F conjugation: Back to the beginning

Plasmid

Volumn 70, Issue 1, 2013, Pages 18-32

  Arutyunov, Denis ^a   Frost, Laura S ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Conjugation; Entry exclusion; F plasmid; Mating pair formation; Mating pair stabilization; Pilus specific bacteriophage

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CARRIER PROTEIN; PILIN; TRAG PROTEIN; TRAN PROTEIN; TRAS PROTEIN; TRAT PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BACTERIOPHAGE; BACTERIUM CONJUGATION; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; COUPLING FACTOR; MATING; NONHUMAN; OPERON; PLASMID; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; RNA PHAGE;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE; COLIPHAGES; CONJUGATION, GENETIC; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; F FACTOR; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 84879191056     PISSN: 0147619X     EISSN: 10959890     Source Type: Journal    
DOI: 10.1016/j.plasmid.2013.03.010     Document Type: Review

References (153)

1. Achtman M. Mating aggregates in Escherichia coli conjugation. J. Bacteriol. 1975, 123:505-515.
2. Achtman M., et al. Cell-cell interactions in conjugating Escherichia coli: role of traT protein in surface exclusion. Proc. Natl. Acad. Sci. USA 1977, 74:5104-5108.
3. Achtman M., et al. Cell-cell interactions in conjugating Escherichia coli: role of F pili and fate of mating aggregates. J. Bacteriol. 1978, 135:1053-1061.
4. Achtman M., Skurray R.A. A redefinition of the mating phenomenon in bacteria. Microbial Interactions Receptors and Recognition 1977, vol. 3:234-279. Chapman and Hall, London.
5. Alvarez-Martinez C.E., Christie P.J. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 2009, 73:775-808.
6. Aly K.A., Baron C. The VirB5 protein localizes to the T-pilus tips in Agrobacterium tumefaciens. Microbiology 2007, 153:3766-3775.
7. Anthony, K.G., 1999. Role of the F Pilus in Conjugation. PhD Thesis, University of Alberta.
8. Anthony K.G., et al. The role of the pilus in recipient cell recognition during bacterial conjugation mediated by F-like plasmids. Mol. Microbiol. 1994, 13:939-953.
9. Anthony K.G., et al. Comparison of proteins involved in pilus synthesis and mating pair stabilization from the related plasmids F and R100-1: insights into the mechanism of conjugation. J. Bacteriol. 1999, 181:5149-5159.
10. Armstrong G.D., et al. Comparative biochemical studies on F and EDP208 conjugative pili. J. Bacteriol. 1980, 141:333-341.
11. Armstrong G.D., et al. Nature of the carbohydrate and phosphate associated with ColB2 and EDP208 pilin. J. Bacteriol. 1981, 145:1167-1176.
12. Arutyunov D., et al. F plasmid TraF and TraH are components of an outer membrane complex involved in conjugation. J. Bacteriol. 2010, 192:1730-1734.
13. Atmakuri K., et al. VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol. Microbiol. 2003, 49:1699-1713.
14. Audette G.F., et al. Entry exclusion in F-like plasmids requires intact TraG in the donor that recognizes its cognate TraS in the recipient. Microbiology 2007, 153:442-451.
15. Babic A., et al. Direct visualization of horizontal gene transfer. Science 2008, 319:1533-1536.
16. Bachmann B.J. Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology 1996, 2460-2488. ASM Press, Washington. F.C.E.A. Neidhardt (Ed.).
17. Baron C., et al. Elevated temperature differentially affects virulence, VirB protein accumulation, and T-pilus formation in different Agrobacterium tumefaciens and Agrobacterium vitis strains. J. Bacteriol. 2001, 183:6852-6861.
18. Bradley D.E. Morphological and serological relationships of conjugative pili. Plasmid 1980, 4:155-169.
19. Bradley D.E., et al. Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J. Bacteriol. 1980, 143:1466-1470.
20. Bradley D.E. Specification of the conjugative pili and surface mating systems of Pseudomonas plasmids. J. Gen. Microbiol. 1983, 129:2545-2556.
