbiology

Volumn 24, Issue 2, 2016, Pages 98-110

  Matthey, Noémie ^a   Blokesch, Melanie ^a  

^a EPFL   (Switzerland)

Author keywords

Brownian ratchet; DNA translocation; Nanomachine; Natural competence; Transformation; Type IV pilus

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; CHITIN; DNA BINDING PROTEIN; PROTEIN COMEA; PROTEIN COMF; UNCLASSIFIED DRUG;

BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; DNA BINDING; DNA STRAND; DNA TRANSFER; GENE TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; VIBRIO CHOLERAE; BACTERIUM TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BACTERIAL PROTEINS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; TRANSFORMATION, BACTERIAL; VIBRIO CHOLERAE;

EID: 84959108621     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.10.008     Document Type: Review

References (104)

1. Lipp E.K., et al. Effects of global climate on infectious disease: the cholera model. Clin. Microbiol. Rev. 2002, 15:757-770.
2. Heidelberg J.F., et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 2000, 406:477-483.
3. Chun J., et al. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15442-15447.
4. Karaolis D.K.R., et al. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 1999, 399:375-379.
5. Waldor M.K., Mekalanos J.J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996, 272:1910-1914.
6. Faruque S.M., et al. Examination of diverse toxin-coregulated pilus-positive Vibrio cholerae strains fails to demonstrate evidence for Vibrio pathogenicity island phage. Infect. Immun. 2003, 71:2993-2999.
7. Davis B.M., Waldor M.K. Filamentous phages linked to virulence of Vibrio cholerae. Curr. Opin. Microbiol. 2003, 6:35-42.
8. Meibom K.L., et al. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2524-2529.
9. Fullner K.J., Mekalanos J.J. Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect. Immun. 1999, 67:1393-1404.
10. Meibom K.L., Blokesch M., et al. Chitin induces natural competence in Vibrio cholerae. Science 2005, 310:1824-1827.
11. Johnston C., et al. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat. Rev. Microbiol. 2014, 12:181-196.
12. Borgeaud S., et al. The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 2015, 347:63-67.
13. Russell A.B., et al. Type VI secretion system effectors: poisons with a purpose. Nat. Rev. Microbiol. 2014, 12:137-148.
14. Ho B.T., et al. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 2014, 15:9-21.
15. Claverys J.P., Havarstein L.S. Cannibalism and fratricide: mechanisms and raisons d'etre. Nat. Rev. Microbiol. 2007, 5:219-229.
16. Blokesch M., Schoolnik G.K. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog. 2007, 3:e81.
17. Shapiro B.J., et al. Population genomics of early events in the ecological differentiation of bacteria. Science 2012, 336:48-51.
18. Redfield R.J. Do bacteria have sex?. Nat. Rev. Genet. 2001, 2:634-639.
19. Vos M. Why do bacteria engage in homologous recombination?. Trends Microbiol. 2009, 17:226-232.
20. Seitz P., Blokesch M. Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental Gram-negative bacteria. FEMS Microbiol. Rev. 2013, 37:336-363.
21. Utnes A.L., et al. Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi. ISME J. 2015, 9:2221-2231.
22. Chen I., Dubnau D. DNA uptake during bacterial transformation. Nat. Rev. Microbiol. 2004, 2:241-249.
23. Suckow G., et al. Quorum sensing contributes to natural transformation of Vibrio cholerae in a species-specific manner. J. Bacteriol. 2011, 193:4914-4924.
24. Lo Scrudato M., Blokesch M. The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet. 2012, 8:e1002778.
25. Korotkov K.V., et al. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol. 2012, 10:336-351.
26. Nivaskumar M., Francetic O. Type II secretion system: a magic beanstalk or a protein escalator. Biochim. Biophys. Acta 2014, 1843:1568-1577.
27. Costa T.R., et al. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 2015, 13:343-359.
28. Thanassi D.G., et al. Surface organelles assembled by secretion systems of Gram-negative bacteria: diversity in structure and function. FEMS Microbiol. Rev. 2012, 36:1046-1082.
29. Berry J.L., Pelicic V. Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiol. Rev. 2015, 39:134-154.
30. Burton B., Dubnau D. Membrane-associated DNA transport machines. Cold Spring Harb. Perspect. Biol. 2010, 2:a000406.
31. Johnston C., et al. Streptococcus pneumoniae, le transformiste. Trends Microbiol. 2014, 22:113-119.
32. Seitz P., Blokesch M. DNA-uptake machinery of naturally competent Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:17987-17992.
33. Seitz P., Blokesch M. DNA transport across the outer and inner membranes of naturally transformable Vibrio cholerae is spatially but not temporally coupled. MBio 2014, 5. e01409-14.
34. Seitz P., et al. ComEA is essential for the transfer of external DNA into the periplasm in naturally transformable Vibrio cholerae cells. PLoS Genet. 2014, 10:e1004066.
