The chromosomal SezAT toxin-antitoxin system promotes the maintenance of the SsPI-1 pathogenicity island in epidemic Streptococcus suis

Molecular Microbiology

Volumn 98, Issue 2, 2015, Pages 243-257

  Yao, Xinyue ^a   Chen, Tian ^a   Shen, Xiaodong ^a   Zhao, Yan ^a   Wang, Min ^a   Rao, Xiancai ^a   Yin, Supeng ^a   Wang, Jing ^a   Gong, Yali ^a   Lu, Shuguang ^a   Le, Shuai ^a   Tan, Yinling ^a   Tang, Jiaqi ^b   Fuquan, Hu ^a   Li, Ming ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b NANJING GENERAL HOSPITAL OF NANJING MILITARY COMMAND   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL TOXIN; SEZAT TOXIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENE DELETION; GENE IDENTIFICATION; GENE LOCUS; GENE OVEREXPRESSION; GENETIC CODE; MOLECULAR EVOLUTION; NONHUMAN; OPERON; PATHOGENICITY ISLAND; PRIORITY JOURNAL; SEZA GENE; SEZT GENE; STREPTOCOCCUS SUIS; GENETICS; GENOMIC ISLAND; HUMAN; MICROBIOLOGY; PATHOGENICITY; STREPTOCOCCUS INFECTION; VIRULENCE;

ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CHROMOSOMES, BACTERIAL; GENOMIC ISLANDS; HUMANS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS SUIS; VIRULENCE;

EID: 84943384668     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13116     Document Type: Article

References (69)

