The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti

BMC Microbiology

Volumn 10, Issue , 2010, Pages

  De Lucena, Daniella K C ^a   Pühler, Alfred ^a   Weidner, Stefan ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; EXOPOLYSACCHARIDE; IRON; MESSENGER RNA; RHIZOBACTIN; SIDEROPHORE; SIGMA FACTOR; SIGMA FACTOR RPOH 1; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GROWTH; BACTERIUM MUTANT; CARBOHYDRATE SYNTHESIS; CELL MOTILITY; CLASSIFICATION; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FUNCTION; HEAT SHOCK RESPONSE; MICROARRAY ANALYSIS; NONHUMAN; PROTEIN FUNCTION; SINORHIZOBIUM MELILOTI; TRANSCRIPTION REGULATION; GENETICS; METABOLISM; MUTATION; PH; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

SINORHIZOBIUM MELILOTI;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; MUTATION; SIGMA FACTOR; SINORHIZOBIUM MELILOTI; STRESS, PHYSIOLOGICAL;

EID: 77957923220     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-10-265     Document Type: Article

References (65)

1. Eubacterial sigma-factors. MM Wösten, FEMS Microbiol Rev 1998 22 127 150 10.1016/S0168-6445(98)00011-4 9818380
2. Multiple sigma subunits and the partitioning of bacterial transcription space. TM Gruber CA Gross, Annu Rev Microbiol 2003 57 441 466 10.1146/annurev.micro.57.030502.090913 14527287
3. Folding of newly translated proteins in vivo: the role of molecular chaperones. J Frydman, Annu Rev Biochem 2001 70 603 647 10.1146/annurev.biochem. 70.1.603 11395418
4. Molecular chaperones in cellular protein folding. FU Hartl, Nature 1996 381 571 579 10.1038/381571a0 8637592
5. Small heat shock proteins are molecular chaperones. U Jakob M Gaestel K Engel J Buchner, J Biol Chem 1993 268 1517 1520 8093612
6. The heat shock response of Escherichia coli. F Arsène T Tomoyasu B Bukau, Int J Food Microbiol 2000 55 3 9 10.1016/S0168-1605(00)00206-3 10791710
7. Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. E Guisbert T Yura VA Rhodius CA Gross, Microbiol Mol Biol Rev 2008 72 545 554 10.1128/MMBR.00007-08 18772288
8. Regulation of the heat-shock response. T Yura K Nakahigashi, Curr Opin Microbiol 1999 2 153 158 10.1016/S1369-5274(99)80027-7 10322172
9. An RpoH-like heat shock sigma factor is involved in stress response and virulence in Brucella melitensis 16M. M Delory R Hallez JJ Letesson X De Bolle, J Bacteriol 2006 188 7707 7710 10.1128/JB.00644-06 16936018
10. Acid shock proteins of Escherichia coli. M Heyde R Portalier, FEMS Microbiol Lett 1990 57 19 26 10.1111/j.1574-6968.1990.tb04168.x 2199304
11. The Rhizobium etli RpoH1 and RpoH2 sigma factors are involved in different stress responses. JM Martínez-Salazar M Sandoval-Calderon X Guo S Castillo-Ramirez A Reyes MG Loza J Rivera X Alvarado-Affantranger F Sanchez V Gonzalez, et al. Microbiology 2009 155 386 397 10.1099/mic.0.021428-0 19202087
12. Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress. G Nonaka M Blankschien C Herman CA Gross VA Rhodius, Genes Dev 2006 20 1776 1789 10.1101/gad.1428206 16818608
13. Surviving heat shock: control strategies for robustness and performance. H El-Samad H Kurata JC Doyle CA Gross M Khammash, Proc Natl Acad Sci USA 2005 102 2736 2741 10.1073/pnas.0403510102 15668395
14. Genes and signals in the rhizobium-legume symbiosis. SR Long, Plant Physiol 2001 125 69 72 10.1104/pp.125.1.69 11154299
15. Bacteroid formation in the Rhizobium-legume symbiosis. V Oke SR Long, Curr Opin Microbiol 1999 2 641 646 10.1016/S1369-5274(99)00035-1 10607628
16. Root nodulation and infection factors produced by rhizobial bacteria. HP Spaink, Annu Rev Microbiol 2000 54 257 288 10.1146/annurev.micro.54.1.257 11018130
17. 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
18. Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. HA Green TJ Donohue, J Bacteriol 2006 188 5712 5721 10.1128/JB.00405-06 16885439
19. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. T Kaneko Y Nakamura S Sato E Asamizu T Kato S Sasamoto A Watanabe K Idesawa A Ishikawa K Kawashima, et al. DNA Res 2000 7 331 338 10.1093/dnares/7.6.331 11214968