35. Pugsley A.P. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 1993, 57:50-108.
36. Gold V.A., et al. Structure of a type IV pilus machinery in the open and closed state. eLife 2015, 4:e07380.
37. Salzer R., et al. Environmental factors affecting the expression of type IV pilus genes as well as piliation of Thermus thermophilus. FEMS Microbiol. Lett. 2014, 357:56-62.
38. Melville S., Craig L. Type IV pili in Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 2013, 77:323-341.
39. Balaban M., et al. Secretion of a pneumococcal type II secretion system pilus correlates with DNA uptake during transformation. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E758-E765.
40. Laurenceau R., et al. A type IV pilus mediates dna binding during natural transformation in Streptococcus pneumoniae. PLoS Pathog. 2013, 9:e1003473.
41. Muschiol S., et al. Uptake of extracellular DNA: competence induced pili in natural transformation of Streptococcus pneumoniae. Bioessays 2015, 37:426-435.
42. Laurenceau R., et al. Conserved Streptococcus pneumoniae spirosomes suggest a single type of transformation pilus in competence. PLoS Pathog. 2015, 11:e1004835.
43. Roux N., et al. Neglected but amazingly diverse type IVb pili. Res. Microbiol. 2012, 163:659-673.
44. Burrows L.L. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu. Rev. Microbiol. 2012, 66:493-520.
45. Wolfgang M., et al. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J. 2000, 19:6408-6418.
46. Collins R.F., et al. Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy. J. Bacteriol. 2003, 185:2611-2617.
47. Collins R.F., et al. Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ. J. Biol. Chem. 2005, 280:18923-18930.
48. Berry J.L., et al. Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS Pathog. 2012, 8:e1002923.
49. Burkhardt J., et al. Unusual N-terminal alphaalphabetaalphabetabetaalpha fold of PilQ from Thermus thermophilus mediates ring formation and is essential for piliation. J. Biol. Chem. 2012, 287:8484-8494.
50. Burkhardt J., et al. Structure and function of PilQ, a secretin of the DNA transporter from the thermophilic bacterium Thermus thermophilus HB27. J. Biol. Chem. 2011, 286:9977-9984.
51. Cehovin A., et al. Specific DNA recognition mediated by a type IV pilin. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:3065-3070.
52. Wolfgang M., et al. The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol. Microbiol. 1999, 31:1345-1357.
53. Draskovic I., Dubnau D. Biogenesis of a putative channel protein, ComEC, required for DNA uptake: membrane topology, oligomerization and formation of disulphide bonds. Mol. Microbiol. 2005, 55:881-896.
54. Stingl K., et al. Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1184-1189.
55. Hofreuter D., et al. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 2001, 41:379-391.
56. Altschul S.F., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
57. Londono-Vallejo J.A., Dubnau D. comF, a Bacillus subtilis late competence locus, encodes a protein similar to ATP-dependent RNA/DNA helicases. Mol. Microbiol. 1993, 9:119-131.
58. Sysoeva T.A., et al. Structural characterization of the late competence protein ComFB from Bacillus subtilis. Biosci. Rep. 2015, 35:e00183.
59. Londono-Vallejo J.A., Dubnau D. Mutation of the putative nucleotide binding site of the Bacillus subtilis membrane protein ComFA abolishes the uptake of DNA during transformation. J. Bacteriol. 1994, 176:4642-4645.
60. Londono-Vallejo J.A., Dubnau D. Membrane association and role in DNA uptake of the Bacillus subtilis PriA analogue ComF1. Mol. Microbiol. 1994, 13:197-205.
61. Chao M.C., et al. High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model-based analyses of transposon-insertion sequencing data. Nucleic Acids Res. 2013, 41:9033-9048.
62. Kamp H.D., et al. Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. PLoS Pathog. 2013, 9:e1003800.
63. Kline K.A., Seifert H.S. Mutation of the priA gene of Neisseria gonorrhoeae affects DNA transformation and DNA repair. J. Bacteriol. 2005, 187:5347-5355.
64. Lee M.S., Marians K.J. Differential ATP requirements distinguish the DNA translocation and DNA unwinding activities of the Escherichia coli PRI A protein. J. Biol. Chem. 1990, 265:17078-17083.
65. Barany F., et al. Directional transport and integration of donor DNA in Haemophilus influenzae transformation. Proc. Natl. Acad. Sci. U.S.A. 1983, 80:7274-7278.
66. Berge M., et al. Transformation of Streptococcus pneumoniae relies on DprA- and RecA-dependent protection of incoming DNA single strands. Mol. Microbiol. 2003, 50:527-536.
67. Mortier-Barriere I., et al. A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 2007, 130:824-836.
68. Inamine G.S., Dubnau D. ComEA, a Bacillus subtilis integral membrane protein required for genetic transformation, is needed for both DNA binding and transport. J. Bacteriol. 1995, 177:3045-3051.
