The Hha protein facilitates incorporation of horizontally acquired DNA in enteric bacteria

Microbiology (United Kingdom)

Volumn 159, Issue PART3, 2013, Pages 545-554

  Aznar, Sonia ^a   Paytubi, Sonia ^a   Juárez, Antonio ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; MUTANT PROTEIN; PROTEIN HHA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA TRANSFER; ESCHERICHIA COLI; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI; GENE KNOCKOUT TECHNIQUES; GENE TRANSFER, HORIZONTAL; PLASMIDS; RECOMBINATION, GENETIC; SALMONELLA;

EID: 84874783243     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.062448-0     Document Type: Article

References (43)

1. Bachmann, B. J. (1987). Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp. 1190-1220. Edited by J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter & H. E. Umbarger. Washington, DC: American Society for Microbiology.
2. Baños, R. C., Vivero, A., Aznar, S., García, J., Pons, M., Madrid, C. & Juárez, A. (2009). Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet 5, e1000513.
3. Baquero, F. (2004). From pieces to patterns: evolutionary engineering in bacterial pathogens. Nat Rev Microbiol 2, 510-518.
4. Cherepanov, P. P. & Wackernagel, W. (1995). Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9-14.
5. Coombes, B. K., Wickham, M. E., Lowden, M. J., Brown, N. F. & Finlay, B. B. (2005). Negative regulation of Salmonella pathogenicity island 2 is required for contextual control of virulence during typhoid. Proc Natl Acad Sci U S A 102, 17460-17465.
6. Datsenko, K. A. & Wanner, B. L. (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.
7. De Gelder, L., Ponciano, J. M., Joyce, P. & Top, E. M. (2007). Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 153, 452-463.
8. Dersch, P., Schmidt, K. & Bremer, E. (1993). Synthesis of the Escherichia coli K-12 nucleoid-associated DNA-binding protein H-NS is subjected to growth-phase control and autoregulation. Mol Microbiol 8, 875-889.
9. Dillon, S. C. & Dorman, C. J. (2010). Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8, 185-195.
10. Dionisio, F., Conceião, I. C., Marques, A. C., Fernandes, L. & Gordo, I. (2005). The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol Lett 1, 250-252.
11. Dorman, C. J. (2004). H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2, 391-400.
12. Dorman, C. J. (2007). H-NS, the genome sentinel. Nat Rev Microbiol 5, 157-161.
13. Doyle, M., Fookes, M., Ivens, A., Mangan, M. W., Wain, J. & Dorman, C. J. (2007). An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315, 251-252.
14. Ellison, D. W. & Miller, V. L. (2006). H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J Bacteriol 188, 5101-5112.
15. Fahlen, T. F., Wilson, R. L., Boddicker, J. D. & Jones, B. D. (2001). Hha is a negative modulator of transcription of hilA, the Salmonella enterica serovar Typhimurium invasion gene transcriptional activator. J Bacteriol 183, 6620-6629.
16. Fica, A., Fernandez-Beros, M. E., Aron-Hott, L., Rivas, A., D'Ottone, K., Chumpitaz, J., Guevara, J. M., Rodriguez, M. & Cabello, F. (1997). Antibiotic-resistant Salmonella typhi from two outbreaks: few ribotypes and IS200 types harbor Inc HI1 plasmids. Microb Drug Resist 3, 339-343.
17. Forns, N., Baños, R. C., Balsalobre, C., Juárez, A. & Madrid, C. (2005). Temperature-dependent conjugative transfer of R27: role of chromosome-and plasmid-encoded Hha and H-NS proteins. J Bacteriol 187, 3950-3959.
18. Frost, L. S., Leplae, R., Summers, A. O. & Toussaint, A. (2005). Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3, 722-732.
19. Godessart, N., Muñoa, F. J., Regue, M. & Juárez, A. (1988). Chromosomal mutations that increase the production of a plasmid-encoded haemolysin in Escherichia coli. J Gen Microbiol 134, 2779-2787.
20. Grindley, N. D., Grindley, J. N. & Anderson, E. S. (1972). R factor compatibility groups. Mol Gen Genet 119, 287-297.
21. Ilatovskiy, A. & Petukhov, M. (2009). Genome-wide search for local DNA segments with anomalous GC-content. J Comput Biol 16, 555-564.
22. Koonin, E. V., Makarova, K. S. & Aravind, L. (2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55, 709-742.
