Proteomic profiling of Rhizobium tropici PRF 81: Identification of conserved and specific responses to heat stress

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Gomes, Douglas Fabiano ^a,b   Batista, Jesiane Stefânia Da Silva ^a,c   Schiavon, Aline Luiza ^a,c   Andrade, Diva Souza ^d   Hungria, Mariangela ^a,b  

^a EMBRAPA CERRADOS   (Brazil)

^b STATE UNIVERSITY OF LONDRINA   (Brazil)

^c Univ Filadélfia de Londrina UNIFIL   (Brazil)

^d INSTITUTO AGRONÔMICO DO PARANÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHAPERONIN 60; PROTEIN; PROTEIN DNAK;

ADAPTATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BEAN; BRAZIL; CROP; GENOME; HEAT STRESS; HEAT TOLERANCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NITROGEN FIXATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEOMICS; RHIZOBIUM TROPICI; TROPICS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BACTERIAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; PROTEOME; PROTEOMICS; RHIZOBIUM TROPICI; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STRESS, PHYSIOLOGICAL; TEMPERATURE;

BACTERIA (MICROORGANISMS); RHIZOBIUM TROPICI;

EID: 84861548330     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-84     Document Type: Article

References (81)

1. Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Vance CP, Plant Physiol 2001 127 390 397 10.1104/pp.010331 11598215
2. Legumes: Importance and constraints to greater utilization. Graham PH, Vance CP, Plant Physiol 2003 131 872 877 10.1104/pp.017004 12644639
3. Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Saravanan VS, Madhaiyan M, Osborne J, Thangaraju M, Sa TM, Microb Ecol 2008 55 130 140 10.1007/s00248-007-9258-6 17574542
4. Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Ribeiro RA, Barcellos FG, Thompson FL, Hungria M, Res Microbiol 2009 160 297 306 10.1016/j.resmic.2009.03.009 19403105
5. Sym plasmid transfer to various symbiotic mutants of Rhizobium trifolii, R. leguminosarum, and R. meliloti. Djordjevic MA, Zurkowski W, Shine J, Rolfe BG, J Bacteriol 1983 156 1035 1045 6315675
6. Induced plasmid-genome rearrangements in Rhizobium japonicum. Berry JO, Atherly AG, J Bacteriol 1984 157 218 224 6360996
7. New sources of high temperature tolerant rhizobia for Phaseolus vulgaris. Hungria M, Franco AA, Sprent JI, Plant Soil 1993 149 103 109 10.1007/BF00010767
8. Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Hungria M, Vargas MAT, Field Crops Res 2000 65 151 164 10.1016/S0378-4290(99)00084-2
9. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Martínez-Romero E, Segovia E, Mercante FM, Franco AA, Graham PH, Pardo MA, Int J System Bacteriol 1991 41 417 426 10.1099/00207713-41-3-417
10. Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Hungria M, Andrade DS, Chueire LMO, Probanza A, Guttierrez-Mañero FJ, Megías M, Soil Biol Biochem 2000 32 1515 1528 10.1016/S0038-0717(00)00063-8
11. Benefits of inoculation of common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Hungria M, Campo RJ, Mendes IC, Biol Fertil Soil 2003 39 88 93 10.1007/s00374-003-0682-6
12. Novel genes related to nodulation, secretion systems, and surface structures revealed by a genome draft of Rhizobium tropici strain PRF 81. Pinto FGS, Chueire LMO, Vasconcelos ATR, Nicolás MF, Almeida LGP, Souza RC, Menna P, Barcellos FG, Megías M, Hungria M, Funct Integr Genomics 2009 9 263 270 10.1007/s10142-009-0109-z 19184146
