Genome-wide transcriptional and physiological responses of Bradyrhizobium japonicum to paraquat-mediated oxidative stress

Applied and Environmental Microbiology

Volumn 77, Issue 11, 2011, Pages 3633-3643

  Donati, Andrew J ^a   Jeon, Jeong Min ^a,b   Sangurdekar, Dipen ^c   So, Jae Seong ^b   Chang, Woo Suk ^a  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

^b Inha University   (South Korea)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP SYNTHASE; BRADYRHIZOBIUM JAPONICUM; CELLULAR PROTEINS; DEFENSE MECHANISM; EPS PRODUCTION; EXOPOLYSACCHARIDES; GENE EXPRESSION DATA; GENES ENCODING; GLYCINE MAX; NODULATION; OXIDATIVE BURSTS; PHYSIOLOGICAL RESPONSE; PUTATIVE OPERONS; REACTIVE OXYGEN SPECIES; RESPONSE ELEMENTS; RHIZOBIAL BACTERIA; RIBOSOMAL PROTEINS; SCAVENGING ENZYMES; SIGMA FACTOR; SOYBEAN PLANTS; STRESS RESPONSE; SUPER OXIDE DISMUTASE; SUPEROXIDES; SYMBIOTIC BACTERIA;

AMINO ACIDS; BACTERIA; BIOCHEMISTRY; HERBICIDES; NITROGEN FIXATION; OXYGEN; PHYSIOLOGICAL MODELS; PHYSIOLOGY; TRANSCRIPTION; TRANSCRIPTION FACTORS;

GENES;

PARAQUAT;

CARBOHYDRATE; DEFENSE MECHANISM; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; GENE EXPRESSION; GENOME; HOST-SYMBIONT INTERACTION; LEGUME; NODULATION; OXIDATION; OXIDE; OXYGEN; PATHOGENICITY; PHYSIOLOGICAL RESPONSE; RHIZOBACTERIUM; SOYBEAN; SYMBIOSIS;

ARTICLE; BRADYRHIZOBIUM; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS;

BRADYRHIZOBIUM; GENE EXPRESSION PROFILING; OXIDATIVE STRESS; PARAQUAT; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM JAPONICUM; GLYCINE MAX;

EID: 79958243757     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00047-11     Document Type: Article

References (60)

