Atypical transcriptional regulation and role of a new toxin-antitoxin-like module and its effect on the lipid composition of Bradyrhizobium japonicum

Molecular Plant-Microbe Interactions

Volumn 23, Issue 5, 2010, Pages 638-650

  Miclea, Paul S ^a   Péter, Mária ^a   Végh, Gergely ^a   Cinege, Gyöngyi ^a   Kiss, Ernö ^a   Váró, György ^a   Horváth, Ibolya ^a   Dusha, Liona ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL PROTEIN; BACTERIAL TOXIN; CARBON; LIPOPOLYSACCHARIDE; NITROGEN; PHOSPHOLIPID;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BIOMECHANICS; BRADYRHIZOBIUM; CELL DIVISION; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; MICROBIAL VIABILITY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PROMOTER REGION; SYMBIOSIS;

AMINO ACID SEQUENCE; ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BASE SEQUENCE; BIOMECHANICS; BRADYRHIZOBIUM; CARBON; CELL DIVISION; CULTURE MEDIA; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; GENOME, BACTERIAL; LIPID METABOLISM; LIPOPOLYSACCHARIDES; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MUTATION; NITROGEN; OPERON; PHENOTYPE; PHOSPHOLIPIDS; PROMOTER REGIONS, GENETIC; SYMBIOSIS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM JAPONICUM;

EID: 77950574625     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-23-5-0638     Document Type: Article

References (66)

