Biosynthesis of compatible solutes in rhizobial strains isolated from Phaseolus vulgaris nodules in Tunisian fields

BMC Microbiology

Volumn 10, Issue , 2010, Pages

  Fernandez Aunián, Cristina ^a   Hamouda, Thouraya Ben ^b   Iglesias Guerra, Fernando ^a   Argandõa, Montserrat ^a   Reina Bueno, Mercedes ^a   Nieto, Joaquín J ^a   Aouani, M Elarbi ^b,c   Vargas, Carmen ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b CENTRE DE BIOTECHNOLOGIE DE BORJ CÉDRIA   (Tunisia)

^c NATIONAL RESEARCH CENTRE   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,2 CYCLIC GLUCAN; GLUCAN; GLUTAMIC ACID; SYNTHETASE; TREHALOSE; TREHALOSE 6 PHOSPHATE SYNTHETASE; UNCLASSIFIED DRUG; ORGANIC COMPOUND; SODIUM CHLORIDE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; CARBON NUCLEAR MAGNETIC RESONANCE; CARBON SOURCE; CHEMICAL STRUCTURE; ENZYME SYNTHESIS; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASEOLUS VULGARIS; PROTON NUCLEAR MAGNETIC RESONANCE; RHIZOBIALES; TUNISIA; UNINDEXED SEQUENCE; BEAN; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NODULATION; PHYLOGENY; RHIZOBIUM;

AGROBACTERIUM TUMEFACIENS; PHASEOLUS VULGARIS; RHIZOBIUM; RHIZOBIUM ETLI; RHIZOBIUM GALLICUM BV. PHASEOLI; RHIZOBIUM LEGUMINOSARUM BV. PHASEOLI; RHIZOBIUM TROPICI; SINORHIZOBIUM MELILOTI;

MOLECULAR SEQUENCE DATA; ORGANIC CHEMICALS; PHASEOLUS; PHYLOGENY; RHIZOBIUM; ROOT NODULES, PLANT; SODIUM CHLORIDE; SOIL MICROBIOLOGY; TUNISIA;

EID: 77954553601     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-10-192     Document Type: Article

References (59)

1. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. HH Zahran, Microbiol Mol Biol Rev 1999 63 968 989 10585971
2. Osmoadaptation in bacteria. EA Galinski, Adv Microb Physiol 1995 37 272 328 8540423
3. Osmoadaptation by rhizosphere bacteria. KJ Miller JM Wood, Annu Rev Microbiol 1996 50 101 136 10.1146/annurev.micro.50.1.101 8905077
4. An overview of the role and diversity of compatible solutes in Bacteria and Archaea. MS da Costa H Santos EA Galinski, Adv Biochem Eng Biotechnol 1998 61 117 153 9670799
5. Microbial water stress. AD Brown, Bacteriol Rev 1976 40 803 846 1008746
6. Ecological significance of compatible solute accumulation by micro organisms: from single cells to global climate. DT Welsh, FEMS Microbiol Rev 2000 24 263 290 10.1111/j.1574-6976.2000.tb00542.x 10841973
7. Compatible solutes of organisms that live in hot saline environments. H Santos MS da Costa, Environ Microbiol 2002 4 501 509 10.1046/j.1462-2920.2002. 00335.x 12220406
8. Cyclic beta-glucans of members of the family Rhizobiaceae. MW Breedveld KJ Miller, Microbiol Rev 1994 58 145 161 8078434
9. Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. JL Botsford TA Lewis, Appl Environ Microbiol 1990 56 488 494 16348124
10. Role of potassium uptake systems in Sinorhizobium meliloti osmoadaptation and symbiotic performance. A Domínguez-Ferreras S Mũoz J Olivares MJ Soto J Sanjun, J Bacteriol 2009 191 2133 2143 10.1128/JB.01567-08 19181803
11. An osmoregulated dipeptide in stressed Rhizobium meliloti. LT Smith JA Pocard LT Bernard-Smith GM Smith, J Bacteriol 1989 171 4714 4717 2768187
12. Importance of trehalose biosynthesis for Sinorhizobium meliloti osmotolerance and nodulation of Alfalfa roots. A Domínguez-Ferreras MJ Soto R Pérez-Arnedo J Olivares J Sanjun, J Bacteriol 2009 191 7490 7499 10.1128/JB.00725-09 19837796
13. Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. M Sugawara EJ Cytryn MJ Sadowsky, Appl Environ Microbiol 2010 76 1071 1081 10.1128/AEM.02483-09 20023090
14. Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. HJ McIntyre H Davies TA Hore SH Miller JP Dufour CW Ronson, Appl Environ Microbiol 2007 73 3984 3992 10.1128/AEM.00412-07 17449695
15. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. E Martínez-Romero L Segovia FM Mercante AA Franco P Graham MA Pardo, Int J System Bacteriol 1991 41 417 426 10.1099/00207713-41-3-417
16. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. N Amarger V Macheret G Laguerre, Int J System Bacteriol 1997 47 996 1006 10.1099/00207713-47-4-996
17. Evolutionary genetics and biogeographic structure of Rhizobium galliucm sensu lato, a widely distributed bacterial symbiont of diverse legumes. C Silva P Vinuesa LE Eguiarte V Souza E Martínez-Romero, Mol Ecol 2005 14 4033 4050 10.1111/j.1365-294X.2005.02721.x 16262857
18. Methods for enhancing symbiotic nitrogen fixation. G Hardarson, Plant soil 1993 152 1 17 10.1007/BF00016329
19. Yield and nodulation of Phaseolus vulgaris and the competitiveness of an introduced Rhizobium strain: effects of lime, mulch and repeated cropping. LMG Ramos RM Boddey, Soil Biol Chem 1987 19 171 177
20. Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris L.: a review. PH Graham, Field Crop Res 1981 4 93 112 10.1016/0378-4290(81)90060-5
21. Advances in Rhizobium research. A Sessitsch JG Howieson X Perret H Antoun E Martínez-Romero, Crit Rev Plant Sci 2002 21 323 378 10.1080/0735-260291044278
22. Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. R Surez A Wong M Ramírez A Barraza MC Orozco MA Cevallos M Lara G Hernndez G Iturriaga, Mol Plant Microb Interact 2008 21 958 966 10.1094/MPMI-21-7-0958 (Pubitemid 352008688)
23. Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. R Mhamdi M Jebara ME Aouani R Ghir M Mars, Biol Fertil Soils 1999 28 313 320 10.1007/s003740050499 (Pubitemid 29053313)
24. Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. R Mhamdi G Laguerre ME Aouani M Mars N Amarger, FEMS Microbiol Ecol 2002 41 77 84 10.1111/j.1574-6941.2002.tb00968.x 19709241
25. Acid pH tolerance in strains of Rhizobium and Bradyrhizobium and initial studies on the basis for acid tolerance of Rhizobium tropici UMR 1899. PH Graham JK Draeger ML Ferrey MJ Conroy BE Hammer E Martine SR Aarons C Quinto, Can J Microbiol 1994 40 198 207 10.1139/m94-033
26. Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. PM Riccillo CI Muglia FJ de Bruijn AJ Roe IR Booth OM Aguilar, J Bacteriol 2000 182 1748 1753 10.1128/JB.182.6.1748-1753.2000 10692382
27. Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. J Nogales R Campos H BenAbdelkhalek J Olivares C Lluch J Sanjun, Mol Plant Microb Interact 2002 15 225 232 10.1094/MPMI.2002.15.3.225
28. Colonization of Phaseolus vulgaris nodules by Agrobacterium-like strains. R Mhamdi M Mrabet G Laguerre R Tiwari ME Aouani, Can J Microbiol 2005 51 105 111 10.1139/w04-120 16091768
29. Agrobacterium strains isolated from root nodules of common bean specifically reduce nodulation by Rhizobium gallicum. M Mrabet B Mnasri SB Romdhane G Laguerre ME Aouani R Mhamdi, FEMS Microbiol Ecol 2006 56 304 309 10.1111/j.1574-6941.2006.00069.x 16629759
30. Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. MH Ramírez-Bahena P García-Fraile A Peix A Valverde R Rivas JM Igual PF Mateos E Martínez-Molina E Velzquez, Int J System Evol Microbiol 2008 58 2484 2490 10.1099/ijs.0.65621-0
31. Osmoregulation in Agrobacterium tumefaciens: accumulation of a novel disaccharide is controlled by osmotic strength and glycine betaine. LT Smith GM Smith MA Madkour, J Bacteriol 1990 172 6849 6855 2254260