13. Polyphasic characterization of Brazilian Rhizobium tropici strains effective in fixing N2 with common bean (Phaseolus vulgaris L.). Pinto FGS, Hungria M, Mercante FM, Soil Biol Biochem 2007 39 1851 1864 10.1016/j.soilbio. 2007.01.001
14. Growth phase and cell division dependent activation and inactivation of the σ32 regulon in Escherichia coli. Wagner MA, Zahrl D, Rieser G, Koraimann G, J Bacteriol 2009 191 1695 1702 10.1128/JB.01536-08 19114495
15. Protein expression profile of Gluconacetobacter diazotrophicus PAL5, a sugarcane endophytic plant growth-promoting bacterium. Lery LM, Coelho A, Von Kruger WM, Gonçalves MS, Santos MF, Valente RH, Proteomics 2008 8 1631 1644 10.1002/pmic.200700912 18340630
16. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Bradford MM, Anal Biochem 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051
17. A two-dimensional electrophoretic profile of the proteins secreted by Herbaspirillum seropedicae strain Z78. Chaves DFS, Souza EM, Monteiro RA, Pedrosa FO, J Proteomics 2009 73 50 56 10.1016/j.jprot.2009.07.012 19664734
18. The COG database: a tool for genome scale analysis of protein functions and evolution. Tatusov RL, Galperin M, Natale DA, Koonin EV, Nucleic Acids Res 2000 28 33 36 10.1093/nar/28.1.33 10592175
19. PSORTb v.2.0: Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Gardy JL, Laird MR, Chen F, Rey S, Walsh CJ, Ester M, Brinkman FS, Bioinformatics 2005 21 617 623 10.1093/bioinformatics/bti057 15501914
20. PSLpred: prediction of subcellular localization of bacterial proteins. Bhasin M, Garg A, Raghava GPS, Bioinformatics 2005 21 2522 2524 10.1093/bioinformatics/bti309 15699023
21. Metabolomic and transcriptomic stress response of Escherichia coli. Szymon J, Sebastian K, Gareth C, Jedrzej S, Alvaro C-I, Dirk S, Joachim S, Lothar W, Mol Syst Biol 2010 6 364 20461071
22. Towards a two-dimensional proteomic reference map of Bradyrhizobium japonicum CPAC 15: spotlighting hypothetical proteins Batista JSS, Torres AR, Hungria M, Proteomics 2010 10 3176 3189 10.1002/pmic.201000092 20806226
23. Octopine and nopaline metabolism in Agrobacterium tumefaciens and crown gall tumor cells: role of plasmid genes. Montoya AL, Chilton MD, Gordon MP, Sciaky D, Nester EW, J Bacteriol 1977 129 101 107 830636
24. An Experimental Test of the Rhizopine Concept in Rhizobium meliloti. Gordon DM, Ryder MH, Heinrich K, Murphy PJ, Appl Environ Microbiol 1996 62 3991 3996 16535438
25. Molecular basis for regulation of the heat shock transcription factor σ32 by the DnaK and DnaJ chaperones. Rodriguez F, Arsene-Ploetze F, Rist W, Rudiger S, Schneider-Mergener J, Mayer MP, Bukau B, Mol Cell 2008 32 347 358 10.1016/j.molcel.2008.09.016 18995833
26. (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Brencic A, Winans SC, Microbiol Mol Biol Rev 2005 69 155 194 10.1128/MMBR.69.1.155-194.2005 15755957
27. Expression and Assembly of a Functional Type IV Secretion System Elicit Extracytoplasmic and Cytoplasmic Stress Responses inEscherichia coli. Zahrl D, Wagner M, Bischof K, Koraimann G, J Bacteriol 2006 188 6611 6621 10.1128/JB.00632-06 16952953
28. Sigma factors inPseudomonas aeruginosa. Potvin E, Sanschagrin F, Levesque RC, FEMS Microbiol Rev 2008 32 38 55 10.1111/j.1574-6976.2007.00092.x 18070067