21. Bradley D.E., Whelan J. Escherichia coli tolQ mutants are resistant to filamentous bacteriophages that adsorb to the tips, not the shafts, of conjugative pili. J. Gen. Microbiol. 1989, 135:1857-1863.
22. Brinton C.C. The properties of sex pili, the viral nature of "conjugal" genetic transfer systems, and some possible approaches to the control of bacterial drug resistance. CRC Crit. Rev. Microbiol. 1971, 1:105-160.
23. Cabeen M.T., et al. The domain organization of the bacterial intermediate filament-like protein crescentin is important for assembly and function. Cytoskeleton 2011, 68:205-219.
24. Caro L.G., Schnös M. The attachment of the male-specific bacteriophage F1 to sensitive strains of Escherichia coli. Proc. Natl. Acad. Sci. USA 1966, 56:126-132.
25. Chandran V., et al. Structure of the outer membrane complex of a type IV secretion system. Nature 2009, 462:1011-1015.
26. Clarke M., et al. F-pili dynamics by live-cell imaging. Proc. Natl. Acad. Sci. USA 2008, 105:17978-17981.
27. Clewell D.B. Bacterial sex pheromone-induced plasmid transfer. Cell 1993, 73:9-12.
28. Click E.M., Webster R.E. The TolQRA proteins are required for membrane insertion of the major capsid protein of the filamentous phage f1 during infection. J. Bacteriol. 1998, 180:1723-1728.
29. Danziger R.E., Paranchych W. Stages in phage R17 infection. II. Ionic requirements for phage R17 attachment to F-pili. Virology 1970, 40:547-553.
30. de la Cruz F., et al. Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol. Rev. 2010, 34:18-40.
31. del Campo I., et al. Determination of conjugation rates on solid surfaces. Plasmid 2012, 67:174-182.
32. Deng L.W., Perham R.N. Delineating the site of interaction on the pIII protein of filamentous bacteriophage fd with the F-pilus of Escherichia coli. J. Mol. Biol. 2002, 319:603-614.
33. Dunny G.M., Leonard B.A. Cell-cell communication in gram-positive bacteria. Annu. Rev. Microbiol. 1997, 51:527-564.
34. Durrenberger M.B., et al. Conjugational junctions: morphology of specific contacts in conjugating Escherichia coli bacteria. J. Struct. Biol. 1991, 107:146-156.
35. Elton T.C., et al. F-like type IV secretion systems encode proteins with thioredoxin folds that are putative DsbC homologues. J. Bacteriol. 2005, 187:8267-8277.
36. Fernandez-Lopez R., et al. Unsaturated fatty acids are inhibitors of bacterial conjugation. Microbiology 2005, 151:3517-3526.
37. Filutowicz M., et al. Bacterial conjugation-based antimicrobial agents. Plasmid 2008, 60:38-44.
38. Finlay B.B., et al. Major antigenic determinants of F and ColB2 pili. J. Bacteriol. 1985, 163:331-335.
39. Finlay B.B., et al. Nucleotide sequences of five IncF plasmid finP alleles. J. Bacteriol. 1986, 167:754-757.
40. Finlay B.B., Paranchych W. Nucleotide sequence of the surface exclusion genes traS and traT from the IncF0 lac plasmid pED208. J. Bacteriol. 1986, 166:713-721.
41. Firth N., Skurray R. Characterization of the F plasmid bifunctional conjugation gene, traG. Mol. Gen. Genet. 1992, 232:145-153.
42. Folkhard W., et al. X-ray diffraction and electron microscope studies on the structure of bacterial F pili. J. Mol. Biol. 1979, 130:145-160.
43. Frost L.S., et al. DNA sequence of the F traALE region that includes the gene for F pilin. J. Bacteriol. 1984, 160:395-401.
44. Frost L.S., et al. Characterization and sequence analysis of pilin from F-like plasmids. J. Bacteriol. 1985, 164:1238-1247.
45. Frost L.S., et al. Two monoclonal antibodies specific for different epitopes within the amino-terminal region of F pilin. J. Bacteriol. 1986, 168:192-198.
46. Frost L.S., Paranchych W. DNA sequence analysis of point mutations in traA, the F pilin gene, reveal two domains involved in F-specific bacteriophage attachment. Mol. Gen. Genet. 1988, 213:134-139.
