Characterisation of the stbD/E toxin-antitoxin system of pEP36, a plasmid of the plant pathogen Erwinia pyrifoliae

Plasmid

Volumn 70, Issue 2, 2013, Pages 216-225

  Unterholzner, Simon J ^a   Hailer, Barbara ^a   Poppenberger, Brigitte ^a   Rozhon, Wilfried ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Erwinia pyrifoliae; PEP36; Protein synthesis; Toxin antitoxin

Indexed keywords

ANTITOXIN; BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL RNA; BACTERIAL TOXIN; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIABILITY; BACTERIUM CULTURE; CELL CYCLE ARREST; CELL GROWTH; CELL SIZE; CONTROLLED STUDY; DNA SYNTHESIS; ERWINIA; ERWINIA PYRIFOLIAE; NONHUMAN; PLANT DISEASE; PLASMID; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN STABILITY; PROTEIN SYNTHESIS; RNA SYNTHESIS; SEQUENCE HOMOLOGY;

ERWINIA PYRIFOLIAE; MALUS X DOMESTICA; PYRUS; PYRUS PYRIFOLIA VAR. CULTA;

EID: 84881025452     PISSN: 0147619X     EISSN: 10959890     Source Type: Journal    
DOI: 10.1016/j.plasmid.2013.04.002     Document Type: Article

References (70)

