Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti

Journal of Bacteriology

Volumn 188, Issue 21, 2006, Pages 7617-7625

  Domínguez Ferreras, Ana ^a   Pérez Arnedo, Rebeca ^a   Becker, Anke ^b   Olivares, José ^a   Soto, María J ^a   Sanjuán, Juan ^a  

^a CSIC   (Spain)

^b BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHLORIDE; SUCROSE; TRANSCRIPTOME;

ADAPTATION; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM CULTURE; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE REPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; OSMOLARITY; OSMOTIC SHOCK; OSMOTIC STRESS; PLASMID; PLASMID PSYMB; PRIORITY JOURNAL; REPLICON; SINORHIZOBIUM MELILOTI; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; CHROMOSOMES, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HYPERTONIC SOLUTIONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOTIC PRESSURE; PLASMIDS; RNA, BACTERIAL; RNA, MESSENGER; SINORHIZOBIUM MELILOTI; SODIUM CHLORIDE; SUCROSE;

SINORHIZOBIUM MELILOTI;

EID: 33750455848     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00719-06     Document Type: Article

References (67)

1. Barnett, M. J., C. J. Toman, R. F. Fisher, and S. R. Long. 2004. A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proc. Natl. Acad. Sci. USA 101:16636-16641.
2. Becker, A., H. Bergès, E. Krol, C. Bruand, S. Rüberg, D. Capela, E. Lauber, E. Meilhoc, F. Ampe, F. J. de Bruijn, J. Fourment, A. Francez-Charlot, D. Kahn, H. Küster, C. Liebe, A. Pühler, S. Weidner, and J. Batut. 2004. Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol. Plant-Microbe Interact. 17:292-303.
3. Beringer, J. E. 1974. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:188-198.
4. Bohin, J.-P. 2000. Osmoregulated periplasmic glucans in proteobacteria. FEMS Microbiol. Lett. 186:11-19.
5. Butler, Y. X., Y. Abhayawardhane, and G. C. Stewart. 1993. Amplification of the Bacillus subtilis maf gene results in arrested septum formation. J. Bacteriol. 175:3139-3145.
6. 2552 23S ribosomal RNA metyltransferase RrmJ/FTSJ. Biochem. Biophys. Res. Commun. 271:714-718.
7. Charles, T. C., and T. M. Finan. 1991. Analysis of a 1600-kilobase Rhizobium meliloti megaplasmid using defined deletions generated in vivo. Genetics 127:5-20.
8. Davey, M. E., and F. J. de Bruijn. 2000. A homologue of the tryptophan-rich sensory protein TspO and FixL regulate a novel nutrient deprivation-induced Sinorhizobium meliloti locus. Appl. Environ. Microbiol. 66:5353-5359.
9. DeRisi, J. L., V. R. Iyer, and P. O. Brown. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:680-686.
10. Djordjevic, M. A., H. C. Chen, S. Natera, G. Van Noorden, C. Menzel, S. Taylor, C. Renard, O. Geiger, the Sinorhizobium DNA Sequencing Consortium, and G. F. Weiller. 2003. A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation. Mol. Plant-Microbe Interact. 16:508-524.
11. Dondrup, M., A. Goesmann, D. Bartels, J. Kalinowski, L. Krause, B. Linke, O. Rupp, A. Sczyrba, A. Pühler, and F. Meyer. 2003. EMMA: a platform for consistent storage and efficient analysis of microarray data. J. Biotechnol. 106:135-146.
12. El-Shinnawi, M. M., N. A. El-Saify, and T. M. Waly. 1989. Influence of the ionic form of mineral salts on growth of faba bean and Rhizobium leguminosarum. World J. Microbiol. Biotechnol. 5:247-254.
13. - mutants of Rhizobium meliloti. J. Bacteriol. 170:474-477.
14. 2-fixing endosymbiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA 98:9889-9894.
15. Galibert, F., T. M. Finan, S. R. Long, A. Pühler, P. Abola, F. Ampe, F. Barloy-Hubler, M. J. Barnett, A. Becker, P. Boistard, G. Bothe, M. Boutry, L. Bowser, J. Buhrmester, E. Cadieu, D. Capela, P. Chain, A. Cowie, R. W. Davis, S. Dréano, N. A. Federspiel, R. F. Fisher, S. Gloux, T. Godrie, A. Goffeau, B. Golding, J. Gouzy, M. Gurjal, I. Hernandez-Lucas, A. Hong, L. Huizar, R. W. Hyman, T. Jones, D. Khan, M. L. Kahn, S. Kalman, D. H. Keating, E. Kiss, C. Komp, V. Lelaure, D. Masuy, C. Palm, M. C. Peck, T. M. Pohl, D. Portetelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thëbault, M. Vandenbol, F.-J. Verhölter, S. Weidner, D. H. Wells, K. Wong, K.-C. Yeh, and J. Batut. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
16. Goloubinoff, P., A. Mogk, A. P. Zvi, T. Tomoyasu, and B. Bukau. 1999. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. USA 96:13732-13737.
