1887

Abstract

CIAT899 displays intrinsic tolerance to acidity, and efficiently nodulates at low pH. By characterizing a mutant strain, glutathione has been previously demonstrated to be essential for tolerance to acid stress. The wild-type gene region has been cloned and its transcription profile has been characterized by using quantitative real-time PCR and transcriptional gene fusions. Activation of the gene under acid-stress conditions was demonstrated. is also induced by UV irradiation. Upstream from a putative promoter element and an inverted repeat sequence were identified, which are proposed to be involved in expression under neutral and acidic conditions, respectively. Gel retardation assays indicate that transcription in acid conditions may involve protein binding to an upstream regulatory region.

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2007-04-01
2024-04-19
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References

  1. Aguilar O. M., Grasso D. H. 1991; The product of the Rhizobium meliloti ilvC gene is required for isoleucine and valine synthesis and nodulation of alfalfa. J Bacteriol 173:7756–7764
    [Google Scholar]
  2. Allocati N., Favaloro B., Masulli M., Alexeyev M. D., Di Ilio C. 2003; Proteus mirabilis glutathione S -transferase B1-1 is involved in protective mechanisms against oxidative and chemical stresses. Biochem J 373:305–311 [CrossRef]
    [Google Scholar]
  3. Anderson M. E. 1985; Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–555
    [Google Scholar]
  4. Becker A., Schmidt M., Jäger W., Pühler A. 1995; New gentamicin-resistance and lacZ promoter probe for insertion mutagenesis and generation of transcriptional fusions. Gene 162:37–39 [CrossRef]
    [Google Scholar]
  5. Beringer J. E. 1974; R factor transfer in Rhizobium leguminosarum . J Gen Microbiol 84:188–198 [CrossRef]
    [Google Scholar]
  6. Carmel-Harel O., Storz G. 2000; Roles of glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461 [CrossRef]
    [Google Scholar]
  7. Dombrecht B., Heusdens H., Beullens S., Verreth C., Mulkers E., Proost P., Vanderleyden J., Michiels J. 2005; Defense of Rhizobium etli bacteroids against oxidative stress involves a complexly regulated atypical 2-Cys peroxiredoxin. Mol Microbiol 55:1207–1221 [CrossRef]
    [Google Scholar]
  8. Escudero P. R., Minchin F. R., Gogorcena Y., Iturbe-Ormaetxe I., Klucas R. V., Becana M. 1996; Involvement of activated oxygen in nitrate-induced senescence of pea root nodules. Plant Physiol 110:1187–1195
    [Google Scholar]
  9. Fenner B. J., Tiwari R. P., Reeve W. J., Dilworth M. J., Glenn A. R. 2004; Sinorhizobium medicae genes whose regulation involves the ActS and/or ActR signal transduction proteins. FEMS Microbiol Lett 236:21–31 [CrossRef]
    [Google Scholar]
  10. Ferguson G. P., Booth I. R. 1998; Importance of glutathione for growth and survival of Escherichia coli cells: detoxification of methylglyoxal and maintenance of intracellular K+ . J Bacteriol 180:4314–4318
    [Google Scholar]
  11. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
    [Google Scholar]
  12. Harrison J., Jamet A., Muglia C., Van de Sype G., Aguilar O. M., Puppo A., Frendo P. 2005; Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti . J Bacteriol 187:168–174 [CrossRef]
    [Google Scholar]
  13. Higgins D. G. 1994; clustal v: multiple alignment of DNA and protein sequences. Methods Mol Biol 25:307–318
    [Google Scholar]
  14. Hoerter J. D., Arnold A. A., Kuczynska D. A., Shibuya A., Ward C. S., Sauer M. G., Gizachew A., Hotchkiss T. M., Fleming T. J., Johnson S. 2005; Effect of sublethal UVA irradiation on activity levels of oxidative defence enzymes and protein oxidation in Escherichia coli . J Photochem Photobiol B 81:171–180 [CrossRef]
    [Google Scholar]
  15. Iturbe-Ormaetxe I., Matamoros M. A., Rubio M. C., Dalton D. A., Becana M. 2001; The antioxidants of legume root nodule mitochondria. Mol Plant Microbe Interact 14:1189–1196 [CrossRef]
    [Google Scholar]
  16. Jamet A., Sigaud S., Van de Sype G., Puppo A., Herouart D. 2003; Expression of the bacterial catalase genes during Sinorhizobium meliloti–Medicago sativa symbiosis and their crucial role during the infection process. Mol Plant Microbe Interact 16:217–225 [CrossRef]
    [Google Scholar]
  17. Kiss G., Forrai T., Vincze È., Kálman Z., Kondorosi Á. 1979; Genetic and biochemical analysis of mutants affects nitrate reduction in Rhizobium meliloti . J Gen Microbiol 113:105–118 [CrossRef]