1. Adler, J. 1973. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J. Gen. Microbiol. 74:77-91.
2. Ahn, S. J., Z. T. Wen, and R. A. Burne. 2007. Effects of oxygen on virulence traits of Streptococcus mutans. J. Bacteriol. 189:8519-8527.
3. Baker, C. J., E. W. Orlandi. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321.
4. Baker, C. J., N. Mock, J. Glazener, and E. Orlandi. 1993. Recognition responses in pathogen/non-host and race/cultivar interactions involving soybean (Glycine max) and Pseudomonas syringae pathovars. Physiol. Mol. Plant Pathol. 43:81-94.
5. Barloy-Hubler, F., A. Cheron, A. Hellegouarch, and F. Galibert. 2004. Smc01944, a secreted peroxidase induced by oxidative stresses in Sinorhizobium meliloti 1021. Microbiology 150:657-664.
6. Bergmaier, D., C. Lacroix, M. G. Macedo, and C. P. Champagne. 2001. New method for exopolysaccharide determination in culture broth using stirred ultrafiltration cells. Appl. Microbiol. Biotechnol. 57:401-406.
7. Bittner, M., et al. 2003. Expression analysis of RNA, p. 101-288. In D. Bowtell and J. Sambrook (ed.), DNA microarrays: a molecular cloning manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
8. Blumenkrantz, N., and G. Asboe-Hansen. 1973. New method for quantitative determination of uronic acids. Anal. Biochem. 54:484-489.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Breedveld, M. W., L. P. T. M. Zevenhuizen, and A. J. B. Zehnder. 1991. Osmotically-regulated trehalose accumulation and cyclic-(1,2)-glucan excretion by Rhizobium leguminosarum biovar trifolii TA-1. Arch. Microbiol. 156: 501-506.
11. Broughton, W. J., S. Jabbouri, and X. Perret. 2000. Keys to symbiotic harmony. J. Bacteriol. 182:5641-5652.
12. Bylund, J., L. A. Burgess, P. Cescutti, R. K. Ernst, and D. P. Speert. 2006. Exopolysaccharides from Burkholderia cenocepacia inhibit neutrophil chemotaxis and scavenge reactive oxygen species. J. Biol. Chem. 281:2526-2532.
13. Carr, R. J. G., R. F. Bilton, and T. Atkinson. 1986. Toxicity of paraquat to microorganisms. Appl. Environ. Microbiol. 52:1112-1116.
14. Chang, W., D. A. Small, F. Toghrol, and W. E. Bentley. 2006. Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide. J. Bacteriol. 188:1648-1659.
15. Chang, W.-S., et al. 2007. An oligonucleotide microarray resource for transcriptional profiling of Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 20:1298-1307.
16. Chang, W.-S., et al. 2007. Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J. Bacteriol. 189:8290-8299.
17. Chang, W.-S., X. Li, and L. J. Halverson. 2009. Reduced water availability influences endogenous oxidative stress and cell death within unsaturated Pseudomonas putida biofilms. Environ. Microbiol. 11:1482-1492.
18. Costerton, J. W., et al. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41:435-464.
19. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
20. Cytryn, E. J., et al. 2007. Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation-induced stress. J. Bacteriol. 189: 6751-6762.
21. Dubois, M., K. A. Giles, J. K. Hamilton, P. A. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350-356.
22. Fellay, R., J. Frey, and H. Krisch. 1987. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52:147-154.
23. Fischer, H. M., et al. 2001. One of two hemN genes in Bradyrhizobium japonicum is functional during anaerobic growth and in symbiosis. J. Bacteriol. 183:1300-1311.
24. Franck, W. L., et al. 2008. Whole-genome transcriptional profiling of Bradyrhizobium japonicum during chemoautotrophic growth. J. Bacteriol. 190: 6697-6705.
25. Gregroy, E. M., F. J. Yost, Jr., and I. Fridovich. 1973. Superoxide dismutases of Escherichia coli: intracellular localization and functions. J. Bacteriol. 115: 987-991.
26. Hassan, H. M., and I. Fridovich. 1977. Enzymatic defenses against the toxicity of oxygen and of streptonigrin in Escherichia coli. J. Bacteriol. 129: 1574-1583.
27. Hassan, H. M., and I. Fridovich. 1979. Paraquat and Escherichia coli: mechanism and production of extracellular superoxide radical. J. Biol. Chem. 254:10846-10852.
28. Hassan, H. M., and I. Fridovich. 1977. Regulation of the synthesis of superoxide dismutase in Escherichia coli. J. Biol. Chem. 252:7667-7672.
29. Hassan, H. M., and I. Fridovich. 1978. Superoxide radical and oxygen enhancement of the toxicity of paraquat to Escherichia coli. J. Biol. Chem. 253:8143-8148.
30. Kachlany, S. C., et al. 2001. Structure and carbohydrate analysis of the exopolysaccharide capsule of Pseudomonas putida G7. Environ. Microbiol. 3:774-784.
