1887

Abstract

Hha-like proteins are an evolutive trait of members of the family . These proteins mimic the oligomerization domain of the nucleoid-associated protein H-NS and interact with this latter protein to modulate gene expression. In this report, we provide evidence that, as has been shown for H-NS, Hha-like proteins play an essential role facilitating acquisition of horizontally transferred DNA in both and . Incorporation of conjugative plasmids such as pHly152 or R27 results in a fitness cost in or strains that lack Hha-like proteins. spontaneous derivatives from double mutants that showed an increased growth rate and a restored fitness overexpressed the H-NS protein. In addition to reinforcing the role of H-NS/Hha-modulating xenogeneic DNA, the results obtained demonstrate that the display regulatory features not found in other bacteria that facilitate incorporation of horizontally transferred DNA.

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2013-03-01
2021-10-17
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References

  1. Bachmann B. J. ( 1987). Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp. 1190–1220 Ingraham J. L., Low K. B., Magasanik B., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  3. Baquero F. ( 2004). From pieces to patterns: evolutionary engineering in bacterial pathogens. Nat Rev Microbiol 2:510–518 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  9. Dillon S. C., Dorman C. J. ( 2010). Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8:185–195 [View Article][PubMed]
    [Google Scholar]
  10. Dionisio F., Conceição 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[PubMed] [CrossRef]
    [Google Scholar]
  11. Dorman C. J. ( 2004). H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391–400 [View Article][PubMed]
    [Google Scholar]
  12. Dorman C. J. ( 2007). H-NS, the genome sentinel. Nat Rev Microbiol 5:157–161 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  20. Grindley N. D., Grindley J. N., Anderson E. S. ( 1972). R factor compatibility groups. Mol Gen Genet 119:287–297[PubMed]
    [Google Scholar]
  21. Ilatovskiy A., Petukhov M. ( 2009). Genome-wide search for local DNA segments with anomalous GC-content. J Comput Biol 16:555–564 [View Article][PubMed]
    [Google Scholar]
  22. Koonin E. V., Makarova K. S., Aravind L. ( 2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  30. Noegel A., Rdest U., Goebel W. ( 1981). Determination of the functions of hemolytic plasmid pHly152 of Escherichia coli . J Bacteriol 145:233–247[PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  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 [View Article][PubMed]
    [Google Scholar]
  40. Suzuki H., Yano H., Brown C. J., Top E. M. ( 2010). Predicting plasmid promiscuity based on genomic signature. J Bacteriol 192:6045–6055 [View Article][PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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[PubMed] [CrossRef]
    [Google Scholar]
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