    [Google Scholar]
  18. Lillig C. H., Potamitou A., Schwenn J. D., Vlamis-Gardikas A., Holmgren A. 2003; Redox regulation of 3′-phosphoadenylylsulfate reductase from Escherichia coli by glutathione and glutaredoxins. J Biol Chem 278:22325–22330 [CrossRef]
    [Google Scholar]
  19. MacLellan S. R., MacLean A. M., Finan T. M. 2006; Promoter prediction in the rhizobia. Microbiology 152:1751–1763 [CrossRef]
    [Google Scholar]
  20. Marsh J. L., Erfle M. P., Wykes E. J. 1984; The pIC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation. Gene 32:481–485 [CrossRef]
    [Google Scholar]
  21. Martínez-Romero E., Segovia L., Mercante F. M., Franco A. A., Graham P., Pardo M. A. 1991; Rhizobium tropici , a novel species nodulating Phaseolus vulgaris beans and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426 [CrossRef]
    [Google Scholar]
  22. Masip L., Veeravalli K., Georgiou G. 2006; The many faces of glutathione in bacteria. Antioxid Redox Signal 8:753–762 [CrossRef]
    [Google Scholar]
  23. Matamoros M. A., Baird L. M., Escudero P. R., Dalton D. A., Minchin F. R., Iturbe-Ormaetxe I., Rubio M. C., Gordon A. J., Becana M., Morán J. F. 1999; Stress-induced legume root nodule senescence. Physiological, biochemical and structural alterations. Plant Physiol 121:97–111 [CrossRef]
    [Google Scholar]
  24. Matamoros M. A., Dalton D. A., Ramos J., Clemente M. R., Rubio M. C., Becana M. 2003; Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 133:499–509 [CrossRef]
    [Google Scholar]
  25. Miller J. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  26. Moran J. F., Iturbe-Ormaetxe I., Matamoros M., Rubio M. C., Clemente M. R., Brewin N. J., Becana M. 2000; Glutathione and homoglutathione synthetases of legume nodules. Cloning, expression, and subcellular localization. Plant Physiol 124:1381–1392 [CrossRef]
    [Google Scholar]
  27. Neumann C., Boubakari, Grunert R., Bednarski P. J. 2003; Nicotinamide adenine dinucleotide phosphate-regenerating system coupled to a glutathione-reductase microtiter method for determination of total glutathione concentrations in adherent growing cancer cell lines. Anal Biochem 320:170–178 [CrossRef]
    [Google Scholar]
  28. Noctor G., Vanacker H., Foyer C. H., Gómez L. D. 2002; Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304 [CrossRef]
    [Google Scholar]
  29. O'Reilly E. K., Kreuzer K. N. 2004; Isolation of SOS constitutive mutants of Escherichia coli . J Bacteriol 186:7149–7160 [CrossRef]
    [Google Scholar]
  30. Penninckx M. J., Elskens M. T. 1993; Metabolism and functions of glutathione in micro-organisms. Adv Microb Physiol 34:239–301
    [Google Scholar]
  31. Pérez-Galdona R., Kahn M. L. 1994; Effects of organic acids and low pH on Rhizobium meliloti 104A14. Microbiology 140:1231–1235 [CrossRef]
    [Google Scholar]
  32. Pflock M., Finsterer N., Joseph B., Mollenkopf H., Meyer T. F., Beier D. J. 2006; Characterization of the ArsRS regulon of Helicobacter pylori , involved in acid adaptation. J Bacteriol 188:3449–3462 [CrossRef]
    [Google Scholar]
  33. Priefer U. B., Simon R., Pühler A. 1985; Extension of the host range of Escherichia coli vectors by incorporation of RSF1010 replication and mobilization functions. J Bacteriol 163:324–330
    [Google Scholar]
  34. Pühler A., Timmis K. editors 1984 Advanced Molecular Genetics Berlin: Springer;
    [Google Scholar]
  35. Ramírez-Romero M. A., Masulis I., Cevallos M. A., González V., Dávila G. 2006; The Rhizobium etli sigma70 (SigA) factor recognizes a lax consensus promoter. Nucleic Acids Res 34:1470–1480 [CrossRef]
    [Google Scholar]
  36. Raya R., Bardowski J., Andersen P. S., Erlich S. D., Chopin A. 1998; Multiple transcriptional control of the Lactococcus lactis trp operon. J Bacteriol 180:3174–3180
    [Google Scholar]
  37. Reeve W. G., Tiwari R. P., Kale N. B., Dilworth M. J., Glenn A. R. 2002; ActP controls copper homeostasis in Rhizobium leguminosarum bv. viciae and Sinorhizobium meliloti preventing low pH-induced copper toxicity. Mol Microbiol 43:981–991 [CrossRef]
    [Google Scholar]
  38. Reeve W. G., Castelli J., Garau G., Sohlenkamp C., Geiger O., Dilworth M. J., Glenn A. R., Howieson J. G., Tiwari R. P., Bräu L. 2006; The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions. Microbiology 152:3049–3059 [CrossRef]
    [Google Scholar]
