Antioxidant enzymes activities of Burkholderia spp. strains—oxidative responses to Ni toxicity

Environmental Science and Pollution Research

Volumn 22, Issue 24, 2015, Pages 19922-19932

  Dourado, M N ^a   Franco, M R ^a   Peters, L P ^a   Martins, P F ^a   Souza, L A ^a   Piotto, F A ^a   Azevedo, R A ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antioxidant defense; Catalase; Glutathione reductase; Heavy metals; Oxidative stress; Rhizosphere bacteria; Superoxide dismutase

Indexed keywords

ANTIOXIDANT; BACTERIUM; ENZYME ACTIVITY; NICKEL; RHIZOSPHERE; TOXICITY;

BACTERIA (MICROORGANISMS); BURKHOLDERIA;

ANTIOXIDANT; NICKEL; SOIL POLLUTANT;

BIOREMEDIATION; BURKHOLDERIA; DRUG EFFECTS; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; SOIL POLLUTANT; SPECIES DIFFERENCE; TOXICITY;

ANTIOXIDANTS; BIODEGRADATION, ENVIRONMENTAL; BURKHOLDERIA; NICKEL; OXIDATION-REDUCTION; OXIDATIVE STRESS; SOIL MICROBIOLOGY; SOIL POLLUTANTS; SPECIES SPECIFICITY;

EID: 84951568221     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-015-5204-1     Document Type: Article

References (70)