17. Gouffi, K., N. Pica, V. Pichereau, and C. Blanco. 1999. Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti. Appl. Environ. Microbiol. 65:1491-1500.
18. Grogan, D. W., and J. E. Cronan, Jr. 1997. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61:429-441.
19. Guillot, A., D. Obis, and M.-Y. Mistou. 2000. Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int. J. Food Microbiol. 55:47-51.
20. Han, Y., D. Zhou, X. Pang, L. Zhang, Y. Song, Z. Tong, J. Bao, E. Dai, J. Wang, Z. Guo, J. Zhai, Z. Du, X. Wang, J. Wang, P. Huang, and R. Yang. 2005. Comparative transcriptome analysis of Yersinia pestis in response to hyperosmotic and high-salinity stress. Res. Microbiol. 156:403-415.
21. Hartl, F. U., and M. Hayer-Hartl. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858.
22. Herrera-Cervera, J. A., J. Olivares, and J. Sanjuan. 1996. Ammonia inhibition of plasmid pRmeGR4a conjugal transfer between Rhizobium meliloti strains. Appl. Environ. Microbiol. 62:1145-1150.
23. Houssin, C., N. Eynard, E. Shechter, and A. Ghazi. 1991. Effect of osmotic pressure on membrane energy-linked functions in Escherichia coli. Biochim. Biophys. Acta 1056:76-84.
24. Igarashi, K., and K. Kashiwagi. 1999. Polyamine transport in bacteria and yeast. Biochem. J. 344:633-642.
25. Jensen, J. B., N. K. Peters, and T. V. Bhuvaneswari. 2002. Redundancy in periplasmic binding protein-dependent transport systems for trehalose, sucrose, and maltose in Sinorhizobium meliloti. J. Bacteriol. 184:2978-2986.
26. Jensen, J. B., O. Y. Ampomah, R. Darrah, N. K. Peters, and T. V. Bhuvaneswari. 2005. Role of trehalose transport and utilization in Sinorhizobium meliloti-alfalfa interactions. Mol. Plant-Microbe Interact. 18:694-702.
27. Kanesaki, Y., I. Suzuki, S. I. Allakhverdiev, K. Mikami, and N. Murata. 2002. Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem. Biophys. Res. Commun. 290:339-348.
28. Kereszt, A., E. Kiss, B. L. Reuhs, R. W. Carlson, A. Kondorosi, and P. Putnoky. 1998. Novel rkp gene clusters of Sinorhizobium meliloti involved in capsular polysaccharide production and invasion of the symbiotic nodule: the rkpK gene encodes a UDP-glucose dehydrogenase. J. Bacteriol. 180:5426-5431.
29. Krol, E., and A. Becker. 2004. Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mol. Genet. Genomics 272:1-17.
30. Lloret, J., L. Bolaños, M. M. Lucas, J. M. Peart, N. J. Brewin, I. Bonilla, and R. Rivilla. 1995. Ionic stress and osmotic pressure induce different alterations in the lipopolysaccharide of a Rhizobium meliloti strain. Appl. Environ. Microbiol. 61:3701-3704.
31. Lloret, J., B. B. H. Wulff, J. M. Rubio, J. A. Downie, I. Bonilla, and R. Rivilla. 1998. Exopolysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. Appl. Environ. Microbiol. 64:1024-1028.
32. Long, S. R. 2001. Genes and signals in the Rhizobium-legume symbiosis. Plant Physiol. 125:69-72.
33. Lund, P. A. 2001. Microbial molecular chaperones. Adv. Microb. Physiol. 44:93-140.
34. Lynch, D., J. O'Brien, T. Welch, P. Clarke, P. O. Cuiv, J. H. Crosa, and M. O'Connell. 2001. Genetic organization of the region encoding regulation, biosynthesis and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J. Bacteriol. 183:2576-2585.
35. + and glutamate accumulation during osmotic adaptation of Escherichia coli. J. Biol. Chem. 269:1911-1917.
36. Meade, H. M., and E. R. Signer. 1977. Genetic mapping of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 74:2076-2078.
37. Miller, K. J., and J. M. Wood. 1996. Osmoadaptation by rhizosphere bacteria. Annu. Rev. Microbiol. 50:101-136.
38. Missiakas, D., and S. Raina. 1998. The extracytoplasmic function sigma factors: role and regulation. Mol. Microbiol. 28:1059-1066.
39. Munro, G. F., K. Hercules, J. Morgan, and W. Sauerbier. 1972. Dependence of putrescine content of Escherichia coli on the osmotic strength of the medium. J. Biol. Chem. 247:1272-1280.
40. Nakahigashi, K., N. Kubo, S. Narita, T. Shimaoka, S. Goto, T. Oshima, H. Mori, M. Maeda, C. Wada, and H. Inokuchi. 2002. HemK, a class of protein methyl transferase with similarity to DNA methyl transferases, methylates polypeptide chain release factors, and hemK knockout induces defects in translational termination. Proc. Natl. Acad. Sci. USA 99:1473-1478.