47. Frost L.S. Bacterial conjugation: everybody's doin' it. Can. J. Microbiol. 1992, 38:1091-1096.
48. Frost L.S. Conjugative pili and pilus-specific phages. Conjugation 1993, 189-221. Plenum Press, New York. D. Clewell (Ed.).
49. Frost L.S., et al. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 1994, 58:162-210.
50. Frost L.S., et al. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 2005, 3:722-732.
51. Frost L.S. Conjugation, bacterial. The Desk Encyclopedia of Microbiology 2009, 294-308. Elsevier, Oxford. M. Shaechter (Ed.).
52. Frost L.S., Koraimann G. Regulation of bacterial conjugation: balancing opportunity with adversity. Future Microbiol. 2010, 5:1057-1071.
53. Frost L.S., Simon J. Studies on the pili of the promiscuous plasmid RP4. Promiscuous Plasmids of Gram-negative and -Positive Bacteria 1993, 47-63. Kluwer Academic Publishers, Dordrecht. C. Kado (Ed.).
54. Garcillan-Barcia M.P., et al. Identification of bacterial plasmids based on mobility and plasmid population biology. FEMS Microbiol. Rev. 2011, 35:936-956.
55. Gilmour M.W., et al. Cellular location and temperature-dependent assembly of IncHI1 plasmid R27-encoded TrhC-associated conjugative transfer protein complexes. Mol. Microbiol. 2001, 42:705-715.
56. Gilmour M.W., Taylor D.E. A subassembly of R27-encoded transfer proteins is dependent on TrhC nucleoside triphosphate-binding motifs for function but not formation. J. Bacteriol. 2004, 186:1606-1613.
57. Gilmour M.W., et al. The complete nucleotide sequence of the resistance plasmid R478: defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics. Plasmid 2004, 52:182-202.
58. Gordon G.S., et al. Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 1997, 90:1113-1121.
59. Grahn A.M., et al. Assembly of a functional phage PRD1 receptor depends on 11 genes of the IncP plasmid mating pair formation complex. J. Bacteriol. 1997, 179:4733-4740.
60. Grohmann E., et al. Conjugative plasmid transfer in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 2003, 67:277-301.
61. Guglielmini J., et al. The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet. 2011, 7:e1002222.
62. Guglielmini J., et al. Evolution of conjugation and type IV secretion systems. Mol. Biol. Evol. 2013, 30:315-331.
63. Gyohda A., et al. Structure and function of the shufflon in plasmid R64. Adv. Biophys. 2004, 38:183-213.
64. Haase J., et al. Bacterial conjugation mediated by plasmid RP4: RSF1010 mobilization, donor-specific phage propagation, and pilus production require the same Tra2 core components of a proposed DNA transport complex. J. Bacteriol. 1995, 177:4779-4791.
65. Haase J., et al. TrbK, a small cytoplasmic membrane lipoprotein, functions in entry exclusion of the IncP alpha plasmid RP4. J. Bacteriol. 1996, 178:6720-6729.
66. Harrington L.C., Rogerson A.C. The F pilus of Escherichia coli appears to support stable DNA transfer in the absence of wall-to-wall contact between cells. J. Bacteriol. 1990, 172:7263-7264.
67. Harris R.L., et al. Evidence that F-plasmid proteins TraV, TraK and TraB assemble into an envelope-spanning structure in Escherichia coli. Mol. Microbiol. 2001, 42:757-766.
68. Harris R.L., Silverman P.M. Tra proteins characteristic of F-like type IV secretion systems constitute an interaction group by yeast two-hybrid analysis. J. Bacteriol. 2004, 186:5480-5485.
69. Harrison J.L., et al. Surface exclusion specificity of the TraT lipoprotein is determined by single alterations in a five-amino-acid region of the protein. Mol. Microbiol. 1992, 6:2825-2832.
70. Heinemann J.A., Sprague G.F. Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 1989, 340:205-209.
71. Horiuchi T., Komano T. Mutational analysis of plasmid R64 thin pilus prepilin: the entire prepilin sequence is required for processing by type IV prepilin peptidase. J. Bacteriol. 1998, 180:4613-4620.