1. Adams J., Kinney T., Thompson S., Rubin L., Helling R.B. Frequency-dependet selection for plasmid-containing cells of Escherichia coli. Genetics 1979, 91:627-637.
2. Alonso J.C., Balsa D., Cherny I., Espinosa M., Francuski D., Gazit E., Gerdes K., Hitchin E., Martin M.T., Nieto C., Overweg K., Pellicer T., Saenger W., Welfe W., Welfe H., Wells J.M. Bacterial toxin-antitoxin systems as targets for the development of novel antibiotics. Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition 2007, 313-329. ASM Press, Washington DC. R.A. Bonomo, M.E. Tolmasky (Eds.).
3. Bagnara A.S., Finch L.R. Relationships between intracellular contents of nucleotides and 5-phosphoribosyl 1-pyrophosphate in Escherichia coli. Eur. J. Biochem. 1973, 36:422-427.
4. Berridge M.V., Tan A.S. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 1993, 303:474-482.
5. Blower T.R., Pei X.Y., Short F.L., Fineran P.C., Humphreys D.P., Luisi B.F., Salmond G.P. A processed noncoding RNA regulates an altruistic bacterial antiviral system. Nat. Struct. Mol. Biol. 2011, 18:185-190.
6. Blower T.R., Short F.L., Rao F., Mizuguchi K., Pei X.Y., Fineran P.C., Luisi B.F., Salmond G.P. Identification and classification of bacterial Type III toxin-antitoxin systems encoded in chromosomal and plasmid genomes. Nucleic Acids Res. 2012, 40:6158-6173.
7. Christensen S.K., Gerdes K. RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol. Microbiol. 2003, 48:1389-1400.
8. Cooper T.F., Heinemann J.A. Postsegregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids. Proc. Natl. Acad. Sci. USA 2000, 97:12643-12648.
9. Falkenstein H., Zeller W., Geider K. The 29 kb plasmid common in strains of Erwinia amylovora, modulates development of fire blight symptoms. J. Gen. Microbiol. 1989, 135:2643-2650.
10. Fiebig A., Castro Rojas C.M., Siegal-Gaskins D., Crosson S. Interaction specificity, toxicity and regulation of a paralogous set of ParE/RelE-family toxin-antitoxin systems. Mol. Microbiol. 2010, 77:236-251.
11. Fineran P.C., Blower T.R., Foulds I.J., Humphreys D.P., Lilley K.S., Salmond G.P. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. USA 2009, 106:894-899.
12. Fozo E.M., Hemm M.R., Storz G. Small toxic proteins and the antisense RNAs that repress them. Microbiol. Mol. Biol. Rev. 2008, 72:579-589.
13. Fozo E.M., Makarova K.S., Shabalina S.A., Yutin N., Koonin E.V., Storz G. Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res. 2010, 38:3743-3759.
14. Galvani C., Terry J., Ishiguro E.E. Purification of the RelB and RelE proteins of Escherichia coli: RelE binds to RelB and to ribosomes. J. Bacteriol. 2001, 183:2700-2703.
15. Geider K. Exopolosaccharides of Erwinia amylovora: structure, biosynthesis, regulation. Fire Blight. The Disease and its Causative Agent Erwinia amylovora 2000, 117-140. CABI Publishing, Oxford, UK. J.L. Vanneste (Ed.).
16. Gerdes K., Christensen S.K., Lobner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 2005, 3:371-382.
17. Gerdes K., Howard M., Szardenings F. Pushing and pulling in prokaryotic DNA segregation. Cell 2010, 141:927-942.
18. Gerdes K., Gultyaev A.P., Franch T., Pedersen K., Mikkelsen N.D. Antisense RNA-regulated programmed cell death. Annu. Rev. Genet. 1997, 31:1-31.
19. Gronlund H., Gerdes K. Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes. J. Mol. Biol. 1999, 285:1401-1415.
20. Guglielmini J., Szpirer C., Milinkovitch M.C. Automated discovery and phylogenetic analysis of new toxin-antitoxin systems. BMC Microbiol. 2008, 8:104.
21. Hallez R., Geeraerts D., Sterckx Y., Mine N., Loris R., Van Melderen L. New toxins homologous to ParE belonging to three-component toxin-antitoxin systems in Escherichia coli O157:H7. Mol. Microbiol. 2010, 76:719-732.
22. Hayes F. A family of stability determinants in pathogenic bacteria. J. Bacteriol. 1998, 180:6415-6418.
23. Hildebrand M., Aldridge P., Geider K. Characterization of hns genes from Erwinia amylovora. Mol. Genet. Genomics 2006, 275:310-319.
24. Inoue H., Nojima H., Okayama H. High efficiency transformation of Escherichia coli with plasmids. Gene 1990, 96:23-28.
25. James R., Gillies N.E. The sensitivity of suppressed and unsuppressed lon strains of Escherichia coli to chemical agents which induce filamentation. J. Gen. Microbiol. 1973, 76:429-436.