1. Allocati N, Federici L, Masulli M, Di Ilio C (2008) Glutathione transferases in bacteria. FEBS J 276:58–75
2. Azcón R, Perálvarez MDC, Roldán A, Barea J-M (2010) Arbuscular mycorrhizal fungi, Bacillus cereus, and Candida parapsilosis from a multicontaminated soil alleviate metal toxicity in plants. Microbial Ecol 59:668–677
3. Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292
4. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay aprlicable to acrylamide gels. Anal Biochem 287:276–287
5. Bradford 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
6. Bulbovas P, Souza SR, Esposito JBN, Moraes RM, Alves ES, Domingos M, Azevedo RA (2014) Assessment of the ozone tolerance of two soybean cultivars (Glycine max cv. Sambaíba and Tracajá) cultivated in Amazonian areas. Environ Sci Pollut Res 21:10514–10524
7. Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668
8. Cabiscol E, Tamarit J, Ros J (2010) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8
9. Chaga G, Widersten M, Andersson L, Porath J, Danielson UH, Mannervik B (1994) Engineering of a metal coordinating site into human glutathione transferase M1-1 based on immobilized metal ion affinity chromatography of homologous rat enzymes. Protein Eng Des Sel 7:1115–1119
10. Cheng Z, Wei YYC, Sung WWL, Glick BR, McConkey BJ (2009) Proteomic analysis of the response of the plant growth-promoting bacterium Pseudomonas putida UW4 to nickel stress. Proteome Sci 7:18
11. Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940
12. Dorogházi OT, Kastori RR, Maksimović IV (2010) Nickel translocation from seed during germination and growth of young maize plants. Matica Srpska J Nat Sci 119:17–25
13. Dourado MN, Martins PF, Quecine MC, Piotto FA, Souza LA, Franco MR, Tezotto T, Azevedo RA (2013) Burkholderia sp. SCMS54 reduces cadmium toxicity and promotes growth in tomato. Ann Appl Biol 163:494–507
14. Dourado MN, Souza LA, Martins PF, Peters LP, Piotto FA, Azevedo RA (2014) Burkholderia sp. SCMS54 triggers a global stress defense in tomato enhancing cadmium tolerance. Water Air Soil Poll 225:2159
15. Dunn KLRD, Farrant JL, Langford PR, Kroll JS (2003) Bacterial [Cu, Zn]-cofactored superoxide dismutase protects opsonized, encapsulated Neisseria meningitides from phagocytosis by human monocytes/macrophages. Infect Immunol 71:1604–1607
16. Dworkin M, Foster JW (1958) Experiments with some microorganisms wich utilize ethane and hydrogen. J Bacteriol 75:592–603
17. Eerd LV, Hoagland R, Zablotowicz R, Hall J (2003) Pesticide metabolism in plants and microorganisms. Weed Sci 51:472–495
18. Esposito JBN, Esposito BP, Azevedo RA, Cruz LS, Silva LC, Souza SR (2015) Protective effect of Mn(III)–desferrioxamine B upon oxidative stress caused by ozone and acid rain in the Brazilian soybean cultivar Glycine max “Sambaiba”. Environ Sci Pollut Res 22:5315–5324
19. Farr SB, Kogoma T (1991) Oxidative Stress Responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev 55:561–585
20. Ferraz P, Fidalgo F, Almeida A, Teixeira J (2012) Phytostabilization of nickel by the zinc and cadmium hyperaccumulator Solanum nigrum L. Are metallothioneins involved? Plant Physiol Biochem 57:254–260
21. Geslin C, Llanos J, Prieur D, Jeanthon C (2001) The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol 152:901–905
22. Ghelfi A, Gaziola SA, Cia MC, Chabregas SM, Falco MC, Kuser-Falcão PR, Azevedo RA (2011) Cloning, expression, molecular modelling and docking analysis of glutathione transferase from Saccharum officinarum. Ann Appl Biol 159:267–280
23. Giannopolitis CN, Ries SK (1977) Superoxide dismutases II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318
24. Gomes-Junior RA, Moldes CA, Delite FS, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006) Nickel elicits a fast antioxidant response in Coffea arabica cells. Plant Physiol Biochem 44:420–429
25. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494
26. Gratão PL, Pompeu GB, Capaldi FR, Vitorello VA, Lea PJ, Azevedo RA (2008) Antioxidant response of Nicotiana tabacum cv. Bright Yellow 2 cells to cadmium and nickel stress. Plant Cell Tiss Organ Cult 94:73–83
27. Gratão PL, Monteiro CC, Carvalho RF, Tezotto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissection of diageotropica and never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96
28. Guelfi A, Azevedo RA, Lea PJ, Molina SMG (2003) Growth innhibition of the filamentous fungus Aspergillus nidulans by cadmium: and antioxidant enzyme approach. J Gen Appl Microbiol 49:63–73
29. Gupta A, Kumar M, Goel R (2004) Bioaccumulation properties of nickel-, cadmium-, and chromium-resistant mutants of Pseudomonas aeruginosa NBRI 4014 at alkaline pH. Biol Trace Elem Res 99:269–277
30. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
31. Han Y-H, Seo HA, Kim GH, Lee CK, Kang YK, Ryu KH, Chung YJ (2010) A histidine substitution confers metal binding affinity to a Schistosoma japonicum glutathione S-transferase. Protein Expres Purif 73:74–77
32. Hassan W, Bano R, Bashir F, David J (2014) Comparative effectiveness of ACC-deaminase and/or nitrogen-fixing rhizobacteria in promotion of maize (Zea mays L.) growth under lead pollution. Environ Sci Pollut Res 21:10983–10996
33. Harrison JJ, Tremaroli V, Stan MA, Chan CS, Vacchi-Suzzi C, Heyne BJ, Parsek MR, Ceri H, Turner RJ (2009) Chromosomal antioxidant genes have metal ion-specific roles as determinants of bacterial metal tolerance. Environ Microbiol 11:2491–2509
34. Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677
35. Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175
36. Kanazawa S, Mori K (1996) Isolation of cadmium-resistant bacteria and their resistance mechanisms. Soil Sci Plant Nutr 42:725–730