72. Ippen-Ihler K.A., Minkley E.G. The conjugation system of F, the fertility factor of Escherichia coli. Annu. Rev. Genet. 1986, 20:593-624.
73. Ishiwa A., Komano T. PilV adhesins of plasmid R64 thin pili specifically bind to the lipopolysaccharides of recipient cells. J. Mol. Biol. 2004, 343:615-625.
74. Jacobson A. Role of F pili in the penetration of bacteriophage fl. J. Virol. 1972, 10:835-843.
75. Kado C.I. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis. Mol. Microbiol. 1994, 12:17-22.
76. Kalkum M., et al. Protein circlets as sex pilus subunits. Curr. Protein Peptide Sci. 2004, 5:417-424.
77. Kingsman A., Willetts N. The requirements for conjugal DNA synthesis in the donor strain during flac transfer. J. Mol. Biol. 1978, 122:287-300.
78. Klimke W.A., Frost L.S. Genetic analysis of the role of the transfer gene, traN, of the F and R100-1 plasmids in mating pair stabilization during conjugation. J. Bacteriol. 1998, 180:4036-4043.
79. Klimke W.A., et al. The mating pair stabilization protein, TraN, of the F plasmid is an outer-membrane protein with two regions that are important for its function in conjugation. Microbiology 2005, 151:3527-3540.
80. Kotilainen M.M., et al. Binding of an Escherichia coli double-stranded DNA virus PRD1 to a receptor coded by an IncP-type plasmid. J. Bacteriol. 1993, 175:3089-3095.
81. Krahn P.M., Paranchych W. Heterogeneous distribution of A protein in R17 phage preparations. Virology 1971, 43:533-535.
82. Krahn P.M., et al. Stages in phage R17 infection. VI. Injection of A protein and RNA into the host cell. Virology 1972, 47:628-637.
83. Kumar R.B., Das A. Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4. Mol. Microbiol. 2002, 43:1523-1532.
84. Lang S., et al. An activation domain of plasmid R1 TraI protein delineates stages of gene transfer initiation. Mol. Microbiol. 2011, 82:1071-1085.
85. Lang S., Zechner E.L. General requirements for protein secretion by the F-like conjugation system R1. Plasmid 2012, 67:128-138.
86. Lawley T.D., et al. Functional and mutational analysis of conjugative transfer region 1 (Tra1) from the IncHI1 plasmid R27. J. Bacteriol. 2002, 184:2173-2180.
87. Lawley T.D., et al. Bacterial conjugative transfer: visualization of successful mating pairs and plasmid establishment in live Escherichia coli. Mol. Microbiol. 2002, 44:947-956.
88. Lawley T.D., et al. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 2003, 224:1-15.
89. Lawn A.M., Meynell E. Serotypes of sex pili. J. Hyg. 1970, 68:683-694.
90. Lawn A.M., et al. Mixed infections with bacterial sex factors: sex pili of pure and mixed phenotype. Annales de l'Institut Pasteur. 1971, 120:3-8.
91. Lessl M., et al. The mating pair formation system of plasmid RP4 defined by RSF1010 mobilization and donor-specific phage propagation. J. Bacteriol. 1993, 175:6415-6425.
92. Low B., Wood T.H. A quick and efficient method for interruption of bacterial conjugation. Genet. Res. 1965, 124:300-303.
93. Lundström K.H., et al. Lipid-containing bacteriophage PR4: structure and life cycle. J Gen Virol. 1979, 43:583-592.
94. Maher D., et al. Bacteriophages for incompatibility group H plasmids: morphological and growth characteristics. Plasmid 1991, 26:141-146.
95. Maher D., et al. H-pilus assembly kinetics determined by electron microscopy. J. Bacteriol. 1993, 175:2175-2183.
96. Maher D., Taylor D.E. Host range and transfer efficiency of incompatibility group HI plasmids. Can. J. Microbiol. 1993, 39:581-587.
97. Majdalani N., Ippen-Ihler K. Membrane insertion of the F-pilin subunit is Sec independent but requires leader peptidase B and the proton motive force. J. Bacteriol. 1996, 178:3742-3747.
