1887

Abstract

The determinants necessary for adaptation to high NaCl concentrations and competition for nodule occupancy in were investigated genetically. Mutations in as well as (transmembrane transglycosylase), trigger factor () and (probably ) gave rise to strains that were unable to tolerate high salt and were uncompetitive for nodule occupancy relative to the wild-type. Moreover , and determinants were determined to be necessary for strain Rm1021 to survive high NaCl and/or MgCl concentrations. The introduction of an allele was capable of suppressing the Mg sensitivity associated with the , but not the , mutation in a manner independent of exopolysaccharide II (EPS II)-associated mucoidy. The results also show that the EPS II-associated mucoid phenotype was affected by either Mgor K, but not by Li, Ca, or high osmolarity.

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2006-07-01
2020-04-02
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References

  1. Altschul S. F, Madden T. L, Zhang J. H, Zhang Z, Miller W, Lipman D. J, Schäffer A. A. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  2. Banfalvi Z, Sakanyan V, Koncz C, Kiss A, Dusha I, Kondorsi A. 1981; Location of nodulation and nitrogen fixation genes on a high molecular weight plasmid of Rhizobium meliloti . Mol Gen Genet184:318–325
    [Google Scholar]
  3. Barnett M. J, Fisher R. F, Jones T.23 other authors 2001; Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci U S A98:9883–9888[CrossRef]
    [Google Scholar]
  4. Barra L, Bowser L, Pica N, Gouffi K, Walker G. C, Blanco C, Trautwetter A. 2003; Glucose 6-phosphate dehydrogenase is required for sucrose and trehalose to be efficient osmoprotectants in Sinorhizobium meliloti . FEMS Microbiol Lett229:183–188[CrossRef]
    [Google Scholar]
  5. Beck K, Wu L, Brunner J, Müller M. 2000; Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J19:134–143[CrossRef]
    [Google Scholar]
  6. Botsford J. L. 1984; Osmoregulation in Rhizobium meliloti : inhibition of growth by salts. Arch Microbiol137:124–127[CrossRef]
    [Google Scholar]
  7. Botsford J. L, Lewis T. A. 1990; Osmoregulation in Rhizobium meliloti : production of glutamic acid in response to osmotic stress. Appl Environ Microbiol56:488–494
    [Google Scholar]
  8. Bowen G. D, Rovira A. D. 1976; Microbial colonisation of plant roots. Annu Rev Phytopathol14:121–144[CrossRef]
    [Google Scholar]
  9. Breedveld M. W, Zevenhuizen L. P. T. M, Zehnder A. J. B. 1990; Osmotically induced oligo- and polysaccharide synthesis by Rhizobium melilot i SU-47. J Gen Microbiol136:2511–2519[CrossRef]
    [Google Scholar]
  10. Caetano-Anollés G. 1993; Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl3:85–94[CrossRef]
    [Google Scholar]
  11. Cronan J. E, Rock C. O. others 1996; Biosynthesis of membrane lipids. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp 612–636 Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  12. de Leeuw E, Graham B, Phillips G. J, Oudega B, Luirink J, ten Hagen-Jongman C. M. 1999; Molecular characterization of Escherichia coli FtsE and FtsX. Mol Microbiol31:983–993[CrossRef]
    [Google Scholar]
  13. de Vos G. F, Walker G. C, Signer E. R. 1986; Genetic manipulations in Rhizobium meliloti utilizing two new transposon Tn 5 derivatives. Mol Gen Genet204:485–491[CrossRef]
    [Google Scholar]
  14. Djordjevic M. A, Chen H. C, Natera S, Van Noorden G, Menzel C, Taylor S, Renard C, Geiger O, Weiller G. F. 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 2003;508–524
    [Google Scholar]
  15. Dylan T, Helinski D. R, Ditta G. S. 1990; Hypoosmotic adaptation in Rhizobium meliloti requires β -(1-2) glucan synthesis. J Bacteriol172:1400–1408
    [Google Scholar]
  16. Finan T. M, Hartwieg E, Lemieux K, Bergman K, Walker G. C, Signer E. R. 1984; General transduction in Rhizobium meliloti . J Bacteriol159:120–124
    [Google Scholar]
  17. Finan T. M, Hirsch A. M, Leigh J. A, Johansen E, Kuldau G. A, Deegan S, Walker G. C, Signer E. R. 1985; Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell40:869–877[CrossRef]
    [Google Scholar]
  18. Finan T. M, Kunkel B, Signer E. R, de Vos G. F. 1986; Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol167:66–72
    [Google Scholar]
  19. Finan T. M, Oresnik I, Bottacin A. 1988; Mutants of Rhizobium meliloti defective in succinate metabolism. J Bacteriol170:3396–3403
    [Google Scholar]
  20. Finan T. M, Weidner S, Wong K.9 other authors 2001; The complete sequence of the 1,683-kb pSymB megaplasmid from the N[sub]2[/sub]-fixing endosymbiont S. meliloti . Proc Natl Acad Sci U S A98:9889–9894[CrossRef]