26. Jiang Y., Pogliano J., Helinski D.R., Konieczny I. ParE toxin encoded by the broad-host-range plasmid RK2 is an inhibitor of Escherichia coli gyrase. Mol. Microbiol. 2002, 44:971-979.
27. Jorgensen M.G., Pandey D.P., Jaskolska M., Gerdes K. HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. J. Bacteriol. 2009, 191:1191-1199.
28. Kamphuis M.B., Monti M.C., van den Heuvel R.H., Lopez-Villarejo J., Diaz-Orejas R., Boelens R. Structure and function of bacterial kid-kis and related toxin-antitoxin systems. Protein Pept. Lett. 2007, 14:113-124.
29. Kim W.S., Gardan L., Rhim S.L., Geider K. Erwinia pyrifoliae sp. nov., a novel pathogen that affects Asian pear trees (Pyrus pyrifolia Nakai). Int. J. Syst. Bacteriol. 1999, 49:899-906.
30. Kim W.S., Schollmeyer M., Nimtz M., Wray V., Geider K. Genetics of biosynthesis and structure of the capsular exopolysaccharide from the Asian pear pathogen Erwinia pyrifoliae. Microbiology 2002, 148:4015-4024.
31. Lauffenburger D.A. Model for the dynamics of colicin plasmids in continuous culture. Ann. N. Y. Acad. Sci. 1986, 469:97-103.
32. Leplae R., Geeraerts D., Hallez R., Guglielmini J., Dreze P., Van Melderen L. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res. 2011, 39:5513-5525.
33. Lioy V.S., Rey O., Balsa D., Pellicer T., Alonso J.C. A toxin-antitoxin module as a target for antimicrobial development. Plasmid 2010, 63:31-39.
34. Lioy V.S., Machon C., Tabone M., Gonzalez-Pastor J.E., Daugelavicius R., Ayora S., Alonso J.C. The eta toxin induces a set of protective responses and dormancy. PLoS One 2012, 7:e30282.
35. Liu M., Zhang Y., Inouye M., Woychik N.A. Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit. Proc. Natl. Acad. Sci. USA 2008, 105:5885-5890.
36. Llop P., Donat V., Rodriguez M., Cabrefiga J., Ruz L., Palomo J.L., Montesinos E., Lopez M.M. An indigenous virulent strain of Erwinia amylovora lacking the ubiquitous plasmid pEA29. Phytopathology 2006, 96:900-907.
37. Llop P., Cabrefiga J., Smits T.H., Dreo T., Barbe S., Pulawska J., Bultreys A., Blom J., Duffy B., Montesinos E., Lopez M.M. Erwinia amylovora novel plasmid pEI70: complete sequence, biogeography, and role in aggressiveness in the fire blight phytopathogen. PLoS One 2011, 6:e28651.
38. Maes M., Orye K., Bobev S., Devreese B., Van Beeumen J., De Bruyn A., Busson R., Herdewijn P., Morreel K., Messens E. Influence of amylovoran production on virulence of Erwinia amylovora and a different amylovoran structure in E. amylovora isolates from Rubus. Eur. J. Plant Pathol. 2001, 107:839-844.
39. Masuda H., Tan Q., Awano N., Wu K.P., Inouye M. YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol. Microbiol. 2012, 84:979-989.
40. McGhee G.C., Jones A.L. Complete nucleotide sequence of ubiquitous plasmid pEA29 from Erwinia amylovora strain Ea88: gene organization and intraspecies variation. Appl. Environ. Microbiol. 2000, 66:4897-4907.
41. McGhee G.C., Schnabel E.L., Maxson-Stein K., Jones B., Stromberg V.K., Lacy G.H., Jones A.L. Relatedness of chromosomal and plasmid DNAs of Erwinia pyrifoliae and Erwinia amylovora. Appl. Environ. Microbiol. 2002, 68:6182-6192.
42. Mohammadi M. Enhanced colonization and pathogenicity of Erwinia amylovora strains transformed with the near-ubiquitous pEA29 plasmid on pear and apple. Plant Pathol. 2010, 59:252-261.
43. Mohammadi M., Moltmann E., Zeller W., Geider K. Characterisation of naturally occuring Erwinia amylovora strains lacking the common plasmid pEA29 and their detection with real-time PCR. Eur. J. Plant Pathol. 2009, 124:293-302.
44. Muñoz-Gómez A.J., Lemonnier M., Santos-Sierra S., Berzal-Herranz A., Díaz-Orejas R. RNase/anti-RNase activities of the bacterial parD toxin-antitoxin system. J. Bacteriol. 2005, 187:3151-3157.
45. Mutschler H., Gebhardt M., Shoeman R.L. A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol. 2011, 9:e1001033.
46. Neubauer C., Gao Y.G., Andersen K.R., Dunham C.M., Kelley A.C., Hentschel J., Gerdes K., Ramakrishnan V., Brodersen D.E. The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell 2009, 139:1084-1095.
47. Nieto C., Sadowy E., de la Campa A.G., Hryniewicz W., Espinosa M. The relBE2Spn toxin-antitoxin system of Streptococcus pneumoniae: role in antibiotic tolerance and functional conservation in clinical isolates. PLoS One 2010, 5:e11289.