20. Three disparately regulated genes for sigma 32-like transcription factors in Bradyrhizobium japonicum. F Narberhaus P Krummenacher HM Fischer H Hennecke, Mol Microbiol 1997 24 93 9104 10.1046/j.1365-2958.1997.3141685.x 9140968
21. The composite genome of the legume symbiont Sinorhizobium meliloti. F Galibert TM Finan SR Long A Pühler P Abola F Ampe F Barloy-Hubler MJ Barnett A Becker P Boistard, et al. Science 2001 293 668 672 10.1126/science.1060966 11474104
22. Multiple groESL operons are not key targets of RpoH1 and RpoH2 in Sinorhizobium meliloti. AN Bittner V Oke, J Bacteriol 2006 188 3507 3515 10.1128/JB.188.10.3507-3515.2006 16672605
23. Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti. V Oke BG Rushing EJ Fisher M Moghadam-Tabrizi SR Long, Microbiology 2001 147 2399 2408 11535780 (Pubitemid 32899236)
24. Two RpoH homologs responsible for the expression of heat shock protein genes in Sinorhizobium meliloti. Y Ono H Mitsui T Sato K Minamisawa, Mol Gen Genet 2001 264 902 912 10.1007/s004380000380 11254138
25. Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa. H Mitsui T Sato Y Sato N Ito K Minamisawa, Mol Genet Genomics 2004 271 416 425 10.1007/s00438-004-0992-x 15007732
26. Acid tolerance in root nodule bacteria. AR Glenn WG Reeve RP Tiwari MJ Dilworth, Novartis Found Symp 1999 221 112 126 10207916
27. Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions. PH Graham, Can J Microbiol 1992 38 475 484 10.1139/m92-079
28. Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. M Hungria MAT Vargas, Field Crops Research 2000 65 151 164 10.1016/S0378-4290(99)00084-2 (Pubitemid 30152847)
29. Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici Umr1899. PH Graham KJ Draeger ML Ferrey MJ Conroy BE Hammer E Martinez SR Aarons C Quinto, Can J Microbiol 1994 40 10.1139/m94-033
30. The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. C Hellweg A Pühler S Weidner, BMC Microbiol 2009 9 37 37 10.1186/1471-2180-9-37 19216801
31. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. RM Horton, Mol Biotechnol 1995 3 93 99 10.1007/BF02789105 7620981
32. Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. D Lynch J O'Brien T Welch P Clarke PO Cuiv JH Crosa M O'Connell, J Bacteriol 2001 183 2576 2585 10.1128/JB.183.8.2576-2585.2001 11274118
33. Universal chemical assay for the detection and determination of siderophores. B Schwyn JB Neilands, Anal Biochem 1987 160 47 56 10.1016/0003-2697(87)90612-9 2952030
34. Regulation of succinoglycan and galactoglucan biosynthesis in Sinorhizobium meliloti. A Becker S Rüberg B Baumgarth PA Bertram-Drogatz I Quester A Pühler, J Mol Microbiol Biotechnol 2002 4 187 190 11931545
35. Sensory transduction to the flagellar motor of Sinorhizobium meliloti. B Scharf R Schmitt, J Mol Microbiol Biotechnol 2002 4 183 186 11931544
36. Probing for pH-regulated proteins in Sinorhizobium medicae using proteomic analysis. WG Reeve RP Tiwari N Guerreiro J Stubbs MJ Dilworth AR Glenn BG Rolfe MA Djordjevic JG Howieson, J Mol Microbiol Biotechnol 2004 7 140 147 10.1159/000078657 15263818
37. A homologue of the tryptophan-rich sensory protein TspO and FixL regulate a novel nutrient deprivation-induced Sinorhizobium meliloti locus. ME Davey FJ de Bruijn, Appl Environ Microbiol 2000 66 5353 5359 10.1128/AEM.66.12.5353-5359. 2000 11097914
38. The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions. WG Reeve L Brau J Castelli G Garau C Sohlenkamp O Geiger MJ Dilworth AR Glenn JG Howieson RP Tiwari, Microbiology 2006 152 3049 3059 10.1099/mic.0.28764-0 17005985
39. The Sinorhizobium meliloti lon protease is involved in regulating exopolysaccharide synthesis and is required for nodulation of alfalfa. ML Summers LM Botero SC Busse TR McDermott, J Bacteriol 2000 182 2551 2558 10.1128/JB.182.9.2551-2558.2000 10762258
40. New substrates for the dicarboxylate transport system of Sinorhizobium meliloti. S Yurgel MW Mortimer KN Rogers ML Kahn, J Bacteriol 2000 182 4216 4221 10.1128/JB.182.15.4216-4221.2000 10894729
41. An extracytoplasmic function sigma factor acts as a general stress response regulator in Sinorhizobium meliloti. L Sauviac H Philippe K Phok C Bruand, J Bacteriol 2007 189 4204 4216 10.1128/JB.00175-07 17400745
42. Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. E Krol A Becker, Mol Genet Genomics 2004 272 1 17 10.1007/s00438-004-1030-8 15221452
43. Sinorhizobium meliloti 1021 loss-of-function deletion mutation in chvI and its phenotypic characteristics. C Wang J Kemp IO Da Fonseca RC Equi X Sheng TC Charles BW Sobral, Mol Plant Microbe Interact 2010 23 153 160 10.1094/MPMI-23-2-0153 20064059
44. The acid-inducible asr gene in Escherichia coli: transcriptional control by the phoBR operon. E Suziedeliene K Suziedelis V Garbenciute S Normark, J Bacteriol 1999 181 2084 2093 10094685
45. A genomic perspective on protein families. RL Tatusov EV Koonin DJ Lipman, Science 1997 278 631 637 10.1126/science.278.5338.631 9381173
46. Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. M Sakoh K Ito Y Akiyama, J Biol Chem 2005 280 33305 33310 10.1074/jbc.M506180200 16076848 (Pubitemid 41397126)
47. GrpE, a nucleotide exchange factor for DnaK. C Harrison, Cell Stress Chaperones 2003 8 218 224 10.1379/1466-1268(2003)008<0218:GANEFF 2.0.CO;2 14984054
48. Multiple small heat shock proteins in rhizobia. M Münchbach A Nocker F Narberhaus, J Bacteriol 1999 181 83 90 9864316
49. Sensitization of Escherichia coli cells to oxidative stress by deletion of the rpoH gene, which encodes the heat shock sigma factor. T Kogoma T Yura, J Bacteriol 1992 174 630 632 1729253
50. Effects of organic acids and low pH on Rhizobium meliloti 104A14. R Perez-Galdona ML Kahn, Microbiology 1994 140 1231 1235 10.1099/13500872-140-5- 1231 8025689
51. Escherichia coli acid resistance: tales of an amateur acidophile. JW Foster, Nat Rev Microbiol 2004 2 898 907 10.1038/nrmicro1021 15494746
52. Sinorhizobium meliloti rpoE2 is necessary for H(2)O(2) stress resistance during the stationary growth phase. M Flechard C Fontenelle A Trautwetter G Ermel C Blanco, FEMS Microbiol Lett 2009 290 25 31 10.1111/j.1574-6968.2008. 01401.x 19025578
53. A sigma54-dependent promoter in the regulatory region of the Escherichia coli rpoH gene. A Janaszak W Majczak B Nadratowska A Szalewska-Palasz G Konopa A Taylor, Microbiology 2007 153 111 123 10.1099/mic.0.2006/000463-0 17185540
54. Exploring the metabolic and genetic control of gene expression on a genomic scale. JL DeRisi VR Iyer PO Brown, Science 1997 278 680 686 10.1126/science.278.5338.680 9381177
55. J Sambrook EF Fritsch T Maniatis, Molecular cloning: A laboratory manual Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press 1989
56. R factor transfer in Rhizobium leguminosarum. JE Beringer, J Gen Microbiol 1974 84 188 198 4612098
57. JM Vincent, A Manual for the Practical Study of the Root-Nodule Bacteria Oxford-Edinburgh Blackwell Scientific (Oxford) 1970
58. 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. A Schäfer A Tauch W Jäger J Kalinowski G Thierbach A Pühler, Gene 1994 145 69 73 10.1016/0378-1119(94) 90324-7 8045426
59. Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. S Rüberg ZX Tian E Krol B Linke F Meyer Y Wang A Pühler S Weidner A Becker, J Biotechnol 2003 106 255 268 10.1016/j.jbiotec.2003.08.005 14651866
60. EMMA: a platform for consistent storage and efficient analysis of microarray data. M Dondrup A Goesmann D Bartels J Kalinowski L Krause B Linke O Rupp A Sczyrba A Pühler F Meyer, J Biotechnol 2003 106 135 146 10.1016/j.jbiotec.2003.08.010 14651856
61. Sinorhizobium meliloti 1021 Sm14kOLI. http://www.cebitec.uni-bielefeld. de/transcriptomics/transcriptomics-facility/sm14koli.html
62. Genesis: cluster analysis of microarray data. A Sturn J Quackenbush Z Trajanoski, Bioinformatics 2002 18 207 208 10.1093/bioinformatics/18.1.207 11836235
63. EMMA server. http://www.cebitec.uni-bielefeld.de/groups/brf/software/ emma-info/
64. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. HM Meade SR Long GB Ruvkun SE Brown FM Ausubel, J Bacteriol 1982 149 114 122 6274841
65. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. SG Grant J Jessee FR Bloom D Hanahan, Proc Natl Acad Sci USA 1990 87 4645 4649 10.1073/pnas.87.12.4645 2162051