23. Lucchini, S., Rowley, G., Goldberg, M. D., Hurd, D., Harrison, M. & Hinton, J. C. (2006). H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2, e81.
24. Madrid, C., Nieto, J. M., Paytubi, S., Falconi, M., Gualerzi, C. O. & Juárez, A. (2002). Temperature-and H-NS-dependent regulation of a plasmid-encoded virulence operon expressing Escherichia coli hemolysin. J Bacteriol 184, 5058-5066.
25. Madrid, C., Balsalobre, C., García, J. & Juárez, A. (2007). The novel Hha/YmoA family of nucleoid-associated proteins: use of structural mimicry to modulate the activity of the H-NS family of proteins. Mol Microbiol 63, 7-14.
26. Mouriño, M., Balsalobre, C., Madrid, C., Nieto, J. M., Prenafeta, A., Muñoa, F. J. & Juárez, A. (1998). Osmolarity modulates the expression of the Hha protein from Escherichia coli. FEMS Microbiol Lett 160, 225-229.
27. Navarre, W. W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S. J. & Fang, F. C. (2006). Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313, 236-238.
28. Nieto, J. M., Madrid, C., Prenafeta, A., Miquelay, E., Balsalobre, C., Carrascal, M. & Juárez, A. (2000). Expression of the hemolysin operon in Escherichia coli is modulated by a nucleoid-protein complex that includes the proteins Hha and H-NS. Mol Gen Genet 263, 349-358.
29. Nieto, J. M., Madrid, C., Miquelay, E., Parra, J. L., Rodríguez, S. & Juárez, A. (2002). Evidence for direct protein-protein interaction between members of the enterobacterial Hha/YmoA and H-NS families of proteins. J Bacteriol 184, 629-635.
30. Noegel, A., Rdest, U. & Goebel, W. (1981). Determination of the functions of hemolytic plasmid pHly152 of Escherichia coli. J Bacteriol 145, 233-247.
31. Norman, A., Hansen, L. H. & Sørensen, S. J. (2009). Conjugative plasmids: vessels of the communal gene pool. Philos Trans R Soc Lond B Biol Sci 364, 2275-2289.
32. Olekhnovich, I. N. & Kadner, R. J. (2006). Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J Mol Biol 357, 373-386.
33. Oshima, T., Ishikawa, S., Kurokawa, K., Aiba, H. & Ogasawara, N. (2006). Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13, 141-153.
34. Owen-Hughes, T. A., Pavitt, G. D., Santos, D. S., Sidebotham, J. M., Hulton, C. S., Hinton, J. C. & Higgins, C. F. (1992). The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression. Cell 71, 255-265.
35. Paytubi, S., Madrid, C., Forns, N., Nieto, J. M., Balsalobre, C., Uhlin, B. E. & Juárez, A. (2004). YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol Microbiol 54, 251-263.
36. Paytubi, S., García, J. & Juárez, A. (2011). Bacterial Hha-like proteins facilitate incorporation of horizontally transferred DNA. Cent Eur J Biol 6, 879-886.
37. Pedró, L., Baños, R. C., Aznar, S., Madrid, C., Balsalobre, C. & Juárez, A. (2011). Antibiotics shaping bacterial genome: deletion of an IS91 flanked virulence determinant upon exposure to subinhibitory antibiotic concentrations. PLoS ONE 6, e27606.
38. Poole, T. L., Brichta-Harhay, D. M., Callaway, T. R., Beier, R. C., Bischoff, K. M., Loneragan, G. H., Anderson, R. C. & Nisbet, D. J. (2011). Persistence of resistance plasmids carried by beta-hemolytic Escherichia coli when maintained in a continuous-flow fermentation system without antimicrobial selection pressure. Foodborne Pathog Dis 8, 535-540.
39. Silphaduang, U., Mascarenhas, M., Karmali, M. & Coombes, B. K. (2007). Repression of intracellular virulence factors in Salmonella by the Hha and YdgT nucleoid-associated proteins. J Bacteriol 189, 3669-3673.
40. Suzuki, H., Yano, H., Brown, C. J. & Top, E. M. (2010). Predicting plasmid promiscuity based on genomic signature. J Bacteriol 192, 6045-6055.
41. Takeda, T., Yun, C. S., Shintani, M., Yamane, H. & Nojiri, H. (2011). Distribution of genes encoding nucleoid-associated protein homologs in plasmids. Int J Evol Biol 2011, 685015.
42. Taylor, D. E. & Levine, J. G. (1980). Studies of temperature-sensitive transfer and maintenance of H incompatibility group plasmids. J Gen Microbiol 116, 475-484.
43. Vivero, A., Baños, R. C., Mariscotti, J. F., Oliveros, J. C., García-del Portillo, F., Juárez, A. & Madrid, C. (2008). Modulation of horizontally acquired genes by the Hha-YdgT proteins in Salmonella enterica serovar Typhimurium. J Bacteriol 190, 1152-1156.