1. Alting-Mees, M. A., and Short, J. M. 1989. pBluescript II: Gene mapping vectors. Nucleic Acids Res. 17:9494.
2. Amitai, S., Yassin, Y., and Engelberg-Kulka, H. 2004. MazF-mediated cell death in Escherichia coli: A. point of no return. J. Bacteriol. 186:8295-8300.
3. Arcus, V. L., Backbro, K., Roos, A., Daniel, E. L., and Baker, E. N. 2004. Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J. Biol. Chem. 279:16471-16478.
4. Bálint, Z., Krizbai, I. A., Wilhelm, L, Farkas, A. E., Pardutz, A., Szegletes, Z., and Varo, G. 2007. Changes induced by hyperosmotic mannitol in cerebral endothelial cells: An atomic force microscopic study. Eur. Biophys. J. 36:113-120.
5. Bodogai, M., Ferenczi, S., Bashtovyy, D., Miclea, P., Papp, P., and Dusha, I. 2006. The ntrPR operon of Sinorhizobium meliloti is organized and functions as a toxin-antitoxin module. Mol. Plant-Microbe Interact. 19:811-822.
6. Boncompagni, E., Osteras, M., Poggi, M. C., and Le Rudulier, D. 1999. Occurrence of choline and glycine betaine uptake and metabolism in. the family Rhizobiaceae and their roles in osmoprotection. Appl. Enviran. Microbiol. 65:2072-2077.
7. Brooun, A., Liu, S., and Lewis, K. 2000. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 44:640-646.
8. Bunker, R. D., McKenzie, J. L., Baker, E. N., and Arcus, V. L. 2008. Crystal structure of PAEO151 from Pyrobaculum aerophilum, a PIN-domain (VapC) protein from a toxin-antitoxin operon. Proteins 72:510-518.
9. Buts, L., Lah, J., Dao-Thi, M. H., Wyns, L., and Loris, R. 2005. Toxinantitoxin modules as bacterial metabolic stress managers. Trends Bioehem. Sci. 30:672-679.
10. Carrion, M., Bhat, U. R., Rheus, B., and Carlson, R. W. 1990. Isolation and characterization of the lipopolysaccharides from Bradyrhizobium. japonicum. J. Bacteriol. 172:1725-1731.
11. Christensen, S. K., Mikkelsen, M., Pedersen, K., and Gerdes, K. 2001. RelE, a global inhibitor of translation, is activated during nutritional stress. Proc. Natl. Acad. Sci. U.S.A. 98:14328-14333.
12. Danilova, L. V., Gelfand, M. S., Lyubetsky, V. A., and Laikova, O. N. 2003. Computer-assisted analysis of regulation of the glycerol-3phosphate metabolism in genomes of Proteobacteria. Mol. Biol. 37:716-722.
13. Dénarié, J., Debellé, F., and Promé, J.-C. 1996. Rhizobium lipochitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65:503-535.
14. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D. R. 1980. Broad host range DNA cloning system for gram-negative bacteria: Construction, of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. U.S.A. 77:7347-7351.
15. Donegan, N. P., and Cheung, A. L. 2009. Regulation of the mazEF toxinantitoxin module in Staphylococcus aureus and its impact on sigB expression. J. Bacteriol. 191:2795-2805.
16. Élo, P., Semsey, S., Kereszt, A., Nagy, T., Papp, P., and Orosz, L. 1998. Integrative promoter cloning plasmid vectors for Rhizobium meliloti. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 159:7-13.
17. Gerdes, K. 2000. Toxin-antitoxin molecules may regulate synthesis of macromolecules during nutritional stress. J. Bacteriol. 182:561-572. (Pubitemid 30053984)
18. Gerdes, K., Christensen, S. K., and Lobner-Olesen, A. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
19. Gibson, K. E., Kobayashi, H., and Walker, G. C.2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42:413-441
20. Guerinot, M. L., Meidl, E. J., and Plessner, O. 1990. Citrate as a siderophore in Bradyrhizobium japonicum. J. Bacteriol. 172:3298-3303.
21. Hacker, S., Sohlenkamp, C., Aktas, M., Geiger, O., and Narberhaus, F. 2008. Multiple phospholipid N-memyltransferases with distinct substrate specificities are encoded in Bradyrhizobium. japonicum. J. Bacteriol. 190:571-580.
22. Hahn, M., and Hennecke, H. 1984. Localized mutagenesis in Rhizobium japonicum. Mol. Gen. Genet. 193:46-52.
23. Hayes, F. 2003. Toxins-antitoxins: Plasmid maintenance, programmed cell death, and cell cycle arrest. Science. 301:1496-1499. (Pubitemid 37128533)
24. Hazan, R., Sat, B., and Engelberg-Kulka, H. 2004. Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol. 186:3663-3669.
25. Horváth, L, Mansourian, A. R., Vigh, L., Thomas, P. G., Joó, F., and Quinn, P. J. 1986. Homogeneous catalytic hydrogenation of the polar lipids of pea chloroplasts in situ and the effects on lipid polymorphism. Chem. Phys. Lipids 39:251-264.
26. Jensen, R. B., and Gerdes, K. 1995. Programmed cell death in bacteria: Proteic plasmid stabilization systems. Mol. Microbiol. 17:205-210.
27. Jones, K. M., Kobayashi, H., Davies, B. W, Taga, M. E., and Walker, G. C. 2007. How rhizobial symbionts invade plants: The SinorhizobiumMedicago model. Nat. Rev. 5:619-633.
28. Jørgensen, M. G., Pandey, D. P., Jaskolska, M., and Gerdes, K. 2009. HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. J. Bacteriol. 191:1191-1199.
29. Kates, M. 1986. Techniques in lipidology. Pages 232-254 in: Isolation, and Identification of Lipids, 2nd ed. R. H. Burdon, P. H. van Knippenberg, eds. Elsevier, Amsterdam.
30. Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K. 2004. Specialized persister cells and the mechanism of multidrug tolerance in. Escherichia coli. J. Bacteriol. 186:8172-8180. (Pubitemid 39603206)
31. Kiss E, Reuhs, B. L., Kim, J. S., Kereszt, A., Petrovics, G., Putnoky, P., Dusha, I., Carlson, R. W, and Kondorosi, A. 1997. The rkpGHI and -J genes are involved in capsular polysaccharide production by Rhizobium meliloti. J. Bacteriol. 179:2132-2140. (Pubitemid 27146865)
32. Korch, S. B., Contreras, H., and Clark-Curtiss, J. E. 2009. Three Mycobacterium tuberculosis Rel toxin-antitoxin modules inhibit mycobacterial growth and are expressed in infected human macrophages. J. Bacteriol. 191:1618-1630.