31. Keppler, L. D., C. J. Baker, and M. M. Atkinson. 1989. Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells. Phytopathology 79:974-978.
32. Kerr, M. K., M. Martin, and G. A. Churchill. 2000. Analysis of variance for gene expression microarray data. J. Comput. Biol. 7:819-837.
33. Kiraly, Z., H. M. El-Zahaby, and Z. Klement. 1997. Role of extracellular polysaccharide (EPS) slime of plant pathogenic bacteria in protecting cells to reactive oxygen species. J. Phytopathol. 145:59-68.
34. Kuzma, M. M., S. Hunt, and D. B. Layzell. 1993. Role of oxygen in the limitation and inhibition of nitrogenase activity and respiration rate in individual soybean nodules. Plant Physiol. 101:161-169.
35. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
36. Mehdy, M. C. 1994. Active oxygen species in plant defense against pathogens. Plant Physiol. 105:467-472.
37. Mesa, S., Z. Ucurum, H. Hennecke, and H. M. Fischer. 2005. Transcription activation in vitro by the Bradyrhizobium japonicum regulatory protein FixK2. J. Bacteriol. 187:3329-3338.
38. Nellen-Anthamatten, D., et al. 1998. Bradyrhizobium japonicum FixK2, a crucial distributor in the FixLJ-dependent regulatory cascade for control of genes inducible by low oxygen levels. J. Bacteriol. 180:5251-5255.
39. Panek, H. R., and M. R. O'Brian. 2004. KatG is the primary detoxifier of hydrogen peroxide produced by aerobic metabolism in Bradyrhizobium japonicum. J. Bacteriol. 186:7874-7880.
40. Parniske, M., and J. A. Downie. 2003. Locks, keys, and symbioses. Nature 425:569-570.
41. Pessi, G., et al. 2007. Genome-wide transcript analysis of Bradyrhizobium japonicum bacteroids in soybean root nodules. Mol. Plant Microbe Interact. 20:1353-1363.
42. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:2002-2007.
43. Pomposiello, P. J., M. H. J. Bennik, and B. Demple. 2001. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J. Bacteriol. 183:3890-3902.
44. Preisig, O., D. Anthamatten, and H. Hennecke. 1993. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. U. S. A. 90:3309-3313.
45. Preisig, O., R. Zufferey, L. Thony-Meyer, C. A. Appleby, and H. Hennecke. 1996. A high-affinity cbb3-type cytochrome oxidase terminates the symbiosisspecific respiratory chain of Bradyrhizobium japonicum. J. Bacteriol. 178: 1532-1538.
46. Read, R. R., and J. W. Costerton. 1987. Purification and characterization of adhesive exopolysaccharides from Pseudomonas putida and Pseudomonas fluorescens. Can. J. Microbiol. 33:1080-1090.
47. Robinson, K. M., et al. 2006. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U. S. A. 103:15038-15043.
48. Sadowsky, M. J., R. E. Tully, P. B. Cregan, and H. H. Keyser. 1987. Genetic diversity in Bradyrhizobium japonicum serogroup 123 and its relation to genotype-specific nodulation of soybean. Appl. Environ. Microbiol. 53:2624-2630.
49. Salunkhe, P., et al. 2002. GeneChip expression analysis of the response of Pseudomonas aeruginosa to paraquat-induced superoxide stress. Genome Lett. 4:165-174.
50. Salunkhe, P., T. Topfer, J. Buer, and B. Tummler. 2005. Genome-wide transcriptional profiling of the steady-state response of Pseudomonas aeruginosa to hydrogen peroxide. J. Bacteriol. 187:2565-2572.
51. Santos, R., D. Herouart, S. Siguad, D. Touati, and A. Puppo. 2001. Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant Microbe Interact. 14:86-89.
52. Sutherland, M. W. 1991. The generation of oxygen radicals during host plant responses to infection. Physiol. Mol. Plant Pathol. 39:79-94.
53. Tamarit, J., E. Cabiscol, and J. Ros. 1998. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J. Biol. Chem. 273:3027-3032.
54. Tamaru, Y., Y. Takani, T. Yoshida, and T. Sakamoto. 2005. Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol. 71: 7327-7333.
55. Tao, H., C. Bausch, C. Richmond, F. R. Blattner, and T. Conway. 1999. Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media. J. Bacteriol. 181:6425-6440.
56. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116-5121.
57. Wang, S., et al. 2009. Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl. Environ. Microbiol. 75:6110-6123.
58. Windgassen, M., A. Urban, and K. E. Jaeger. 2000. Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 193:201-205.
59. Zhao, H., et al. 2005. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc. Natl. Acad. Sci. U. S. A. 102:5727-5732.
60. Zhao, H., et al. 2003. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34:1359-1368.