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The Influence of Glutathione on the Tolerance of Rhizobium leguminosarum to Cadmium

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Toxicity of Heavy Metals to Legumes and Bioremediation

Abstract

Rhizobia play an important role in agriculture and crop production as they induce nitrogen-fixing nodules on the roots of leguminous plants. Due to the injudicious use of fertilizers and industrial and domestic sludges, the heavy-metal contamination of soils is becoming one of the most concerning environmental problems, which negatively affects the soil microbial communities and consequently the crop productivity. Among the nonessential metals, cadmium (Cd) poses a major threat due to its high mobility and bioavailability. Cadmium affects the survival and the ability of rhizobia to form nitrogen-fixing nodules. The identification of mechanisms that improve rhizobial tolerance to Cd, its persistence in soil, and its ability to improve nodulation efficiency of rhizobia in Cd-contaminated soils is an important issue that requires urgent attention for maintaining fertility of soils polluted with metals. Here we discuss the influence of glutathione (GSH) on Cd tolerance of Rhizobium leguminosarum and have tried to establish the chronology of Cd tolerance mechanism. To understand this, several strains were screened for their Cd tolerance, and the effect of bacterial pregrowth in the presence of extracellular GSH was determined. Cadmium and GSH levels were also monitored over 72 h. The importance of GSH in Cd tolerance was confirmed by the intracellular levels of this tripeptide: GSH intracellular levels remained unaffected in the sensitive strain, yet it increased significantly in the tolerant strain. Moreover, GSH synthesis was induced by intracellular Cd levels; the addition of extracellular GSH had a protective effect toward Cd, particularly in the sensitive strains. These results lead to a better understanding of the metal tolerance mechanisms in free-living bacteria and are likely to improve the Rhizobium-plant symbiosis in heavy-metal-contaminated soils.

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References

  • Abbas SM, Kamel EA (2004) Rhizobium as a biological agent for preventing heavy metal stress. Asian J Plant Sci 3:416–424

    Article  Google Scholar 

  • Abd-Alla HM, Yan F, Schubert S (1999) Effects of sewage sludge application on nodulation, nitrogen fixation, and plant growth of faba bean, soybean and lupin. J Appl Bot 73:69–75

    CAS  Google Scholar 

  • Alloway BJ (1995a) Introduction. In: Alloway BJ (ed) Heavy metals in soils. Blackie Academic & Professional, New York, NY, pp 3–9

    Chapter  Google Scholar 

  • Alloway BJ (1995b) Cadmium. In: Alloway BJ (ed) Heavy metals in soils. Blackie Academic & Professional, New York, NY, pp 122–147

    Chapter  Google Scholar 

  • Alloway BJ, Steinnes E (1999) Anthropogenic addictions of cadmium to soils. In: McLaughlin ML, Singh BR (eds) Cadmium in soils and plants. Kluwer, Dordrecht, pp 97–118

    Chapter  Google Scholar 

  • Atlas RM, Bartha R (1997) Microbial ecology – fundamentals and applications. Benjamin/Cummings, Menlo Park, CA

    Google Scholar 

  • Balestrasse KB, Gardey L, Gallego SM, Tomaro ML (2001) Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Aust J Plant Physiol 28:497–504

    CAS  Google Scholar 

  • Blake RC, Choate DM, Bardhan S, Revis N, Barton LL, Zocco TG (1993) Chemical transformation of toxic metals by a Pseudomonas strain from a toxic waste site. Environ Toxicol Chem 12:1365–1376

    CAS  Google Scholar 

  • Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, López R, Chamber MA, Palomares AJ (2005) Isolation and characterization of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcóllar pyrite mine. Soil Biol Biochem 37:1131–1140

    Article  CAS  Google Scholar 

  • Cervantes C, Gutierrez-Corona F (1994) Cooper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137

    Article  PubMed  CAS  Google Scholar 

  • Chander K, Brookes PC (1993) Residual effects of zinc, copper and nickel in sewage sludge on microbial biomass in a sandy loam. Soil Biol Biochem 25:1231–1239

    Article  CAS  Google Scholar 

  • Chaudri AM, McGrath SP, Giller KE, Rietz E, Sauerbeck D (1993) Enumeration of indigenous Rhizobium leguminosarum biovar trifolii in soils previously treated with metal-contaminated sewage sludge. Soil Biol Biochem 25:301–309

    Article  CAS  Google Scholar 

  • Chesney JA, Eaton JW, Mahoney JR (1996) Bacterial glutathione: a sacrificial defence against chlorine compounds. J Bacteriol 178:2131–2135

    PubMed  CAS  Google Scholar 

  • Corticeiro SC, Lima AIG, Figueira EMAP (2006) The importance of glutathione in oxidative status of Rhizobium leguminosarum biovar viciae under Cd exposure. Enzyme Microb Technol 40:132–137

    Article  CAS  Google Scholar 

  • Ferguson GP, Booth IR (1998) Importance of glutathione for growth and survival of Escherichia coli cells: detoxification of methylglyoxal and maintenance of intracellular K+. J Bacteriol 180:4314–4318

    PubMed  CAS  Google Scholar 

  • Figueira EMAP (2000) Aspectos da tolerância salina em Pisum sativum: influência da nutrição azotada. PhD thesis, Biology Department, University of Aveiro, Portugal