41. Nogales, J., R. Campos, H. BenAbdelkhalek, J. Olivares, C. Lluch, and J. Sanjuan. 2002. Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol. Plant-Microbe Interact. 15:225-232.
42. Oke, V., B. G. Rushing, E. J. Fisher, M. Moghadam-Tabrizi, and S. R. Long. 2001. Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti. Microbiology 147:2399-2408.
43. Ono, Y., H. Mitsui, T. Sato, and K. Minamisawa. 2001. Two RpoH homologs responsible for the expression of heat shock protein genes in Sinorhizobium meliloti. Mol. Gen. Genet. 264:902-912.
44. Perret, X., C. Staehelin, and W. J. Broughton. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64:180-201.
45. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
46. Raivio, T. L. 2005. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 56:1119-1128.
47. Raivio, T. L., and T. J. Silhavy. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591-624.
48. Rao, D. L. N., and P. C. Sharma. 1995. Effectiveness of rhizobial strains for chickpea under salinity stress and recovery of nodulation on desalinization. Indian J. Exp. Biol. 33:500-504.
49. - phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K polysaccharide. J. Bacteriol. 177:4289-4296.
50. Rüberg, S., Z.-X. Tian, E. Krol, B. Linke, F. Meyer, Y. Wang, A. Pühler, S. Weidner, and A. Becker. 2003. Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. J. Biotechnol. 106:255-268.
51. Schiller, D., D. Kruse, H. Kneifel, R. Krämer, and A. Burkovski. 2000. Polyamine transport and role of potE in response to osmotic stress in Escherichia coli. J. Bacteriol. 182:6247-6249.
52. Sharypova, L. A., S. N. Yurgel, M. Keller, B. V. Simarov, A. Pühler, and A. Becker. 1999. The eff-482 locus of Sinorhizobium meliloti CXM1-105 that influences symbiotic effectiveness consists of three genes encoding an endoglycanase, a transcriptional regulator and an adenylate cyclase. Mol. Gen. Genet. 261:1032-1044.
53. Sleator, R. D., and C. Hill. 2001. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26:49-71.
54. Soussi, M., M. Santamaría, A. Ocaña, and C. Lluch. 2001. Effects of salinity on protein and lipopolysaccharide pattern in a salt-tolerant strain of Mesorhizobium ciceri. J. Appl. Microbiol. 90:476-481.
55. Soutuurina, O. A., and P. N. Berlin. 2003. Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol. Rev. 27:505-523.
56. Spaink, H. P. 2000. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54:257-288.
57. Stougaard, J. 2001. Genetics and genomics of root symbiosis. Curr. Opin. Plant Biol. 4:328-335.
58. Vinés, E. D., C. L. Marolda, A. Balachandran, and M. A. Valvano. 2005. Defective O-antigen polymerization in tolA and pal mutants of Escherichia coli in response to extracytoplasmic stress. J. Bacteriol. 187:3350-3368.
59. Weber, A., and K. Jung. 2002. Profiling early osmostress-dependent gene expression in Escherichia coli using DNA macroarrays. J. Bacteriol. 184:5502-5507.
60. Wei, W., J. Jiang, W. Li, L. Wang, and S. S. Yang. 2004. Isolation of salt-sensitive mutants from Sinorhizobium meliloti and characterization of genes involved in salt tolerance. Lett. Appl. Microbiol. 39:278-283.
61. Xia, B., H. Ke, U. Shinde, and M. Unouye. 2003. The role of RbfA in 16S rRNA processing and cell growth at low temperature in Escherichia coli. J. Mol. Biol. 332:575-584.
62. Yang, Y. H., S. Dudoit, P. Luu, D. M. Lin, V. Peng, J. Ngai, and T. P. Speed. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:e15.
63. Yoon, S. H., M. J. Han, S. Y. Lee, K. J. Jeong, and J. S. Yoo. 2003. Combined transcriptome and proteome analysis of Escherichia coli during high cell density culture. Biotechnol. Bioeng. 81:753-767.
64. York, G. M., and G. C. Walker. 1998. The succinyl and acetyl modifications of succinoglycan influence susceptibility of succinoglycan to cleavage by the Rhizobium meliloti glycanases ExoK and ExsH. J. Bacteriol. 180:4184-4191.
65. Zahran, H. H. 1991. Conditions for successful Rhizobium-legume symbiosis in saline environments. Biol. Fertil. Soils 12:73-80.
66. Zahran, H. H. 1999. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Mol. Biol. Rev. 63:968-989.
67. Zolkiewski, M. 1999. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. J. Biol. Chem. 274:28083-28086.