29. Identification and characterization of the ntrcBC and ntrYX genes in Acetobacter diazotrophicus. Meletzus D, Zellermann EM, Kennedy C, Biological Nitrogen Fixation for the 21st Century Kluwer Academic Publishers, Dordrecht, Elmerich C, Kondorosi A, Newton WE, 1998 125 126
30. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Capela D, Barloy-Hubler F, Gouzy J, Bothe G, Ampe F, Batut J, Boistard P, Becker A, Boutry M, Cadieu E, Dréano S, Gloux S, Godrie T, Goffeau A, Kahn D, Kiss E, Lelaure V, Masuy D, Pohl T, Portetelle D, Pühler A, Purnelle B, Ramsperger U, Renard C, Thébault P, Vandenbol M, Weidner S, Galibert F, Proc Natl Acad Sci 2001 98 9877 9882 10.1073/pnas.161294398 11481430
31. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S, DNA Res 2000 7 331 338 10.1093/dnares/7.6.331 11214968
32. Identification and characterization of the two component NtrY/NtrX regulatory system in Azospirillum brasilense. Ishida ML, Assumpção MC, Machado HB, Benelli EM, Souza EM, Pedrosa FO, Braz J Med Biol Res 2002 35 651 661 10.1590/S0100-879X2002000600004 12045829
33. Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Pawlowski K, Klosse U, de Bruijn FJ, Mol Gen Genomics 1991 231 124 138 10.1007/BF00293830
34. The periplasmic regulator ExoR inhibits ExoS/ChvI two-component signaling in Sinorhizobium meliloti. Chen EJ, Sabio EA, Long SR, Mol Microbiol 2008 69 1290 1303 10.1111/j.1365-2958.2008.06362.x 18631237
35. Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 55) and a complex acidmediated signaling involved in Agrobacterium-plant interactions. Yuan ZC, Liu P, Saenkham P, Kerr K, Nester EW, J Bacteriol 2008 190 494 507 10.1128/JB.01387-07 17993523
36. Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. Cheng HP, Walker GC, J Bacteriol 1998 180 20 26 9422587
37. Investigations of Rhizobium biofilm formation. Fujishige NA, Kapadia NN, de Hoff PL, Hirsch AM, FEMS Microbiol Ecol 2006 56 195 206 10.1111/j.1574-6941. 2005.00044.x 16629750
38. ExoR is genetically coupled to the ExoS-ChvI two-component system and located in the periplasm of Sinorhizobium meliloti. Wells DH, Chen EJ, Fisher RF, Long SR, Mol Microbiol 2007 64 647 664 10.1111/j.1365-2958.2007.05680.x 17462014
39. Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. Yao SY, Luo L, Har KJ, Becker A, Rüberg S, Yu GQ, Zhu JB, Cheng HP, J Bacteriol 2004 186 6042 6049 10.1128/JB.186.18.6042- 6049.2004 15342573
40. Identification of novel Sinorhizobium meliloti mutants compromised for oxidative stress protection and symbiosis. Davies BW, Walker GC, J Bacteriol 2007 189 2110 2113 10.1128/JB.01802-06 17172326
41. Evolution of the chaperonin families (Hsp60, Hsp10, and Tcp-1) of proteins and the origin of eukaryotic cells. Gupta RS, Mol Microbiol 1995 15 1 11 10.1111/j.1365-2958.1995.tb02216.x 7752884
42. A two-dimensional protein gel electrophoresis study of the heat stress response of Bacillus subtilis cells during sporulation. Movahedi S, Waites W, J Bacteriol 2000 182 4758 4763 10.1128/JB.182.17.4758-4763.2000 10940015
43. Multiple small heat shock proteins in rhizobia. Münchbach M, Nocker A, Narberhaus F, J Bacteriol 1999 181 83 90 9864316
44. A genome-scale proteomic screen identifies a role for DnaK in chaperoning of polar autotransporters in Shigella. Janakiraman A, Fixen KR, Gray AN, Niki H, Goldberg MB, J Bacterioly 2009 191 6300 6311 10.1128/JB.00833-09
45. Converging concepts of protein folding in vitro and in vivo. Hartl FU, Hayer-Hartl M, Nature Struct Mol Biol 2009 16 574 581 10.1038/nsmb.1591
