Inactivation of PbTopo IIIβ causes hyper-excision of the Pathogenicity Island HAI2 resulting in reduced virulence of Pectobacterium atrosepticum

Molecular Microbiology

Volumn 84, Issue 4, 2012, Pages 648-663

  Vanga, Bhanupratap R ^a,b   Butler, Ruth C ^a   Toth, Ian K ^c   Ronson, Clive W ^b   Pitman, Andrew R ^a,d  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^d LINCOLN UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CORONAFACIC ACID; DNA TOPOISOMERASE; PROTEIN PBTOPO IIIBETA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL STRAIN; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENZYME INACTIVATION; EPISOME; GROWTH CURVE; HORIZONTAL GENE TRANSFER; HORIZONTALLY ACQUIRED ISLAND 2; HOST CELL; IN VITRO STUDY; NONHUMAN; PATHOGENICITY ISLAND; PECTOBACTERIUM; PECTOBACTERIUM ATROSEPTICUM; POTATO; PRIORITY JOURNAL;

DNA TOPOISOMERASES, TYPE I; DNA, BACTERIAL; GENOMIC ISLANDS; PECTOBACTERIUM; PLANT DISEASES; RECOMBINATION, GENETIC; SOLANUM TUBEROSUM; VIRULENCE;

BACTERIA (MICROORGANISMS); PECTOBACTERIUM ATROSEPTICUM; SOLANUM TUBEROSUM;

EID: 84860591021     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08050.x     Document Type: Article

References (51)