  39. Riccillo P. M., Muglia C., De Bruijn F. J., Roe A., Booth I. R., Aguilar O. M. 2000; Glutathione is involved in environmental stress responses in Rhizobium tropici , including acid tolerance. J Bacteriol 182:1748–1753 [CrossRef]
    [Google Scholar]
  40. Roe A. J., McLaggan D., Davidson I., O'Byrne C., Booth I. R. 1998; Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J Bacteriol 180:767–772
    [Google Scholar]
  41. Rojas-Jiménez K., Sohlenkamp K., Geiger O., Martínez-Romero E., Werner D., Vinuesa P. 2005; A ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Mol Plant Microbe Interact 18:1175–1185 [CrossRef]
    [Google Scholar]
  42. Sambrook J., Fritsch E., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  43. Santos R., Herouart D., Puppo A., Touati D. 2000; Critical protective role of bacterial superoxide dismutase in Rhizobium –legume symbiosis. Mol Microbiol 38:750–759 [CrossRef]
    [Google Scholar]
  44. Schafer A., Tauch A., Jager W., Kalinowski J., Thierbach G., Pühler A. 1994; Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum . Gene 145:69–73 [CrossRef]
    [Google Scholar]
  45. Schujman G. E., Paoletti L., Grossman A. D., de Mendoza D. 2003; FapR, a bacterial transcription factor involved in global regulation of membrane lipid biosynthesis. Dev Cell 4:663–672 [CrossRef]
    [Google Scholar]
  46. Sherrill C., Fahey R. C. 1998; Import and metabolism of glutathione by Streptococcus mutans . J Bacteriol 180:1454–1459
    [Google Scholar]
  47. Sigaud S., Becquet V., Frendo P., Puppo A., Herouart D. 1999; Differential regulation of two divergent Sinorhizobium meliloti genes for HPII-like catalases during free-living growth and protective role of both catalases during symbiosis. J Bacteriol 181:2634–2639
    [Google Scholar]
  48. Simon R., Priefer U., Pühler A. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. BioTechnology 1:784–791 [CrossRef]
    [Google Scholar]
  49. Simon R., O'Connell M., Labes M., Pühler A. 1986; Plasmid vectors for the genetic analysis and manipulation of rhizobia and other gram-negative bacteria. Methods Enzymol 118:640–659
    [Google Scholar]
  50. Smith R. F., Wiese B. A., Wojzynski M. K., Davison D. B., Worley K. C. 1996; BCM search launcher – an integrated interface to molecular biology data base search and analysis services available on the world wide web. Genome Res 6:454–462 [CrossRef]
    [Google Scholar]
  51. Spaink H. P., Okker R. J., Wijffelman C. A., Pees E., Lugtenberg B. J. 1987; Promoters in the nodulation region of the Rhizobium leguminosarum sym plasmid pRL1JI. Plant Mol Biol 9:27–39 [CrossRef]
    [Google Scholar]
  52. Tiwari R. P., Reeve W. G., Dilworth M. J., Glenn A. R. 1996a; An essential role for actA in acid tolerance in Rhizobium meliloti . Microbiology 142:601–602 [CrossRef]
    [Google Scholar]
  53. Tiwari R. P., Reeve W. G., Dilworth M. J., Glenn A. R. 1996b; Acid tolerance in Rhizobium meliloti strain WSM419 involves a two-component sensor-regulator system. Microbiology 142:1693–1704 [CrossRef]
    [Google Scholar]
  54. Tiwari R. P., Reeve W. G., Fenner B. J., Glenn A. R., Howeison J. G. 2004; Probing for pH-regulated genes in Sinorhizobium medicae using transcriptional analysis. J Mol Microbiol Biotechnol 7:133–139 [CrossRef]
    [Google Scholar]
  55. Tyagi R., Lai R., Duggleby R. G. 2004; A new approach to ‘megaprimer’ polymerase chain reaction mutagenesis without an intermediate gel purification step. BMC Biotechnol 4:2 [CrossRef]
    [Google Scholar]
  56. Vinuesa P., Neumann-Silkow F., Pacios-Bras C., Spaink H. P., Werner D., Martínez-Romero E. 2003; Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol Plant Microbe Interact 16:159–168 [CrossRef]
    [Google Scholar]
  57. Vlahovicek K., Kajan L., Pongor S. 2003; DNA analysis servers: plot.it, bend.it, model.it and IS. Nucleic Acids Res 31:3686–3687 [CrossRef]
    [Google Scholar]
  58. Worley K. C., Wiese B. A., Smith R. F. 1995; beauty: an enhanced blast-based search tool that integrates multiple biological information resources into sequence similarity search results. Genome Res 5:173–184 [CrossRef]
    [Google Scholar]
  59. Worley K. C., Culpepper P., Wiese B. A., Smith R. F. 1998; beauty-x: enhanced blast searches for DNA queries. Bioinformatics 14:890–891 [CrossRef]
    [Google Scholar]
  60. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [CrossRef]
    [Google Scholar]
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