48. Nimtz M., Mort A., Domke T., Wray V., Zhang Y., Qiu F., Coplin D., Geider K. Structure of amylovoran, the capsular exopolysaccharide from the fire blight pathogen Erwinia amylovora. Carbohydr. Res. 1996, 287:59-76.
49. Pandey D.P., Gerdes K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 2005, 33:966-976.
50. Pedersen K., Zavialov A.V., Pavlov M.Y., Elf J., Gerdes K., Ehrenberg M. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 2003, 112:131-140.
51. Rhim S.L., Vösch B., Gardan L., Paulin J.-P., Langlotz C., Kim W.S., Geider K. Erwinia pyrifoliae, an Erwinia species different from Erwinia amylovora, causes a necrotic disease of Asian pear trees. Plant Pathol. 1999, 48:514-520.
52. Rozhon W., Khan M., Poppenberger B. The natural antibiotic resistances of the enterobacteriaceae Rahnella and Ewingella. Antibiotic Resistant Bacteria 2012, 77-104. InTech. M. Pana (Ed.).
53. Rozhon W., Khan M., Poppenberger B. Identification of the region required for maintaining pHW126 in its monomeric form. FEMS Microbiol. Lett. 2012, 331:89-96.
54. Rozhon W., Khan M., Petutschnig E., Poppenberger B. Identification of cis- and trans-acting elements in pHW126, a representative of a novel group of rolling circle plasmids. Plasmid 2011, 65:70-76.
55. Rozhon W.M., Petutschnig E.K., Jonak C. Isolation and characterization of pHW15, a small cryptic plasmid from Rahnella genomospecies 2. Plasmid 2006, 56:202-215.
56. Sambrook J., Russell D.W. Molecular Cloning, A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
57. Schumacher M.A., Piro K.M., Xu W., Hansen S., Lewis K., Brennan R.G. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 2009, 323:396-401.
58. Sjulin T.M., Beer S.V. Mechanism of wilting induction by amylovoran in cotoneaster shoots and its relation to wilting of shoots infected by Erwinia amylovora. Phytopathol 1977, 68:89-94.
59. Smith A.B., López-Villarejo J., Diago-Navarro E., Mitchenall L.A., Barendregt A., Heck A.J., Lemonnier M., Anthony Maxwell A., Díaz-Orejas R. A common origin for the bacterial toxin-antitoxin systems parD and ccd, suggested by analyses of toxin/target and toxin/antitoxin interactions. PLoS One 2012, 7:e46499.
60. Summers D.K., Sherratt D.J. Multimerization of high copy number plasmids causes instability: CoIE1 encodes a determinant essential for plasmid monomerization and stability. Cell 1984, 36:1097-1103.
61. Summers D.K., Beton C.W., Withers H.L. Multicopy plasmid instability: the dimer catastrophe hypothesis. Mol. Microbiol. 1993, 8:1031-1038.
62. Szekeres S., Dauti M., Wilde C., Mazel D., Rowe-Magnus D.A. Chromosomal toxin-antitoxin loci can diminish large-scale genome reductions in the absence of selection. Mol. Microbiol. 2007, 63:1588-1605.
63. Van Melderen L. Molecular interactions of the CcdB poison with its bacterial target, the DNA gyrase. Int. J. Med. Microbiol. 2002, 291:537-544.
64. Wang H., Cheng H., Wang F., Wei D., Wang X. An improved 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) reduction assay for evaluating the viability of Escherichia coli cells. J. Microbiol. Methods 2010, 82:330-333.
65. Wang X., Lord D.M., Cheng H.Y., Osbourne D.O., Hong S.H., Sanchez-Torres V., Quiroga C., Zheng K., Herrmann T., Peti W., Benedik M.J., Page R., Wood T.K. A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol. 2012, 8:855-861.
66. Williams J.J., Hergenrother P.J. Artificial activation of toxin-antitoxin systems as an antibacterial strategy. Trends Microbiol. 2012, 20:291-298.
67. Williams S.C., Hong Y., Danavall D.C.A., Howard-Jones M.H., Gibson D., Frischer M.E., Verity P.G. Distinguishing between living and nonliving bacteria: Evaluation of the vital stain propidium iodide and its combined use with molecular probes in aquatic samples. J. Microbiol. Methods 1998, 32:225-246.
68. Winther K.S., Gerdes K. Ectopic production of VapCs from Enterobacteria inhibits translation and trans-activates YoeB mRNA interferase. Mol. Microbiol. 2009, 72:918-930.
69. Wozniak R.A., Waldor M.K. A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet. 2009, 5:e1000439.
70. Zhang Y., Zhang J., Hoeflich K.P., Ikura M., Qing G., Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell 2003, 12:913-923.