33. Krauss, J. H., Weckesser, J., and Mayer, H. 1988. Electrophoretic analysis of lipopolysaccharides of purple nonsulfur bacteria. Int. J. Syst. Bacteriol. 38:157-163.
34. Lehnherr, H., Magnuson, R., Jafri, S., and Yarmolinsky, M. B. 1993. Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. Mol. Biol. 233:414-428.
35. Lodeiro, A. R., and Favelukes, G. 1999. Early interactions of Bradyrhizobium japonicum and soybean roots: Specificity in the process of adsorption. Soil Biol. Biochem. 31:1405-1411.
36. Lewis, K. 2005. Persister cells and the riddle of biofilm survival. Biochemistry-Moscow 70:267-274. (Pubitemid 40512338)
37. Magnuson, R., and Yarmolinsky, M. B. 1998. Corepression of the P1 addiction operon by Phd and Doc. J. Bacteriol. 180:6342-6351. (Pubitemid 28544268)
38. Akarova, K. S., Aravind, L., Galperin, M. Y., Grishin, N. V., Tatusov, R. L., Wolf, Y. L, and Koonin, E. V. 1999. Comparative genomics of the Archaea (Euryarchaeota): Evolution of conserved protein families, the stable core, and the variable shell. Genome Res. 9:608-628.
39. Maniatis, T, Fritsch, E. E, and Sambrook, J. E. 1982. Molecular Cloning. A laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, U.S.A.
40. Marianovsky, L, Aizenman, E., Engelberg-Kulka, H., and Glaser, G. 2001. The regulation of the Escherichia coli mazEF promoter involves an unusual alternating palindrome. J. Biol. Chem. 276:5975-5984.
41. Martinez-Morales, F., Schobert, M., López-Lara I. M., and Geiger O. 2003. Pathways for phosphatidylcholine biosynthesis in bacteria. Microbiology 149:3461-3471.
42. Mattison, K., Wilbur, J. C, So, M., and Brennan, R. G. 2006. Structure of FitAB from. Neisseria gonorrhoeae bound to DNA reveals a tetramer of toxin-antitoxin heterodimers containing PIN domains and ribbon-helixhelix motifs. J. Biol. Chem. 281:37942-37951.
43. Mileykovskaya, E., and Dowhan, W. 2005. Role of membrane lipids in bacterial division-site selection. Curr. Opin. Microbiol. 8:135-142.
44. Mine, N., Guglielmini, J., Wilbaux, M., and Van Melderen, M. 2009. The decay of the chromosomally encoded ccdD157 toxin-antitoxin system in. the Escherichia coli species. Genetics, 181:1557-1566.
45. Oláh, B., Kiss, E., Gyorgypál, Z., Borzi, J., Cinege, G., Csanádi, G., Batut, J., Kondorosi, A., and Dusha, I. 2001. Mutation in the ntrR gene, a member of the vap gene family, increases the symbiotic efficiency of Sinorhizobium meliloti. Mol. Plant-Microbe Interact. 14:887-894. (Pubitemid 32575666)
46. 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. (Pubitemid 41430517)
47. 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.
48. Pedersen, K., Zavialov, A. V, Pavlov, M. Y, Elf, J., Gerdes, K., and Ehrenberg, M. 2003. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell. 112:131-140.
49. Puskás, L. G., Nagy, Z. B., Kelemen, J. Z., Rüberg, S., Bodogai, M., Becker, A., and Dusha, I. 2004. Wide-range transcriptional modulating effect of ntrR under microaerobiosis in Sinorhizobium meliloti. Mol. Gen. Genomics 272:275-289.
50. Regensburger, B., and Hennecke, H. 1983. RNA polymerase from Rhizobium japonicum. Arch. Microbiol. 135:103-109.
51. Rietveld, A. G., Killian, J. A, Dowhan, W, and de Kruijff, B. 1993. Polymorphic regulation of membrane phospholipid composition in Escherichia coli. J. Biol. Chem. 15:12427-12433
52. Sat, B., Hazan, R., Fisher, T, Khaner, H., Glaser, G., and EngelbergKulka, H. 2001. Programmed cell death in Escherichia coli: Some antibiotics can trigger mazEF lethality. J. Bacteriol. 183:2041-2045. (Pubitemid 32226000)
53. Smith, J. A., and Magnuson, R. D. 2004. Modular organization of the Phd repressor/antitoxin protein. J. Bacteriol. 186:2692-2698.
54. Stacey, G., So, J. S., Roth, L. E., Lakshmi, S. K. B., and Carlson, R. W. 199.1. A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol. Plant-Microbe Interact. 4:332-340.
55. Tsilibaris, V., Maenhaut-Michel, G., Mine, N., and Van. Melderen, L. 2007. What is the benefit of Escherichia coli of having multiple toxin-antitoxin systems in its genome? J. Bacteriol. 189:6101-6108.
56. Vigh, L., Escribá, P. V, Sonnleitner, A., Sonnleitner, M., Piotto, S., Maresca, B., Horváth L, and John L. Harwood. 2005. The significance of lipid composition for membrane activity: New concepts and ways of assessing function. Progr. Lipid. Res. 44:303-344.
57. Vincent, J. M. 1970. A. manual for the practical study of root nodule bacteria. International Biological Program Handbook 15. Blackwell Scientifie Publications, Oxford.
58. Wilhelm, I., Parkas, A. E., Nagyöszi, P., Varó, G., Bálint, Z., Végh, G. A., Couraud, P-O., Romero, I. A., Weksler, B., and Krizbai, I. A. 2007. Regulation of cerebral endothelial cell morphology by extracellular calcium. Phys. Med. Biol. 52:6261-6274.
59. Yang, B., and Larson, T. J. 1996. Action at a distance for negative control of transcription of the glpD gene encoding sn-glycerol 3-phosphate dehydrogenase of Escherichia coli K-12. J. Bacteriol. 178:7090-7098. (Pubitemid 26424620)
60. Yang, B., and Larson, T. J. 1998. Multiple promoters are responsible for transcription of the glpEGR operon of Escherichia coli K-12. Biochim. Biophys. Acta 1396:114-126.
61. Ye, S. Z., and Larson, T. J. 1988. Structures of the promoter and operator of the glpD gene encoding aerobic sn-glycerol-3-phosphate dehydrogenase oí Escherichia coli K-12. J. Bacteriol. 170:4209-4215.
62. Zhang, Y, Zhang, J., Hoeflich, K. P., Ikura, M., Qing, G., and Inouye, M. 2003. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coll Mol. Cell 12:913-923. (Pubitemid 37352784)
63. BacMap Genome Atlas: wishart.biology.ualberta.ca/BacMap
64. European Molecular Biology Laboratory-European Bioinformatics Institute ClustalW2 website: www.ebi.ac.uk/Tools/clustalw2/index.html
65. Kazusa Research Institute RhizoBase webpage: bacteria.kazusa.or.jp/rh. izobase
66. Queens Universitys Promscan: molbiol-tools.ca/promscan