37. Keith KE, Valvano MA (2007) Characterization of SodC, a periplasmic superoxide dismutase from Burkholderia cenocepacia. Infect Immun 75:2451–2460
38. Kraus TE, Mckersie BD, Fletcher RA (1995) Paclobutrazol-induced tolerance of wheat leaves to paraquat may involve increased antioxidant enzyme activity. J Plant Physiol 145:570–576
39. Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
40. Lloyd JR, Lovley DR (2001) Microbial detoxification of metals and radionuclides. Curr Opin Biotechnol 12:248–253
41. Luvizotto DM, Marcon J, Andreote FD, Dini-Andreote F, Neves AAC, Araújo WL, Pizzirani-Kleiner AA (2010) Genetic diversity and plant-growth related features of Burkholderia spp. from sugarcane roots. World J Microbiol Biotechnol 26:1829–1836
42. Ma X-X, Jiang Y-L, He Y-X, Bao R, Chen Y, Zhou C-Z (2009) Structures of yeast glutathione-S-transferase Gtt2 reveal a new catalytic type of GST family. EMBO Rep 10:1320–1326
43. Ma Y, Rajkumar M, Vicente JAF, Freitas H (2011) Inoculation of Ni-resistant plant growth promoting bacterium Psychrobacter sp. strain srs8 for the improvement of nickel phytoextraction by energy crops. Int J Phytoremediation 13:126–139
44. Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L). Chemosphere 69:220–228
45. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: Costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13
46. Maksimović I, Kastori R, Krstić L, Luković J (2007) Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol Plant 51:589–592
47. Martins PF, Carvalho G, Gratão PL, Dourado MN, Pileggi M, Araújo WL, Azevedo RA (2011) Effects of the herbicides acetochlor and metolachlor on antioxidant enzymes in soil bacteria. Process Biochem 46:1186–1195
48. Masip L, Veeravalli K, Georgiou G (2006) The many faces of glutathione in bacteria. Antioxid Redox Signal 8:753–762
49. Nogueirol RC, Monteiro FA, Gratão PL, Borgo L, Azevedo RA (2015) Tropical soils with high aluminum concentrations cause oxidative stress in two tomato genotypes. Environ Monit Assess 187:73
50. Olchanheski LR, Dourado MN, Beltrame FL, Zielinski AAF, Demiate IM, Pileggi SAV, Azevedo RA, Sadowsky MJ, Pileggi M (2014) Mechanisms of tolerance and high degradation capacity of the herbicide mesotrione by Escherichia coli Strain DH5-a. PloS One 9:e99960
51. Pacheco CC, Passos JF, Castro AR, Moradas-Ferreira P, De Marco P (2008) Role of respiration and glutathione in cadmium-induced oxidative stress in Escherichia coli K-12. Arch Microbiol 189:271–278
52. Payne GW, Ramette A, Rose HL, Weightman AJ, Jones TH, Tiedje JM, Mahenthiralingam E (2006) Application of a recA gene-based identification approach to the maize rhizosphere reveals novel diversity in Burkholderia species. FEMS Microbiol Lett 259:126–132
53. Peters LP, Carvalho G, Martins PF, Dourado MN, Vilhena MB, Pileggi M, Azevedo RA (2014) Differential responses of the antioxidant system of ametryn and clomazone tolerant bacteria. Plos One 9:e112271
54. Pilon-Smits E, Ebskamp M, Paul MJ, Jeuken M, Weisbeek PJ, Smeekens S (1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol 107:125–130
55. Rehman A, Anjum MS (2011) Multiple metal tolerance and biosorption of cadmium by Candida tropicalis isolated from industrial effluents: glutathione as detoxifying agent. Environ Monit Assess 174:585–595
56. Ritz D, Beckwith J (2001) Roles of thiol - redox pathways in Bacteria. Annu Rev Microbiol 55:21–48
57. Sangali S, Brandelli A (2000) Feather keratin hydrolysis by a Vibrio sp. strain kr2. J Appl Microbiol 89:735–743
58. Sharma S, Singh B, Manchanda VK (2014) Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environ Sci Pollut Res 22:946–962
59. Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346
60. Skopelitou K, Dhavala P, Papageorgiou AC, Labrou NE (2012) A glutathione transferase from Agrobacterium tumefaciens reveals a novel class of bacterial GST superfamily. PloS One 7:e34263
61. Smirnova GV, Oktyabrsky ON (2005) Glutathione in bacteria. Biochemistry 70:1199–1211
62. Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5’-dithiobis(2-nitrobenzoic acid). Anal Biochem 175:408–413
63. Tezotto T, Favarin JL, Azevedo RA, Alleoni LRF, Mazzafera P (2012) Coffee is highly tolerant to cadmium, nickel and zinc: plant and soil nutritional status, metal distribution and bean yield. Field Crops Res 125:25–34
64. Tuggle C, Fuchs J (1985) Glutathione reductase is not required for maintenance of reduced glutathione in Escherichia coli K-12. J Bacteriol 162:448–450
65. Ullah A, Mushtaq H, Ali H, Munis MFH, Javed MT, Chaudhary HJ (2014) Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res 22:2505–2514
66. Vuilleumier M, Pagni S (2002) The elusive roles of bacterial glutathione S- transferases: new lessons from genomes. Appl Microbiol Biotechnol 58:138–146
67. Weyens N, Truyens S, Saenen E, Boulet J, Dupae J, Taghavi S, Van der Lelie D, Carleer R, Vangronsveld J (2011) Endophytes and their potential to deal with co-contamination of organic contaminants (toluene) and toxic metals (nickel) during phytoremediation. Int J Phytoremediation 13:244–255
68. Woodbury W, Spencer A, Stahman M (1971) Improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 547:301–305
69. Xia J-L, Wu S, Zhang R, Zhang C, He H, Jiang H, Nie Z, Qiu G (2011) Effects of copper exposure on expression of glutathione-related genes in Acidithiobacillus ferrooxidans. Curr Microbiol 62:1460–1466
70. Yilmaz S, Widersten M, Emahazion T, Mannervik B (1995) Generation of a Ni(II) binding site by introduction of a histidine cluster in the structure of human glutathione transferase A1-1. Protein Eng Des Sel 8:1163–1169