1. Bell, K.S., Sebaihia, M., Pritchard, L., Holden, M.T.G., Hyman, L.J., Holeva, M.C., etal. (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA 101: 11105-11110.
2. Blakely, G., May, G., McCulloch, R., Arciszewska, L.K., Burke, M., Lovett, S.T., and Sherratt, D.J. (1993) Two related recombinases are required for site-specific recombination at dif and cer in Escherichia coli K12. Cell 75: 351-361.
3. Buchrieser, C., Brosch, R., Bach, S., Guiyoule, A., and Carniel, E. (1998) Thehigh-pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal asn tRNA genes. Mol Microbiol 30: 965-978.
4. Cheng, Q., Sutanto, Y., Shoemaker, N.B., Gardner, J.F., and Salyers, A.A. (2001) Identification of genes required for excision of CTnDOT, a Bacteroides conjugative transposon. Mol Microbiol 41: 625-632.
5. Colloms, S.D., Alen, C., and Sherratt, D.J. (1998) The ArcA/ArcB two-component regulatory system of Escherichia coli is essential for Xer site-specific recombination at psi. Mol Microbiol 28: 521-530.
6. Cornet, F., Mortier, I., Patte, J., and Louarn, J.M. (1994) Plasmid pSC101harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J Bacteriol 176: 3188-3195.
7. DiGate, R.J., and Marians, K.J. (1988) Identification of a potent decatenating enzyme from Escherichia coli. J Biol Chem 263: 13366-13373.
8. Dombrecht, B., Vanderleyden, J., and Michiels, J. (2001) Stable RK2-derived cloning vectors for the analysis of gene expression and gene function in gram-negative bacteria. Mol Plant Microbe Interact 14: 426-430.
9. Gaillard, M., Vallaeys, T., Vorhölter, F.J., Minoia, M., Werlen, C., Sentchilo, V., etal. (2006) The clc element of Pseudomonas sp. strain B13, a genomic island with various catabolic properties. J Bacteriol 188: 1999-2013.
10. Gangloff, S., de Massy, B., Arthur, L., Rothstein, R., and Fabre, F. (1999) The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J 18: 1701-1711.
11. GenStat Committee, G.S. (2010a) The Guide to GenStat Release 13 - Part 2, Statistics. Oxford: VSN International.
12. GenStat Committee, G.S. (2010b) The Guide to GenStat Release 13 - Parts 1-3. Oxford: VSN International.
13. Godfrey, S.A.C., Lovell, H.C., Mansfield, J.W., Corry, D.S., Jackson, R.W., and Arnold, D.L. (2011) The stealth episome: suppression of gene expression on the excised genomic island PPHGI-1 from Pseudomonas syringae pv. phaseolicola. PLoS Pathog 7: e1002010.
14. Hiasa, H., DiGate, R.J., and Marians, K.J. (1994) Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro. J Biol Chem 269: 2093-2099.
15. Holeva, M.C., Bell, K.S., Hyman, L.J., Avrova, A.O., Whisson, S.C., Birch, P.R.J., and Toth, I.K. (2004) Use of a pooled transposon mutation grid to demonstrate roles in disease development for Erwinia carotovora subsp. atroseptica putative type III secreted effector (DspE/A) andhelper (HrpN) proteins. Mol Plant Microbe Interact 17: 943-950.
16. Kenward, M.G., and Roger, J.H. (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53: 983-997.
17. Lenski, R.E., Rose, M.R., Simpson, S.C., and Tadler, S.C. (1991) Long-term experimental evolution in Escherichia coli. 1. Adaptation and divergence during 2, 000 generations. Am Nat 138: 1315-1341.
18. Lesic, B., Bach, S., Ghigo, J.M., Dobrindt, U., Hacker, J., and Carniel, E. (2004) Excision of thehigh-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol Microbiol 52: 1337-1348.
19. Li, Z., Hiasa, H., and DiGate, R. (2006) Characterization of a unique type IA topoisomerase in Bacillus cereus. Mol Microbiol 60: 140-151.
20. Li, Z.Y., Hiasa, H., Kumar, U., and DiGate, R.J. (1997) The traE gene of plasmid RP4 encodes ahomologue of Escherichia coli DNA topoisomerase III. J Biol Chem 272: 19582-19587.
21. Li, Z.Y., Mondragon, A., Hiasa, H., Marians, K.J., and DiGate, R.J. (2000) Identification of a unique domain essential for Escherichia coli DNA topoisomerase III-catalysed decatenation of replication intermediates. Mol Microbiol 35: 888-895.
22. Li, Z.Y., Hiasa, H., and DiGate, R. (2005) Bacillus cereus DNA topoisomerase I and IIIα: purification, characterization and complementation of Escherichia coli TopoIII activity. Nucleic Acids Res 33: 5415-5425.
23. Liu, H., Coulthurst, S.J., Pritchard, L., Hedley, P.E., Ravensdale, M., Humphris, S., etal. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4: e1000093.
24. Lovell, H.C., Jackson, R.W., Mansfield, J.W., Godfrey, S.A.C., Hancock, J.T., Desikan, R., and Arnold, D.L. (2011) In planta conditions induce genomic changes in Pseudomonas syringae pv. phaseolicola. Mol Plant Pathol 12: 167-176.
25. Luttinger, A. (1995) The twisted life of DNA in the cell-bacterial topoisomerases. Mol Microbiol 15: 601-606.
