Interbacterial macromolecular transfer by the Campylobacter fetus subsp. venerealis type IV secretion system

Journal of Bacteriology

Volumn 193, Issue 3, 2011, Pages 744-758

  Kienesberger, Sabine ^a,b   Trummler, Caroline Schober ^a   Fauster, Astrid ^a   Lang, Silvia ^a   Sprenger, Hanna ^a,b   Gorkiewicz, Gregor ^b   Zechner, Ellen L ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

PLASMID DNA;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; CAMPYLOBACTER FETUS; DNA TRANSFER; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROMOTER REGION; TEMPERATURE DEPENDENCE; THERMOREGULATION;

CAMPYLOBACTER FETUS; CELL SURFACE EXTENSIONS; CONJUGATION, GENETIC; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENOMIC ISLANDS; MACROMOLECULAR SUBSTANCES; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PLASMIDS; SEQUENCE ANALYSIS, DNA; TEMPERATURE;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER COLI; CAMPYLOBACTER FETUS; CAMPYLOBACTER FETUS SUBSP. VENEREALIS; ESCHERICHIA COLI;

EID: 78751536675     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00798-10     Document Type: Article

References (78)

1. Abril, C., I. Brodard, and V. Perreten. 2010. Two novel antibiotic resistance genes, tet(44) and ant(6)-Ib, are located within a transferable pathogenicity island in Campylobacter fetus subsp. fetus. Antimicrob. Agents Chemother. 54:3052-3055.
2. Abril, C., et al. 2007. Discovery of insertion element ISCfe1: a new tool for Campylobacter fetus subspecies differentiation. Clin. Microbiol. Infect. 13: 993-1000.
3. Alvarez-Martinez, C. E., and P. J. Christie. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808.
4. Andersen, J. B., et al. 2001. gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67:575-585.
5. Backert, S., and T. F. Meyer. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9:207-217.
6. Barrios, A. F., R. Zuo, D. Ren, and T. K. Wood. 2006. Hha, YbaJ, and OmpA regulate Escherichia coli K12 biofilm formation and conjugation plasmids abolish motility. Biotechnol. Bioeng. 93:188-200.
7. Blaser, M. J. 1998. Campylobacter fetus-emerging infection and model system for bacterial pathogenesis at mucosal surfaces. Clin. Infect. Dis. 27:256-258.
8. Blaser, M. J., D. G. Newell, S. A. Thompson, and E. L. Zechner. 2008. Pathogenesis of Campylobacter fetus infections, p. 401-428. In I. Nachamkin, C. M. Szymanski, and M. J. Blaser (ed.), Campylobacter, 3rd ed. ASM Press, Washington, D.C.
9. Boschiroli, M. L., et al. 2002. Type IV secretion and Brucella virulence. Vet. Microbiol. 90:341-348.
10. Buchanan-Wollaston, V., J. E. Passiatore, and F. Cannon. 1987. The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328:172-175.
11. Cambronne, E. D., and C. R. Roy. 2006. Recognition and delivery of effector proteins into eukaryotic cells by bacterial secretion systems. Traffic 7:929-939.
12. Cascales, E., and P. J. Christie. 2003. The versatile bacterial type IV secretion systems. Nat. Rev. Microbiol. 1:137-149.
13. Chandler, M., and D. J. Galas. 1983. Cointegrate formation mediated by Tn9. II. Activity of IS1 is modulated by external DNA sequences. J. Mol. Biol. 170:61-91.
14. Chatfield, L. K., E. Orr, G. J. Boulnois, and B. M. Wilkins. 1982. DNA primase of plasmid ColIb is involved in conjugal DNA synthesis in donor and recipient bacteria. J. Bacteriol. 152:1188-1195.
15. Chen, I., P. J. Christie, and D. Dubnau. 2005. The ins and outs of DNA transfer in bacteria. Science 310:1456-1460.
16. Christie, P. J., K. Atmakuri, V. Krishnamoorthy, S. Jakubowski, and E. Cascales. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485.
17. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
18. de Lorenzo, V., and K. N. Timmis. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
19. Ding, Z., K. Atmakuri, and P. J. Christie. 2003. The outs and ins of bacterial type IV secretion substrates. Trends Microbiol. 11:527-535.
20. Fernandez-Lopez, R., et al. 2006. Dynamics of the IncW genetic backbone imply general trends in conjugative plasmid evolution. FEMS Microbiol. Rev. 30:942-966.
21. Fischer, W., R. Haas, and S. Odenbreit. 2002. Type IV secretion systems in pathogenic bacteria. Int. J. Med. Microbiol. 292:159-168.
22. Fischer, W., et al. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
23. Franco, I. S., H. A. Shuman, and X. Charpentier. 2009. The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell Microbiol. 11:1435-1443.