    [Google Scholar]
  21. Galibert F, Finan T. M, Long S. R.53 other authors 2001; The composite genome of the legume symbiont Sinorhizobium meliloti . Science293:668–672[CrossRef]
    [Google Scholar]
  22. Glazebrook J, Walker G. C. 1989; A novel exopolysaccharide can function in place of calcofluor-binding exopolysaccharide in nodulation on alfalfa. Cell56:661–672[CrossRef]
    [Google Scholar]
  23. Glazebrook J, Walker G. C. 1991; Genetic techniques in Rhizobium meliloti . Methods Enzymol204:398–418
    [Google Scholar]
  24. González J. E, Reuhs B. L, Walker G. C. 1996a; Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa . Proc Natl Acad Sci U S A93:8636–8641[CrossRef]
    [Google Scholar]
  25. González J. E, York G. M, Walker G. C. 1996b; Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene179:141–146[CrossRef]
    [Google Scholar]
  26. Gore R. S, Miller J. M. 1993; Cyclic β -1,6-1,3 glucans are synthesized by Bradyrhizobium japonicum bacteroids within soybean (Glycine max) root nodules. Plant Physiol102:191–194[CrossRef]
    [Google Scholar]
  27. Gouffi K, Pica N, Pichereau V, Blanco C. 1999; Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti . Appl Environ Microbiol65:1491–1500
    [Google Scholar]
  28. Gouffi K, Bernard T, Blanco C. 2000; Osmoprotection by pipecolic acid in Sinorhizobium meliloti : specific effects of d and l isomers. Appl Environ Microbiol66:2358–2364[CrossRef]
    [Google Scholar]
  29. Hoang H. H, Becker A, González J. E. 2004; The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J Bacteriol186:5460–5472[CrossRef]
    [Google Scholar]
  30. Hoang T. T, Sullivan S. A, Cusick J. K, Schweizer H. P. 2002; Beta-ketoacyl acyl carrier protein reductase (FabG) activity of the fatty acid biosynthetic pathway is a determining factor of 3-oxo-homoserine lactone acyl chain lengths. Microbiology148:3849–3856
    [Google Scholar]
  31. Jordan D. C. 1984; Rhizobiaceae. In Bergey's Manual of Systematic Bacteriology pp 234–241 Edited by Kreig N. R.. Baltimore: Williams & Wilkins;
    [Google Scholar]
  32. Kaufusi P. H, Forsberg L. S, Tittabutr P, Borthakur D. 2004; Regulation of exopolysaccharide synthesis in Rhizobium sp. strain TAL1145 involves an alternative sigma factor gene, rpoH2 . Microbiology150:3473–3482[CrossRef]
    [Google Scholar]
  33. Keller M, Simon R, Müller P, Pühler A. 1988; Rhizobium meliloti genes for exopolysaccharide synthesis and nodule infection located on megaplasmid 2 are actively transcribed during symbiosis. Mol Plant Microbe Interact1:267–274[CrossRef]
    [Google Scholar]
  34. Lai C, Cronan J. E. 2004; Isolation and characterization of β -keto-acyl carrier protein reductase (fabG) mutants of Escherichia coli and Salmonella enterica serovar Typhimurium. J Bacteriol186:1869–1878[CrossRef]
    [Google Scholar]
  35. Leigh J. A, Coplin D. C. 1992; Exopolysaccharides in plant-bacterial interactions. Annu Rev Microbiol46:307–346[CrossRef]
    [Google Scholar]
  36. Leigh J. A, Signer E. R, Walker G. C. 1985; Exopolysaccharide deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A82:6231–6235[CrossRef]
    [Google Scholar]
  37. Le Rudulier D, Bernard T. 1986; Salt tolerance in Rhizobium : a possible role for betaines. FEMS Microbiol Rev39:67–72[CrossRef]
    [Google Scholar]
  38. Lloret J, Bolanos L, Lucas M. M, Peart J. M, Brewin N. J, Bonilla I, Rivilla R. 1995; Ionic stress and osmotic pressure induce different alterations in the lipopolysaccharide of a Rhizobium meliloti strain. Appl Environ Microbiol61:3701–3704
    [Google Scholar]
  39. Lloret J, Wiulff B. B. H, Rubio J. M, Downie J. A, Bonilla I, Rivilla R. 1998; Exopolysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. Appl Environ Microbiol64:1024–1028
    [Google Scholar]
  40. López-Lara I. M., Geiger O. 2001; The nodulation protein NodG shows the enzymatic activity of an 3-oxoacyl-acyl carrier protein reductase. Mol Plant Microbe Interact14:349–357[CrossRef]
    [Google Scholar]
  41. Maillet F, Debellé F, Dénarie J. 1990; Role of the nodD and syrM genes in the activation of the regulatory gene nodD3 , and the common and host-specific nod genes of Rhizobium meliloti . Mol Microbiol4:1975–1984[CrossRef]
    [Google Scholar]
  42. Marroquí S, Zorreguieta A, Temprano F, Downie J. A, Santamaría C, Soberón M, Mégias M. 2001; Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. J Bacteriol183:854–864[CrossRef]
    [Google Scholar]