46. Regulation of the Escherichia coli heat shock response. Bukau B, Mol Microbiol 1993 9 671 680 10.1111/j.1365-2958.1993.tb01727.x 7901731
47. Georgopoulos C, Liberek K, Zylicz M, Ang D, The Biology of Heat Shock Proteins and Molecular Chaperones: Monograph 26 Cold Spring Harbor Laboratory, Cold Spring Harbor 1994 209 249
48. Regulation and conservation of the heat-shock transcription factor sigma32. Yura T, Genes Cells 1996 1 277 284 10.1046/j.1365-2443.1996.28028.x 9133661
49. Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. Alexandre A, Oliveira S, FEMS Microbiol Ecol 2011 75 28 36 10.1111/j.1574-6941.2010.00993.x 21073488
50. A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates the activity of the Escherichia coli heat shock transcription factor sigma32. Gamer J, Multhaup G, Tomoyasu T, McCarty JS, Rudiger S, Schonfeld HJ, Schirra C, Bujard H, Bukau BA, EMBO J 1996 15 607 617 8599944
51. Function and regulation of the heat shock proteins. Gross CA, Escherichia coli and Samonella ASM Press, Washington DC, Neidhard FC, 1996 1382 1399
52. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. Fayet O, Ziegelhoffer T, Georgopoulos C, J Bacteriol 1989 171 1379 1385 2563997
53. Identification of proteins involved in the heat stress response of Bacillus cereus ATCC 14579. Periago PM, Van Schaik W, Abee T, Wouters JA, Appl Environ Microbiol 2002 68 3486 3495 10.1128/AEM.68.7.3486-3495.2002 12089032
54. DnaK and GroEL are induced in response to antibiotic and heat shock in Acinetobacter baumannii. Cardoso K, Gandra RF, Wisniewski ES, Osaku CA, Kadowaki MK, Felipach-Neto V, Haus LFA, Simão RCG, J Med Microbiol 2010 59 1061 1068 10.1099/jmm.0.020339-0 20576751
55. Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP. Goloubinoff P, Christeller JT, Gatenby AA, Lorimer GH, Nature 1989 342 884 889 10.1038/342884a0 10532860
56. Structure and function in GroEL mediated protein folding. Sigler PB, Xu Z, Rye HS, Burston SG, Fenton WA, Horwich AL, Annu Rev Biochem 1998 67 581 608 10.1146/annurev.biochem.67.1.581 9759498
57. Chaperone properties of bacterial elongation factor EF-Tu. Caldas TD, Yaagoubi A, Richarme G, J Biol Chem 1998 273 11478 11482 10.1074/jbc.273.19. 11478 9565560
58. Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. Caldas T, Laalami S, Richarme G, J Biol Chem 2000 275 855 860 10.1074/jbc.275.2.855 10625618
59. Translation. Brot N, Molecular Mechanisms of Protein Synthesis Academic, New York, Weissbach H, Pestka S, 1977 375 411
60. Molecular chaperone functions of heat shock proteins. Hendrick JP, Hartl FU, Annu Rev Biochem 1993 62 349 384 10.1146/annurev.bi.62.070193.002025 8102520
61. Abundance and membrane association of elongation factor Tu in E. coli. Jacobson GR, Rosenbuch JP, Nature 1976 261 23 26 10.1038/261023a0 775340
62. Renaturation of rhodanese by translational elongation factor (EF) Tu-protein refolding by EF-Tu flexing. Kudlicki W, Coffman A, Kramer G, Hardesty B, J Biol Chem 1997 272 32206 32210 10.1074/jbc.272.51.32206 9405422
63. Grunberg-Manago M, Escherichia coli and Salmonella typhimurium Cellular and Molecular biology ASM Press, Washington, DC, Neidhardt FC, 2 1996 1432 1457
64. Reactive Oxygen Species during Plant-microorganism Early Interactions. Nanda AK, Andrio E, Marino D, Pauly N, Dunand C, J Integr Plant Biol 2010 52 195 204 10.1111/j.1744-7909.2010.00933.x 20377681