98. Majdalani N., et al. Role of the propilin leader peptide in the maturation of F pilin. J. Bacteriol. 1996, 178:3748-3754.
99. Manchak J., et al. Mutational analysis of F-pilin reveals domains for pilus assembly, phage infection and DNA transfer. Mol. Microbiol. 2002, 43:195-205.
100. Maneewannakul K., et al. Characterization of traX, the F plasmid locus required for acetylation of F-pilin subunits. J. Bacteriol. 1995, 177:2957-2964.
101. Maneewannakul S., et al. Characterization, localization, and sequence of F transfer region products: the pilus assembly gene product TraW and a new product, TrbI. J. Bacteriol. 1992, 174:5567-5574.
102. Manning P.A., et al. TraG protein of the F sex factor of Escherichia coli K-12 and its role in conjugation. Proc. Natl. Acad. Sci. USA 1981, 78:7487-7491.
103. Manoil C., Rosenbusch J.P. Conjugation-deficient mutants of Escherichia coli distinguish classes of functions of the outer membrane OmpA protein. Mol. Gen. Genet. 1982, 187:148-156.
104. Manoil C., Bailey J. A simple screen for permissive sites in proteins: analysis of Escherichia coli lac permease. J. Mol. Biol. 1997, 267:250-263.
105. Marrero J., Waldor M.K. Interactions between inner membrane proteins in donor and recipient cells limit conjugal DNA transfer. Dev. Cell 2005, 8:963-970.
106. Marvin D.A., Folkhard W. Structure of F-pili: reassessment of the symmetry. J. Mol. Biol. 1986, 191:299-300.
107. Marvin D.A. Dynamics of telescoping Inovirus: a mechanism for assembly at membrane adhesions. Int. J. Biol. Macromol. 1989, 11:159-164.
108. Meynell E., et al. Antigenic differences between the ends and shafts of sex pili. J. Gen. Microbiol. 1974, 82:203-205.
109. Moll A., et al. Plasmid-determined resistance to serum bactericidal activity: a major outer membrane protein, the traT gene product, is responsible for plasmid-specified serum resistance in Escherichia coli. Infect. Immun. 1980, 28:359-367.
110. Moore D., et al. Characterization of the F-plasmid conjugative transfer gene traU. J. Bacteriol. 1990, 172:4263-4270.
111. Morona R., et al. Escherichia coli K-12 outer membrane protein (OmpA) as a bacteriophage receptor: analysis of mutant genes expressing altered proteins. J. Bacteriol. 1984, 159:570-578.
112. Novotny C.P., Fives-Taylor P. Retraction of F pili. J. Bacteriol. 1974, 117:1306-1311.
113. O'Callaghan R., et al. The effect of M13 phage infection upon the F pili of E. coli. Virology 1973, 54:220-229.
114. O'Callaghan R.J., et al. Unusual arsenate poisoning of the F pili of Escherichia coli. J. Bacteriol. 1973, 115:76-81.
115. Olsen R.H., et al. Characteristics of PRD1, a plasmid-dependent broad host range DNA bacteriophage. J. Virol. 1974, 14:689-699.
116. Ottow J.C. Ecology, physiology, and genetics of fimbriae and pili. Annu. Rev. Microbiol. 1975, 29:79-108.
117. Pansegrau W., et al. Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis. J. Mol. Biol. 1994, 239:623-663.
118. Paranchych W., et al. Stages in phage R17 infection. Virology 1970, 41:465-473.
119. Paranchych W., et al. Stages in phage R17 infection. V. Phage eclipse and the role of F pili. Virology 1971, 45:615-628.
120. Paranchych W., Frost L.S. The physiology and biochemistry of pili. Adv. Microb. Physiol. 1988, 29:53-114.
121. Perez-Mendoza D., de la Cruz F. Escherichia coli genes affecting recipient ability in plasmid conjugation: are there any?. BMC Genomics 2009, 10:71.
122. Perumal N.B., Minkley E.G. The product of the F sex factor traT surface exclusion gene is a lipoprotein. J. Biol. Chem. 1984, 259:5357-5360.