24. Frank, A. C., C. M. Alsmark, M. Thollesson, and S. G. Andersson. 2005. Functional divergence and horizontal transfer of type IV secretion systems. Mol. Biol. Evol. 22:1325-1336.
25. Garcillan-Barcia, M. P., and F. de la Cruz. 2008. Why is entry exclusion an essential feature of conjugative plasmids? Plasmid 60:1-18.
26. Ghigo, J. M. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442-445.
27. Goebel, W., W. Lindenmaier, H. Schrempf, R. Kollek, and D. Blohm. 1977. Dissociation and recombination of fragments with defined functions of the antibiotic resistance factor R1, p. 261-275. In J. Drews and G. Högenauer (ed.), Topics in infectious diseases, vol. 2. Springer-Verlag, New York, NY.
28. Gorkiewicz, G., et al. 2010. A genomic island defines subspecies-specific virulence features of the host-adapted pathogen Campylobacter fetus subsp. venerealis. J. Bacteriol. 192:502-517.
29. Grandoso, G., M. Llosa, J. C. Zabala, and F. de la Cruz. 1994. Purification and biochemical characterization of TrwC, the helicase involved in plasmid R388 conjugal DNA transfer. Eur. J. Biochem. 226:403-412.
30. Haft, R. J., et al. 2006. General mutagenesis of F plasmid TraI reveals its role in conjugative regulation. J. Bacteriol. 188:6346-6353.
31. Hu, L., and D. J. Kopecko. 2000. Interactions of Campylobacter with eukaryotic cells: gut luminal colonization and mucosal invasion mechanisms, p. 191-215. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, DC.
32. Juhas, M., D. W. Crook, and D. W. Hood. 2008. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol. 10:2377-2386.
33. Kienesberger, S., et al. 2007. Development of experimental genetic tools for Campylobacter fetus. Appl. Environ. Microbiol. 73:4619-4630.
34. Kienesberger, S., G. Gorkiewicz, H. Wolinski, and E. L. Zechner. 2010. New molecular microbiology approaches in the study of Campylobacter fetus. Microb. Biotechnol., in press. doi:10.1111/j.1751-7915.2010.00173.x.
35. Kinch, L. N., M. L. Yarbrough, K. Orth, and N. V. Grishin. 2009. Fido, a novel AMPylation domain common to fic, doc, and AvrB. PLoS One 4:e5818.
36. Komano, T., R. Utsumi, and M. Kawamukai. 1991. Functional analysis of the fic gene involved in regulation of cell division. Res. Microbiol. 142:269-277.
37. Krause, R., et al. 2002. Recurrent septicemia due to Campylobacter fetus and Campylobacter lari in an immunocompetent patient. Infection 30:171-174.
38. Lambert, T., G. Gerbaud, P. Trieu-Cuot, and P. Courvalin. 1985. Structural relationship between the genes encoding 3′-aminoglycoside phosphotransferases in Campylobacter and in gram-positive cocci. Ann. Inst. Pasteur Microbiol. 136B:135-150.
39. Lang, S., et al. 2010. Molecular recognition determinants for type IV secretion of diverse families of conjugative relaxases. Mol. Microbiol., in press.
40. Lawley, T. D., W. A. Klimke, M. J. Gubbins, and L. S. Frost. 2003. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224: 1-15.
41. Lin, T. S., and C. I. Kado. 1993. The virD4 gene is required for virulence while virD3 and orf5 are not required for virulence of Agrobacterium tumefaciens. Mol. Microbiol. 9:803-812.
42. Lu, J., et al. 2008. Structural basis of specific TraD-TraM recognition during F plasmid-mediated bacterial conjugation. Mol. Microbiol. 70:89-99.
43. Maneewannakul, K., et al. 1996. Construction of derivatives of the F plasmid pOX-tra715: characterization of traY and traD mutants that can be complemented in trans. Mol. Microbiol. 22:197-205.
44. Martinez, E., and F. de la Cruz. 1988. Transposon Tn21 encodes a RecAindependent site-specific integration system. Mol. Gen. Genet. 211:320-325.
45. Nagai, H., et al. 2005. A C-terminal translocation signal required for Dot/ Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. U. S. A. 102:826-831.
46. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
47. Pan, X., A. Luhrmann, A. Satoh, M. A. Laskowski-Arce, and C. R. Roy. 2008. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320:1651-1654.
48. Pansegrau, W., et al. 1994. Complete nucleotide sequence of Birmingham IncP alpha plasmids: compilation and comparative analysis. J. Mol. Biol. 239:623-663.
49. Parker, C., and R. J. Meyer. 2007. The R1162 relaxase/primase contains two, type IV transport signals that require the small plasmid protein MobB. Mol. Microbiol. 66:252-261.