26. McCullagh, P., and Nelder, J.A. (1989) Generalized Linear Models. London: Chapman & Hall.
27. Mohd-Zain, Z., Turner, S.L., Cerdeño-Tárraga, A.M., Lilley, A.K., Inzana, T.J., Duncan, A.J., etal. (2004) Transferable antibiotic resistance elements in Haemophilus influenzae share a common evolutionary origin with a diverse family of syntenic genomic islands. J Bacteriol 186: 8114-8122.
28. Moon, K., Sonnenburg, J., and Salyers, A.A. (2007) Unexpected effect of a Bacteroides conjugative transposon, CTnDOT, on chromosomal gene expression in its bacterialhost. Mol Microbiol 64: 1562-1571.
29. Morschhäuser, J., Köhler, G., Ziebuhr, W., Blum-Oehler, G., Dobrindt, U., and Hacker, J. (2000) Evolution of microbial pathogens. Philos Trans R Soc Lond B Biol Sci 355: 695-704.
30. Nitiss, J.L. (1998) Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim Biophys Acta 1400: 63-81.
31. Rampakakis, E., Gkogkas, C., Paola, D.D., and Zannis-Hadjopoulos, M. (2010) Replication initiation and DNA topology: the twisted life of the origin. J Cell Biochem 110: 35-43.
32. Ramsay, J.P., Sullivan, J.T., Stuart, G.S., Lamont, I.L., and Ronson, C.W. (2006) Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62: 723-734.
33. Sakellaris, H., Luck, S.N., Al-Hasani, K., Rajakumar, K., Turner, S.A., and Adler, B. (2004) Regulated site-specific recombination of the she pathogenicity island of Shigella flexneri. Mol Microbiol 52: 1329-1336.
34. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35. Schofield, M.A., Agbunag, R., Michaels, M.L., and Miller, J.H. (1992) Cloning and sequencing of Escherichia coli mutR shows its identity to topB, encoding topoisomerase III. J Bacteriol 174: 5168-5170.
36. Sentchilo, V., Czechowska, K., Pradervand, N., Minoia, M., Miyazaki, R., and van der Meer, J.R. (2009) Intracellular excision and reintegration dynamics of the ICEclc genomic island of Pseudomonas knackmussii sp. strain B13. Mol Microbiol 72: 1293-1306.
37. Shen, K., Sayeed, S., Antalis, P., Gladitz, J., Ahmed, A., Dice, B., etal. (2006) Extensive genomic plasticity in Pseudomonas aeruginosa revealed by identification and distribution studies of novel genes among clinical isolates. Infect Immun 74: 5272-5283.
38. Spell, R.M., and Holm, C. (1994) Nature and distribution of chromosomal intertwinings in Saccharomyces cerevisiae. Mol Cell Biol 14: 1465-1476.
39. Stirling, C.J., Colloms, S.D., Collins, J.F., Szatmari, G., and Sherratt, D.J. (1989) xerB, an Escherichia coli gene required for plasmid ColE1 site-specific recombination, is identical to pepA, encoding aminopeptidase A, a protein with substantial similarity to bovine lens leucine aminopeptidase. EMBO J 8: 1623-1627.
40. Stupina, V.A., and Wang, J.C. (2005) Viability of Escherichia coli topA mutants lacking DNA topoisomerase I. J Biol Chem 280: 355-360.
41. Sutanto, Y., Shoemaker, N.B., Gardner, J.F., and Salyers, A.A. (2002) Characterization of Exc, a novel protein required for the excision of Bacteroides conjugative transposon. Mol Microbiol 46: 1239-1246.
42. Sutanto, Y., DiChiara, J.M., Shoemaker, N.B., Gardner, J.F., and Salyers, A.A. (2004) Factors required in vitro for excision of the Bacteroides conjugative transposon, CTnDOT. Plasmid 52: 119-130.
43. Swofford, D.L. (1998) PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0 Beta. Sunderland, MA: Sinauer Associates.
44. Takle, G.W., Toth, I.K., and Brurberg, M.B. (2007) Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum. BMC Plant Biol 7: 50.
45. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
46. Toth, I.K., Mulholland, V., Cooper, V., Bentley, S., Shih, Y.L., Perombelon, M.C.M., and Salmond, G.P.C. (1997) Generalized transduction in the potato blackleg pathogen Erwinia carotovora subsp. atroseptica by bacteriophage φ{symbol}M1. Microbiology 143: 2433-2438.
47. Tse-Dinh, Y.C. (1998) Bacterial and archeal type I topoisomerases. Biochim Biophys Acta 1400: 19-27.
48. Uematsu, N., Eda, S., and Yamamoto, K. (1997) An Escherichia coli topB mutant increases deletion and frameshift mutations in the supF target gene. Mutat Res 383: 223-230.
49. Wallis, J.W., Chrebet, G., Brodsky, G., Rolfe, M., and Rothstein, R. (1989) Ahyper-recombination mutation in Saccharomyces cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409-419.
50. Whoriskey, S.K., Schofield, M.A., and Miller, J.H. (1991) Isolation and characterization of Escherichia coli mutants with altered rates of deletion formation. Genetics 127: 21-30.
51. Wu, H.Y., Shyy, S., Wang, J.C., and Liu, L.F. (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell 53: 433-440.