65. Localization of Reactive Oxygen species During Symbiosis of Early clover and Rhizobium leguminosarum bv Trifolii. Kopcinska J, Acta Biologica Cracoviensia Series Botanica 2009 51 93 98
66. Nitric Oxide in Legume-Rhizobium Symbiosis. Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R, Plant Sci 2011 181 573 581 10.1016/j.plantsci.2011.04. 007 21893254
67. ROS production during symbiotic infection suppresses pathogenesis-related gene expression. Peleg-Grossman S, Melamed-Book N, Levine A, Plant Signal Behav 2012 7 409 416 10.4161/psb.19217 22499208
68. Genome characteristics of facultatively symbioticFrankiasp. strains reflect host range and host plant biogeography. Normand P, Lapierre P, Tisa LS, Gogarten JP, Genome Res 2007 17 7 15 17151343
69. Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. Pauly N, Pucciariello C, Mandon K, Innocenti G, J Exp Bot 2006 57 1769 1776 10.1093/jxb/erj184 16698817
70. Thioredoxin regenerates proteins inactivated by oxidative stress in endothelial cells. Fernando MR, Nanri H, Yoshitake S, Nagato-Kuno K, Minakami S, Eur J Biochem 1992 209 917 922 10.1111/j.1432-1033.1992.tb17363.x 1425698
71. Oxidative stress in bacteria and protein damage by reactive oxygen species. Cabiscol E, Tamarit J, Ros J, Internatl Microbiol 2000 3 3 8
72. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. Scharf C, Riethdorf S, Ernst H, Engelmann S, Volker U, Hecker M, J Bacteriol 1998 180 1869 1877 9537387
73. Proteomics reveals differential expression of proteins related to a variety of metabolic pathways by genistein-induced Bradyrhizobium japonicum strains. Batista JSS, Hungria M, J Proteomics 2012 75 1211 1219 10.1016/j.jprot.2011.10.032 22119543
74. Proteome of Gluconacetobacter diazotrophicus co-cultivated with sugarcane plantlets. Santos MF, Pádua VLM, Nogueira EM, Hemerly AS, Domont GB, J Proteomics 2010 73 917 931 10.1016/j.jprot.2009.12.005 20026003
75. Overexpression of bacterioferritin comigratory protein (Bcp) enhance viability and reduced glutathione level in the fission yeast under stress. Kang G, Park E, Kim K, Lim C, J Microbiol 2009 47 60 67 10.1007/s12275-008-0077-3 19229492
76. Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Morgan RW, Christman MF, Jacobson FS, Storz G, Ames BN, Proc Nati Acad Sci USA 1986 83 8059 8063 10.1073/pnas.83.21. 8059
77. Insights into the oxidative stress response in Francisella tularensis LVS and its mutant DiglC1+2 by proteomics analysis. Lenco J, Pavkova I, Hubalek M, Stulik J, FEMS Microbiol Lett 2006 246 47 54
78. NADPH recycling systems in oxidative stressed pea nodules: a key role for the NADP+-dependent isocitrate dehydrogenase. Marino D, González EM, Frendo P, Puppo A, Arrese-Igor C, Planta 2007 225 413 421 16896792
79. Isocitrate dehydrogenase is important for nitrosative stress resistance in Cryptococcus neoformans, but oxidative stress resistance is not dependent on glucose-6-phosphate dehydrogenase. Brown SM, Upadhya R, Shoemaker JD, Lodge JK, Eukaryot Cell 2010 9 971 980 10.1128/EC.00271-09 20400467
80. WrbA from Escherichia coli and Archaeoglobus fulgidusIs an NAD(P)H: quinone oxidoreductase. Patridge EV, Ferry JG, J Bacteriol 2006 188 3498 3506 10.1128/JB.188.10.3498-3506.2006 16672604
81. Crystal structure of the NADH:quinone oxidoreductase WrbA from Escherichia coli. Andrade SLA, Patridge EV, Ferry JG, Einsle O, J Bacteriol 2007 189 9101 9107 10.1128/JB.01336-07 17951395