32. Insights on the evolution of trehalose biosynthesis. N Avonce A Mendoza-Vargas E Morett G Iturriaga, BMC Evol Biol 2006 6 109 10.1186/1471-2148-6-109 17178000
33. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. OB Styrvold I Kaasen AR Strøm, J Bacteriol 1998 170 2841 2849
34. The structure and molecular mechanisms calculations of the cyclic (12) - D-glucan secreted by Rhizobium tropici CIAT 899. G Franco-Rodríguez I Gonzlez-Jiménez P Tejero-Mateo J Molina-Molina JA Doblado M Megías MJ Romero, J Mol Struct 1993 301 211 226 10.1016/0022-2860(93)80246-R
35. Sucrose is a nonaccumulated osmoprotectant in Sinorhizobium meliloti. K Gouffi V Pichereau JP Rolland D Thomas T Bernard C Blanco, J Bacteriol 1998 180 5044 5051 9748435
36. Osmoadaptative responses in the rhizobia nodulating Acacia isolated from south-eastern Moroccan Sahara. M Essendoubi F Brhada JE Eljamali A Filali-Maltouf S Bonnassie S Georgeault C Blanco M Jebbar, Environ Microbiol 2007 9 603 611 10.1111/j.1462-2920.2006.01176.x 17298361
37. Bioenergetic aspects of halophilism. A Oren, Microbiol Mol Biol Rev 1999 63 334 348 10357854
38. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. AR Strøm I Kaasen, Mol Microbiol 1993 8 205 210 10.1111/j.1365-2958.1993.tb01564.x 8391102
39. Distribution of genes for synthesis of trehalose and mannosylglycerate in Thermus spp. and direct correlation of these genes with halotolerance. S Alarico N Empadinhas C Simes Z Silva A Henne A Mingote H Santos MS da Costa, Appl Environ Microbiol 2005 71 2460 2466 10.1128/AEM.71.5.2460-2466.2005 15870334
40. Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroids from soybean nodules. JG Streeter ML Gámez, Appl Environ Microbiol 2006 72 4250 4255 10.1128/AEM.00256-06 16751539
41. Biosynthesis of trehalose from maltooligosaccharides in Rhizobia. JG Streeter A Bhagwat, Can J Microbiol 1999 45 716 721 10.1139/cjm-45-8-716 10528404
42. The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. PA Frey, FASEB J 1996 10 461 70 8647345
43. EcoSal- Escherichia coli and Salmonella: Cellular and Molecular Biology. A Bock R Curtiss III JB Kaper PD Karp FC Neidhardt T Nystrom JM Slauch CL Squires (eds), http://www.ecosal.org ASMOnline
44. Pathway for the synthesis of mannosylglycerate in the hyperthermophilic archaeon Pyrococcus horikoshii. Biochemical and genetic characterization of key enzymes. N Empadinhas JD Marugg N Borges H Santos MS da Costa, J Biol Chem 2001 276 43580 43588 10.1074/jbc.M108054200 11562374
45. Kyoto Encyclopedia of Genes and Genomes. KEGG, http://www.genome.jp/kegg/ kegg2.html
46. RpoE2 of Sinorhizobium meliloti is necessary for trehalose synthesis and growth in hyperosmotic media. M Flechard C Fontenelle C Blanco R Goude G Ermel A Trautwetter, Microbiology 2010 156 1708 1718 10.1099/mic.0.034850-0 20223801
47. Regulatory and DNA repair genes contribute to the desiccation resistance of Sinorhizobium meliloti Rm1021. JL Humann HT Ziemkiewicz SN Yurgel ML Kahn, Appl Environ Microbiol 2009 75 446 453 10.1128/AEM.02207-08 19028909
48. R factor transfer in Rhizobium leguminosarum. JE Beringer, J Gen Microbiol 1974 84 188 198 4612098
49. Choline and glycine betaine uptake in various strains of Rhizobia isolated from nodules of Vicia faba var. major and Cicer arietinum l.: modulation by salt, choline, and glycine betaine. F Brhada MC Poggi D Le Rudulier, Curr Microbiol 1997 34 167 172 10.1007/s002849900163 9009070
50. A Manual for the Practical Study of the Root-nodule Bacteria. JM Vincent, International Biological Programme Handbook. No. 15 Blackwell Sci. Pub., Oxford 1970
51. The ectD gene, which is involved in the synthesis of the compatible solute hydroxyectoine, is essential for thermoprotection of the halophilic bacterium Chromohalobacter salexigens. R García-Estepa M Argandõa M Reina-Bueno N Capote F Iglesias-Guerra JJ Nieto C Vargas, J Bacteriol 2006 188 3774 3784 10.1128/JB.00136-06 16707670
52. Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe. MA Blzquez R Stucka H Feldmann C Gancedo, J Bacteriol 1994 176 3895 3902 8021171
53. Current Protocols in Molecular Biology. FM Ausubel R Brent RE Kinston DD Moore JG Seidman JA Smith K Struhl, Green Publishing Associates, NY: John Wiley and Sons 1989
54. Phylogenetic inferences and taxonomic consequences of 16S ribosomal DNA sequence comparison of Chromohalobacter marismortui, Volcaniella eurihalina, and Deleya salina and reclassification of V. eurihalina as Halomonas eurihalina comb. nov. E Mellado ERB Moore JJ Nieto A Ventosa, Int J System Bacteriol 1995 45 712 716 10.1099/00207713-45-4-712
55. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. K Tamura J Dudley M Nei S Kumar, Mol Biol Evol 2007 24 1596 1599 10.1093/molbev/msm092 17488738
56. The neighbor-joining method: a new method for reconstructing phylogenetic trees. N Saitou M Nei, Mol Biol Evol 1987 4 406 425 3447015
57. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. M Kimura, J Mol Evol 1980 16 111 120 10.1007/BF01731581 7463489
58. Confidence limits on phylogenies: an approach using the bootstrap. J Felsenstein, Evolution 1985 39 783 791 10.2307/2408678
59. The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name 'Sinorhizobium adhaerens' is not validly published. Opinion 84. Judicial Commission of the International Committee on Systematics of Prokaryotes, Int J Syst Evol Microbiol 2008 58 1973 10.1099/ijs.0.2008/005991-0 18676490