  43. Meade H. M, Long S. R, Ruvkin G. B, Brown S. E, Ausubel F. M. R. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn 5 mutagenesis. J Bacteriol149:114–122
    [Google Scholar]
  44. Mendrygal K, González J. E. 2000; Environmental regulation of exopolysaccharide production in Sinorhizobium meliloti . J Bacteriol182:599–606[CrossRef]
    [Google Scholar]
  45. Miller J. H. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  46. Miller K. J, Wood J. M. 1996; Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol50:101–136[CrossRef]
    [Google Scholar]
  47. Nagpal P, Khanuja S. P. S, Stanfield S. W. 1992; Suppression of the ndv mutant phenotype of Rhizobium meliloti by cloned exo genes. Mol Microbiol6:479–488[CrossRef]
    [Google Scholar]
  48. Nogales J, Campos R, BenAbdelkhalek H, Olivares J, Lluch C, Sanjuan J. 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 Interact15:225–232[CrossRef]
    [Google Scholar]
  49. Oresnik I. J, Charles T. C, Finan T. M. 1994; Second site mutations specifically suppress the Fix[sup]−[/sup] phenotype of Rhizobium meliloti ndvF mutations on alfalfa: identification of a conditional ndvF -dependent mucoid colony phenotype. Genetics136:1233–1243
    [Google Scholar]
  50. Oresnik I. J, Pacarynuk L. A, O'Brien S. A. P, Yost C. K, Hynes M. F. 1998; Plasmid encoded catabolic genes in Rhizobium leguminosarum bv. trifolii : evidence for a plant-inducible rhamnose locus involved in competition for nodulation. Mol Plant Microbe Interact11:1175–1185[CrossRef]
    [Google Scholar]
  51. Pellock B. J, Cheng H, Walker G. C. 2000; Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J Bacteriol182:4310–4318[CrossRef]
    [Google Scholar]
  52. Pellock B. J, Teplitski M, Boinay R. P, Bauer W. D, Walker G. C. 2002; A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti . J Bacteriol184:5067–5076[CrossRef]
    [Google Scholar]
  53. Raffa G. R, Raivio T. L. 2002; A third envelope stress signal transduction pathway in Escherichia coli . Mol Microbiol45:1599–1611[CrossRef]
    [Google Scholar]
  54. Reuber T. L, Walker G. C. 1993; Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti . Cell74:269–280[CrossRef]
    [Google Scholar]
  55. Reuhs B. L, Williams M. N. V, Kim J. S, Carlson R. W, Côté F. 1995; Suppression of the Fix[sup]−[/sup] phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to modified expression of the K polysaccharide. J Bacteriol177:4289–4296
    [Google Scholar]
  56. Rüberg S, Pühler A., Becker A. 1999; Biosynthesis of the exopolysaccharide galactoglucan in Sinorhizobium meliloti is subject to a complex control by the phosphate-dependent regulator PhoB and the proteins ExpG and MucR. Microbiology145:603–611[CrossRef]
    [Google Scholar]
  57. Rüberg S, Tian Z, Krol E, Linke B, Meyer F, Wang Y, Weidner S, Becker A, Pühler A. 2003; Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. J Biotechnol106:255–268[CrossRef]
    [Google Scholar]
  58. Sambrook J, Fritsch E. F, Maniatis T. A. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  59. Schmidt K. L, Peterson N. D, Kustusch R. J, Wissel M. C, Graham B, Phillips G. J, Weiss D. S. 2004; A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli . J Bacteriol186:785–793[CrossRef]
    [Google Scholar]
  60. Smith L. T, Smith G. M. 1989; An osmoregulated dipeptide in stressed Rhizobium meliloti . J Bacteriol171:4714–4717
    [Google Scholar]
  61. Smith L. T, Smith G. B, D'Souza M, Pocard J.-A, Le Rudulier D, Madkour M. A. 1994; Osmoregulation in Rhizobium meliloti : mechanism and control by other environmental signals. J Exp Zool268:162–165[CrossRef]
    [Google Scholar]
  62. Spaink H. P. 2000; Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol54:257–288[CrossRef]
    [Google Scholar]
  63. Vedam V, Kannenberg E. L, Haynes J. G, Sherrier D. J, Datta A, Carlson R. W. 2003; A Rhizobium leguminosarum AcpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J Bacteriol185:1841–1850[CrossRef]
    [Google Scholar]
  64. Vincent J. M. 1970; A Manual for the Practical Study of Root-Nodule Bacteria Oxford, UK: Blackwell Scientific Publications;
    [Google Scholar]
  65. Zhan H. J, Lee C. C, Leigh J. A. 1991; Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations. J Bacteriol173:7391–7394
    [Google Scholar]
  66. Zhang Y, Cronan J. E. 1998; Transcriptional analysis of essential genes of the Escherichia coli fatty acid biosynthesis gene cluster by functional replacement with the analogous Salmonella typhimurium gene cluster. J Bacteriol180:3295–3303
    [Google Scholar]
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