1. Albert, H., Dale, E.C., Lee, E., and Ow, D.W. (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7: 649-659.
2. Alonso, J.C., Weise, F., and Rojo, F. (1995) The Bacillus subtilis histone-like protein Hbsu is required for DNA resolution and DNA inversion mediated by the beta recombinase of plasmid pSM19035. J Biol Chem 270: 2938-2945.
3. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
4. Brown, J.S., Gilliland, S.M., Spratt, B.G., and Holden, D.W. (2004) A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice. Infect Immun 72: 1587-1593.
5. Brzozowska, I., Brzozowska, K., and Zielenkiewicz, U. (2012) Functioning of the TA cassette of streptococcal plasmid pSM19035 in various Gram-positive bacteria. Plasmid 68: 51-60.
6. Campo, N., Daveran-Mingot, M.L., Leenhouts, K., Ritzenthaler, P., and Le Bourgeois, P. (2002) Cre-loxP recombination system for large genome rearrangements in Lactococcus lactis. Appl Environ Microbiol 68: 2359-2367.
7. Campo, N., Dias, M.J., Daveran-Mingot, M.L., Ritzenthaler, P., and Le Bourgeois, P. (2004) Chromosomal constraints in Gram-positive bacteria revealed by artificial inversions. Mol Microbiol 51: 511-522.
8. Canosa, I., Rojo, F., and Alonso, J.C. (1996) Site-specific recombination by the beta protein from the streptococcal plasmid pSM19035: minimal recombination sequences and crossing over site. Nucleic Acids Res 24: 2712-2717.
9. Castro-Roa, D., Garcia-Pino, A., De Gieter, S., van Nuland, N.A., Loris, R., and Zenkin, N. (2013) The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu. Nat Chem Biol 9: 811-817.
10. Ceglowski, P., and Alonso, J.C. (1994) Gene organization of the Streptococcus pyogenes plasmid pDB101: sequence analysis of the orf eta-copS region. Gene 145: 33-39.
11. Ceglowski, P., Boitsov, A., Chai, S., and Alonso, J.C. (1993a) Analysis of the stabilization system of pSM19035-derived plasmid pBT233 in Bacillus subtilis. Gene 136: 1-12.
12. Ceglowski, P., Boitsov, A., Karamyan, N., Chai, S., and Alonso, J.C. (1993b) Characterization of the effectors required for stable inheritance of Streptococcus pyogenes pSM19035-derived plasmids in Bacillus subtilis. Mol Gen Genet 241: 579-585.
13. Chen, C., Tang, J., Dong, W., Wang, C., Feng, Y., Wang, J., etal. (2007) A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PLoS ONE 2: e315.
14. Christensen-Dalsgaard, M., and Gerdes, K. (2006) Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Mol Microbiol 62: 397-411.
15. Cordell, S.C., Robinson, E.J., and Lowe, J. (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci USA 100: 7889-7894.
16. Diaz, V., Rojo, F., Martinez, A.C., Alonso, J.C., and Bernad, A. (1999) The prokaryotic beta-recombinase catalyzes site-specific recombination in mammalian cells. J Biol Chem 274: 6634-6640.
17. Fittipaldi, N., Segura, M., Grenier, D., and Gottschalk, M. (2012) Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol 7: 259-279.
18. Fulde, M., and Valentin-Weigand, P. (2013) Epidemiology and pathogenicity of zoonotic streptococci. Curr Top Microbiol Immunol 368: 49-81.
19. Germain, E., Castro-Roa, D., Zenkin, N., and Gerdes, K. (2013) Molecular mechanism of bacterial persistence by HipA. Mol Cell 52: 248-254.
20. Goeders, N., and Van Melderen, L. (2014) Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6: 304-324.
21. Gottschalk, M., Xu, J., Calzas, C., and Segura, M. (2010) Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol 5: 371-391.
22. Gronlund, J.T., Stemmer, C., Lichota, J., Merkle, T., and Grasser, K.D. (2007) Functionality of the beta/six site-specific recombination system in tobacco and Arabidopsis: a novel tool for genetic engineering of plant genomes. Plant Mol Biol 63: 545-556.
23. Hartmann, T., Dumig, M., Jaber, B.M., Szewczyk, E., Olbermann, P., Morschhauser, J., and Krappmann, S. (2010) Validation of a self-excising marker in the human pathogen Aspergillus fumigatus by employing the beta-rec/six site-specific recombination system. Appl Environ Microbiol 76: 6313-6317.
24. Hayes, F. (1998) A family of stability determinants in pathogenic bacteria. J Bacteriol 180: 6415-6418.
25. Hayes, F. (2000) The partition system of multidrug resistance plasmid TP228 includes a novel protein that epitomizes an evolutionarily distinct subgroup of the ParA superfamily. Mol Microbiol 37: 528-541.
26. de la Hoz, A.B., Ayora, S., Sitkiewicz, I., Fernandez, S., Pankiewicz, R., Alonso, J.C., and Ceglowski, P. (2000) Plasmid copy-number control and better-than-random segregation genes of pSM19035 share a common regulator. Proc Natl Acad Sci USA 97: 728-733.
27. Huong, V.T., Ha, N., Huy, N.T., Horby, P., Nghia, H.D., Thiem, V.D., etal. (2014) Epidemiology, clinical manifestations, and outcomes of Streptococcus suis infection in humans. Emerg Infect Dis 20: 1105-1114.
28. Jordan, I.K., Rogozin, I.B., Wolf, Y.I., and Koonin, E.V. (2002) Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 12: 962-968.
29. Khoo, S.K., Loll, B., Chan, W.T., Shoeman, R.L., Ngoo, L., Yeo, C.C., and Meinhart, A. (2007) Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. J Biol Chem 282: 19606-19618.
30. Koczula, A., Willenborg, J., Bertram, R., Takamatsu, D., Valentin-Weigand, P., and Goethe, R. (2014) Establishment of a Cre recombinase based mutagenesis protocol for markerless gene deletion in Streptococcus suis. J Microbiol Methods 107: 80-83.
31. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
32. Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Dreze, P., and Van Melderen, L. (2011) Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39: 5513-5525.
33. Li, M., Wang, C., Feng, Y., Pan, X., Cheng, G., Wang, J., etal. (2008) SalK/SalR, a two-component signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2. PLoS ONE 3: e2080.