69. Provvedi R., Dubnau D. ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Mol. Microbiol. 1999, 31:271-280.
70. Berge M., et al. Uptake of transforming DNA in Gram-positive bacteria: a view from Streptococcus pneumoniae. Mol. Microbiol. 2002, 45:411-421.
71. Doherty A.J., et al. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res. 1996, 24:2488-2497.
72. Chen I., Gotschlich E.C. ComE, a competence protein from Neisseria gonorrhoeae with DNA-binding activity. J. Bacteriol. 2001, 183:3160-3168.
73. Steinbock L.J., et al. Probing the size of proteins with glass nanopores. Nanoscale 2014, 6:14380-14387.
74. Krüger N.J., Stingl K. Two steps away from novelty-principles of bacterial DNA uptake. Mol. Microbiol. 2011, 80:860-867.
75. Gangel H., et al. Concerted spatio-temporal dynamics of imported DNA and ComE DNA uptake protein during gonococcal transformation. PLoS Pathog. 2014, 10:e1004043.
76. Ambjörnsson T., Metzler R. Chaperone-assisted translocation. Phys. Biol. 2004, 1:77-88.
77. Maier B., et al. DNA transport into Bacillus subtilis requires proton motive force to generate large molecular forces. Nat. Struct. Mol. Biol. 2004, 11:643-649.
78. Berge M.J., et al. Midcell recruitment of the DNA uptake and virulence nuclease, EndA, for pneumococcal transformation. PLoS Pathog. 2013, 9:e1003596.
79. Hahn J., et al. Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 2005, 122:59-71.
80. Kidane D., Graumann P.L. Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 2005, 122:73-84.
81. Metzger L.C., Blokesch M. Composition of the DNA-uptake complex of Vibrio cholerae. Mob. Genet. Elements 2014, 4:e28142.
82. Salzer R., et al. Zinc and ATP binding of the hexameric AAA-ATPase PilF from Thermus thermophilus: role in complex stability, piliation, adhesion, twitching motility, and natural transformation. J. Biol. Chem. 2014, 289:30343-30354.
83. Durand E., et al. Biogenesis and structure of a type VI secretion membrane core complex. Nature 2015, 523:555-560.
84. Fussenegger M., et al. Transformation competence and type-4 pilus biogenesis in Neisseria gonorrhoeae - a review. Gene 1997, 192:125-134.
85. Sparling P.F. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J. Bacteriol. 1966, 92:1364-1371.
86. Redfield R.J. sxy-1, a Haemophilus influenzae mutation causing greatly enhanced spontaneous competence. J. Bacteriol. 1991, 173:5612-5618.
87. Lorenz M.G., Wackernagel W. High frequency of natural genetic transformation of Pseudomonas stutzeri in soil extract supplemented with a carbon/energy and phosphorus source. Appl. Environ. Microbiol. 1991, 57:1246-1251.
88. Blokesch M., Schoolnik G.K. The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J. Bacteriol. 2008, 190:7232-7240.
89. Yamamoto S., et al. Identification of a chitin-induced small RNA that regulates translation of the tfoX gene, encoding a positive regulator of natural competence in Vibrio cholerae. J. Bacteriol. 2011, 193:1953-1965.
90. Blokesch M. Chitin colonization, chitin degradation and chitin-induced natural competence of Vibrio cholerae are subject to catabolite repression. Environ. Microbiol. 2012, 14:1898-1912.
91. Blokesch M. A quorum sensing-mediated switch contributes to natural transformation of Vibrio cholerae. Mob. Genet. Elements 2012, 2:224-227.
92. Lo Scrudato M., Blokesch M. A transcriptional regulator linking quorum sensing and chitin induction to render Vibrio cholerae naturally transformable. Nucleic Acids Res. 2013, 41:3644-3658.
93. Lo Scrudato M., et al. Regulatory elements involved in the expression of competence genes in naturally transformable Vibrio cholerae. BMC Microbiol. 2014, 14:327.
94. Yamamoto S., et al. Regulation of natural competence by the orphan two-component system sensor kinase ChiS involves a non-canonical transmembrane regulator in Vibrio cholerae. Mol. Microbiol. 2014, 91:326-347.
95. Dalia A.B., et al. Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. MBio 2014, 5. e01028-13.
96. Keyhani N.O., Roseman S. Physiological aspects of chitin catabolism in marine bacteria. Biochim. Biophys. Acta 1999, 1473:108-122.
97. Giltner C.L., et al. Type IV pilin proteins: versatile molecular modules. Microbiol. Mol. Biol. Rev. 2012, 76:740-772.
98. Pelicic V. Type IV pili: e pluribus unum?. Mol. Microbiol. 2008, 68:827-837.
99. Persat A., et al. Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:7563-7568.
100. Craig L., Li J. Type IV pili: paradoxes in form and function. Curr. Opin. Struct. Biol. 2008, 18:267-277.
101. Merz A.J., et al. Pilus retraction powers bacterial twitching motility. Nature 2000, 407:98-102.
102. Herrington D.A., et al. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 1988, 168:1487-1492.
103. Watnick P.I., et al. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 1999, 181:3606-3609.
104. Chiavelli D.A., et al. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 2001, 67:3220-3225.