50. Perez-Perez, G. I., M. J. Blaser, and J. H. Bryner. 1986. Lipopolysaccharide structures of Campylobacter fetus are related to heat-stable serogroups. Infect. Immun. 51:209-212.
51. Reisner, A., J. A. Haagensen, M. A. Schembri, E. L. Zechner, and S. Molin. 2003. Development and maturation of Escherichia coli K-12 biofilms. Mol. Microbiol. 48:933-946.
52. Reisner, A., S. Molin, and E. L. Zechner. 2002. Recombinogenic engineering of conjugative plasmids with fluorescent marker cassettes. FEMS Microbiol. Ecol. 42:251-259.
53. Roy, C. R., and S. Mukherjee. 2009. Bacterial FIC proteins AMP up infection. Sci. Signal 2:pe14.
54. Salgado Pabon, W., et al. 2010. Increased expression of the type IV secretion system in piliated Neisseria gonorrhoeae variants. J. Bacteriol. 192:1912-1920.
55. Sastre, J. I., E. Cabezon, and F. de la Cruz. 1998. The carboxyl terminus of protein TraD adds specificity and efficiency to F-plasmid conjugative transfer. J. Bacteriol. 180:6039-6042.
56. Schmid, M. C., et al. 2006. A translocated bacterial protein protects vascular endothelial cells from apoptosis. PLoS Pathog. 2:e115.
57. Schroder, G., and C. Dehio. 2005. Virulence-associated type IV secretion systems of Bartonella. Trends Microbiol. 13:336-342.
58. Schroder, G., and E. Lanka. 2005. The mating pair formation system of conjugative plasmids: a versatile secretion machinery for transfer of proteins and DNA. Plasmid 54:1-25.
59. Schulein, R., and C. Dehio. 2002. The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol. Microbiol. 46:1053-1067.
60. Schulein, R., et al. 2005. A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc. Natl. Acad. Sci. U. S. A. 102:856-861.
61. Skirrow, M. B., and M. J. Blaser. 2000. Clinical aspects of Campylobacter infections, p. 69-88. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. American Society for Microbiology, Washington, DC.
62. Sory, M. P., and G. R. Cornelis. 1994. Translocation of a hybrid YopEadenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
63. Thompson, S. A., and M. J. Blaser. 2000. Pathogenesis of Campylobacter fetus infections, p. 321-347. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, DC.
64. Tummuru, M. K., and M. J. Blaser. 1993. Rearrangement of sapA homologs with conserved and variable regions in Campylobacter fetus. Proc. Natl. Acad. Sci. U. S. A. 90:7265-7269.
65. van Bergen, M. A., et al. 2005. Clonal nature of Campylobacter fetus as defined by multilocus sequence typing. J. Clin. Microbiol. 43:5888-5898.
66. van Bergen, M. A., et al. 2005. Amplified fragment length polymorphism based identification of genetic markers and novel PCR assay for differentiation of Campylobacter fetus subspecies. J. Med. Microbiol. 54:1217-1224.
67. Vergunst, A. C., et al. 2000. VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:979-982.
68. Vergunst, A. C., et al. 2005. Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc. Natl. Acad. Sci. U. S. A. 102:832-837.
69. Vogel, J. P., H. L. Andrews, S. K. Wong, and R. R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279:873-876.
70. Voth, D. E., and R. A. Heinzen. 2009. Coxiella type IV secretion and cellular microbiology. Curr. Opin. Microbiol. 12:74-80.
71. Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586-595.
72. Willoughby, K., et al. 2005. A multiplex polymerase chain reaction to detect and differentiate Campylobacter fetus subspecies fetus and Campylobacter fetus subspecies venerealis: use on UK isolates of C. fetus and other Campylobacter spp. J. Appl. Microbiol. 99:758-766.
73. Woodcock, D. M., et al. 1989. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17:3469-3478.
74. Worby, C. A., et al. 2009. The fic domain: regulation of cell signaling by adenylylation. Mol. Cell 34:93-103.
75. Yao, R., R. A. Alm, T. J. Trust, and P. Guerry. 1993. Construction of new Campylobacter cloning vectors and a new mutational cat cassette. Gene 130:127-130.
76. Yarbrough, M. L., et al. 2009. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323:269-272.
77. Zechner, E. L., et al. 2000. Conjugative-DNA transfer processes, p. 87-174. In C. M. Thomas (ed.), The horizontal gene pool: bacterial plasmids and gene spread. Harwood Academic Publishers, Amsterdam, Netherlands.
78. Zekarias, B., et al. Histophilus somni IbpA DR2/Fic in virulence and immunoprotection at the natural host alveolar epithelial barrier. Infect. Immun. 78:1850-1858.