34. Li, M., Diep, B.A., Villaruz, A.E., Braughton, K.R., Jiang, X., DeLeo, F.R., etal. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA 106: 5883-5888.
35. Li, M., Shen, X., Yan, J., Han, H., Zheng, B., Liu, D., etal. (2011) GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2. Mol Microbiol 79: 1670-1683.
36. Ludtke, D.N., Eichorn, B.G., and Austin, S.J. (1989) Plasmid-partition functions of the P7 prophage. J Mol Biol 209: 393-406.
37. Lun, Z.R., Wang, Q.P., Chen, X.G., Li, A.X., and Zhu, X.Q. (2007) Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 7: 201-209.
38. Maisonneuve, E., Shakespeare, L.J., Jorgensen, M.G., and Gerdes, K. (2011) Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci USA 108: 13206-13211.
39. Maisonneuve, E., Castro-Camargo, M., and Gerdes, K. (2013) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154: 1140-1150.
40. Makarova, K.S., Wolf, Y.I., Snir, S., and Koonin, E.V. (2011) Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J Bacteriol 193: 6039-6056.
41. Meinhart, A., Alonso, J.C., Strater, N., and Saenger, W. (2003) Crystal structure of the plasmid maintenance system epsilon/zeta: functional mechanism of toxin zeta and inactivation by epsilon 2 zeta 2 complex formation. Proc Natl Acad Sci USA 100: 1661-1666.
42. Milunovic, B., diCenzo, G.C., Morton, R.A., and Finan, T.M. (2014) Cell growth inhibition upon deletion of four toxin-antitoxin loci from the megaplasmids of Sinorhizobium meliloti. J Bacteriol 196: 811-824.
43. Musser, J.M. (1996) Molecular population genetic analysis of emerged bacterial pathogens: selected insights. Emerg Infect Dis 2: 1-17.
44. Mutschler, H., and Meinhart, A. (2011) Epsilon/zeta systems: their role in resistance, virulence, and their potential for antibiotic development. J Mol Med (Berl) 89: 1183-1194.
45. Mutschler, H., Reinstein, J., and Meinhart, A. (2010) Assembly dynamics and stability of the pneumococcal epsilon zeta antitoxin toxin (PezAT) system from Streptococcus pneumoniae. J Biol Chem 285: 21797-21806.
46. Mutschler, H., Gebhardt, M., Shoeman, R.L., and Meinhart, A. (2011) A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol 9: e1001033.
47. Ning, D., Jiang, Y., Liu, Z., and Xu, Q. (2013) Characterization of a chromosomal type II toxin-antitoxin system mazEaFa in the cyanobacterium Anabaena sp. PCC 7120. PLoS ONE 8: e56035.
48. Ogura, T., and Hiraga, S. (1983) Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci USA 80: 4784-4788.
49. Pandey, D.P., and Gerdes, K. (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33: 966-976.
50. Pedersen, K., Christensen, S.K., and Gerdes, K. (2002) Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol Microbiol 45: 501-510.
51. Pomerantsev, A.P., Sitaraman, R., Galloway, C.R., Kivovich, V., and Leppla, S.H. (2006) Genome engineering in Bacillus anthracis using Cre recombinase. Infect Immun 74: 682-693.
52. Robert, X., and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42: W320-W324.
53. Schuster, C.F., and Bertram, R. (2013) Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. FEMS Microbiol Lett 340: 73-85.
54. Suzuki, N., Nonaka, H., Tsuge, Y., Inui, M., and Yukawa, H. (2005) New multiple-deletion method for the Corynebacterium glutamicum genome, using a mutant lox sequence. Appl Environ Microbiol 71: 8472-8480.
55. Syed, M.A., and Levesque, C.M. (2012) Chromosomal bacterial type II toxin-antitoxin systems. Can J Microbiol 58: 553-562.
56. Szekeres, S., Dauti, M., Wilde, C., Mazel, D., and Rowe-Magnus, D.A. (2007) Chromosomal toxin-antitoxin loci can diminish large-scale genome reductions in the absence of selection. Mol Microbiol 63: 1588-1605.
57. Tabone, M., Ayora, S., and Alonso, J.C. (2014a) Toxin zeta reversible induces dormancy and reduces the UDP-N-acetylglucosamine pool as one of the protective responses to cope with stress. Toxins (Basel) 6: 2787-2803.
58. Tabone, M., Lioy, V.S., Ayora, S., Machon, C., and Alonso, J.C. (2014b) Role of toxin zeta and starvation responses in the sensitivity to antimicrobials. PLoS ONE 9: e86615.
59. Tang, J., Wang, C., Feng, Y., Yang, W., Song, H., Chen, Z., etal. (2006) Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med 3: e151.
60. Tsilibaris, V., Maenhaut-Michel, G., Mine, N., and Van Melderen, L. (2007) What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome? J Bacteriol 189: 6101-6108.
61. Van Melderen, L. (2010) Toxin-antitoxin systems: why so many, what for? Curr Opin Microbiol 13: 781-785.
62. Van Melderen, L., and Saavedra De Bast, M. (2009) Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet 5: e1000437.
63. Wen, Y., Behiels, E., Felix, J., Elegheert, J., Vergauwen, B., Devreese, B., and Savvides, S.N. (2014) The bacterial antitoxin HipB establishes a ternary complex with operator DNA and phosphorylated toxin HipA to regulate bacterial persistence. Nucleic Acids Res 42: 10134-10147.
64. Wertheim, H.F., Nghia, H.D., Taylor, W., and Schultsz, C. (2009) Streptococcus suis: an emerging human pathogen. Clin Infect Dis 48: 617-625.
65. Wozniak, R.A., and Waldor, M.K. (2009) A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet 5: e1000439.
66. Yamaguchi, Y., and Inouye, M. (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9: 779-790.
67. Yamaguchi, Y., Park, J.H., and Inouye, M. (2011) Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45: 61-79.
68. Yuan, J., Yamaichi, Y., and Waldor, M.K. (2011) The three Vibrio cholerae chromosome II-encoded ParE toxins degrade chromosome I following loss of chromosome II. J Bacteriol 193: 611-619.
69. Zielenkiewicz, U., and Ceglowski, P. (2005) The toxin-antitoxin system of the streptococcal plasmid pSM19035. J Bacteriol 187: 6094-6105.