123. Riechmann L., Holliger P. The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell 1997, 90:351-360.
124. Riede I., Eschbach M.L. Evidence that TraT interacts with OmpA of Escherichia coli. FEBS Lett. 1986, 205:241-245.
125. Rondot S., et al. Epitopes fused to F-pilin are incorporated into functional recombinant pili. J. Mol. Biol. 1998, 279:589-603.
126. Russel M. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J. Mol. Biol. 1998, 279:485-499.
127. Sampei G., et al. Complete genome sequence of the incompatibility group I1 plasmid R64. Plasmid 2010, 64:92-103.
128. Samuels A.L., et al. Conjugative junctions in RP4-mediated mating of Escherichia coli. J. Bacteriol. 2000, 182:2709-2715.
129. Sarkar M.K., et al. Isolation of bacterial type IV machine subassemblies. Methods Mol. Biol. 2013, 966:187-204.
130. Schandel K.A., et al. A traC mutant that retains sensitivity to f1 bacteriophage but lacks F pili. J. Bacteriol. 1987, 169:3151-3159.
131. Schmidt-Eisenlohr H., et al. Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J. Bacteriol. 1999, 181:7485-7492.
132. Schnaitman C.A., Klena J.D. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol. Rev. 1993, 57:655-682.
133. Schroder G., Lanka E. The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid 2005, 54:1-25.
134. Shiba T., Suzuki Y. Localization of A protein in the RNA-A protein complex of RNA phage MS2. Biochim. Biophys. Acta 1981, 654:249-255.
135. Silverman P.M. Towards a structural biology of bacterial conjugation. Mol. Microbiol. 1997, 23:423-429.
136. Skurray R.A., Reeves P. F factor-mediated immunity to lethal zygosis in Escherichia coli K-12. J. Bacteriol. 1974, 117:100-106.
137. Smillie C., et al. Mobility of plasmids. Microbiol. Mol. Biol. Rev. 2010, 74:434-452.
138. Sowa B.A., et al. Physiology of F-pilin synthesis and utilization. J. Bacteriol. 1983, 153:962-968.
139. Stallions D.R., Curtiss R. Bacterial conjugation under anaerobic conditions. J. Bacteriol. 1972, 111:294-295.
140. 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.
141. Tomoeda M., et al. Bacterial sex pili. Prog. Biophys. Mol. Biol. 1975, 30:23-56.
142. Wang Y.A., et al. The structure of F-pili. J. Mol. Biol. 2009, 385:22-29.
143. Willetts N., Skurray R. The conjugation system of F-like plasmids. Annu. Rev. Genet. 1980, 14:41-76.
144. Willetts N., Maule J. Specificities of IncF plasmid conjugation genes. Genet. Res. 1986, 47:1-11.
145. Williams J.J., Hergenrother P.J. Exposing plasmids as the Achilles' heel of drug-resistant bacteria. Curr. Opin. Chem. Biol. 2008, 12:389-399.
146. Winans S.C. Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol. Rev. 1992, 56:12-31.
147. Wong J.J., et al. Relaxosome function and conjugation regulation in F-like plasmids - a structural biology perspective. Mol. Microbiol. 2012, 85:602-617.
148. Wong K., et al. Controlled cleavage of phage R17 RNA within the virion by treatment with ascorbate and copper (II). Can. J. Biochem. 1974, 52:950-958.
149. Wong K., Paranchych W. The preservation of the secondary structure of R17 RNA during penetration into host bacteria. Virology 1976, 73:476-488.
150. Wong K., Paranchych W. The effect of ribonuclease on the penetration of R17 phage A-protein and RNA. Can. J. Microbiol. 1976, 22:826-831.
151. Worobec E.A., et al. Location of the antigenic determinants of conjugative F-like pili. J. Bacteriol. 1986, 167:660-665.
152. Zechner E.L., et al. Assembly and mechanisms of bacterial type IV secretion machines. Phil. Trans. R. Soc. B. 2012, 367:1073-1087.
153. Zuckerman H., Lederberg J. Forty years of genetic recombination in bacteria. Postmature scientific discovery?. Nature 1986, 324:629-631.