    Google Scholar 

  • Figueira EMAP, Lima AIG, Pereira SAI (2005) Cadmium tolerance plasticity in Rhizobium leguminosarum bv. viciae: glutathione as a detoxifying agent. Can J Microbiol 51:1–6

    Article  Google Scholar 

  • Fink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci USA 96:1175–1180

    Article  Google Scholar 

  • Giller KE, McGrath SP, Hirsch PR (1989) Absence of nitrogen fixation in clover grown on soil subject to long-term contamination with heavy metals is due to survival of only ineffective Rhizobium. Soil Biol Biochem 21:841–848

    Article  CAS  Google Scholar 

  • Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    Article  CAS  Google Scholar 

  • Goldberg M, Pribyl T, Juhnke S, Nies DH (1999) Energetics and topology of a CzcA, a cation/proton antiporter of the resistance – nodulation – cell division protein family. J Biol Chem 274:26065–26070

    Article  PubMed  CAS  Google Scholar 

  • Grass G, Große C, Nies DH (2000) Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34. J Bacteriol 182:1390–1398

    Article  PubMed  CAS  Google Scholar 

  • Harrison J, Jamet A, Muglia CI, Van de Sype G, Aguilar OM, Puppo A, Frendo P (2005) Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti. J Bacteriol 187:168–174

    Article  PubMed  CAS  Google Scholar 

  • He ZL, Xu HP, Zhu YM, Yang XE, Chen GC (2005) Adsorption-desorption characteristics of cadmium in variable charge soils. J Environ Sci Health A Tox Hazard Subst Environ Eng 40:805–822

    Article  PubMed  CAS  Google Scholar 

  • Hirsch PR, Jones MJ, McGrath SP, Giller KE (1993) Heavy metals from past applications of sewage sludge decrease the genetic diversity of Rhizobium leguminosarum biovar trifolii populations. Soil Biol Biochem 25:1485–1490

    Article  Google Scholar 

  • Horswell J, Speir TW, van Schaik PA (2003) Bio-indicators to assess impacts of heavy metals in land-applied sewage sludge. Soil Biol Biochem 35:1501–1505

    Article  CAS  Google Scholar 

  • Ibekwe AM, Angle JS, Chaney RL, van Berkum P (1995) Sewage sludge and heavy metal effects on nodulation and nitrogen fixation legumes. J Environ Qual 24:1199–1204

    Article  CAS  Google Scholar 

  • Kang YJ (1992) Exogenous glutathione decreases cellular cadmium uptake and toxicity. Drug Metabol Dispos 20:714–718

    CAS  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19

    Article  Google Scholar 

  • Lima AIG, Corticeiro SC, Figueira EMAP (2006a) Glutathione-mediated cadmium sequestration in Rhizobium leguminosarum. Enzyme Microb Technol 39:763–769

    Article  CAS  Google Scholar 

  • Lima AIG, Pereira SAI, Figueira EMAP, Caldeira GCN, Caldeira HDQM (2006b) Cadmium detoxification in roots of Pisum sativum seedlings: relationship between toxicity levels, thiol pool alterations and growth. Environ Exp Bot 55:149–162

    Article  CAS  Google Scholar 

  • McGrath SP, Lane PW (1989) An explanation for the apparent losses of metals in a long-term field experiment with sewage sludge. Environ Pollut 60:235–256

    Article  PubMed  CAS  Google Scholar 

  • McGrath SP, Chaudri AM, Giller KE (1995) Long-term effects of metals in sewage sludge on soils, microorganisms and plants. J Ind Microbiol 14:94–104

    Article  PubMed  CAS  Google Scholar 

  • Meister A (1995) Glutathione metabolism. Methods Enzymol 251:3–13

    Article  PubMed  CAS  Google Scholar 

  • Muglia CI, Grasso DH, Aguilar OM (2007) Rhizobium tropici response to acidity involves activation of glutathione synthesis. Microbiology 153:1286–1296

    Article  PubMed  CAS  Google Scholar 

  • Munson GP, Lam DL, Outten FW, O’Halloran TO (2000) Identification of copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182:5864–5871

    Article  PubMed  CAS  Google Scholar 

  • Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytol 181:532–552

    Article  PubMed  CAS  Google Scholar 

  • Nies DH, Koch S, Wachi S, Peitzsch N, Saier MH (1998) CHR of prokaryotic proton motive force-driven transporters probably contains chromate/sulphate antiporters. J Bacteriol 180:5799–5802

    PubMed  CAS  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Obbard JP (2001) Ecotoxicological assessment of heavy metals in sewage sludge amended soils. Appl Geochem 16:1405–1411

    Article  CAS  Google Scholar 

  • Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2009) Cadmium levels in Europe: implications for human health. Environ Geochem Health 32:1–12

    Article  PubMed  CAS  Google Scholar 

  • Pazirandeh M, Mauro JM (2000) Production and cellular localization of functional oligomeric peptides in E. coli: expression of the N. crassa polymetallothionein. Colloids Surf A 177:197–202

    Article  Google Scholar 

  • Pazirandeh M, Wells BM, Ryan RL (1998) Development of bacterium-based heavy metal biosorbents: enhanced uptake of cadmium and mercury by Escherichia coli expressing a metal binding motif. Appl Environ Microbiol 64:4068–4072

    PubMed  CAS  Google Scholar 

  • Peitzsch N, Eberz G, Nies DH (1998) Alcaligenes eutrophus as a bacterial chromate sensor. Appl Environ Microbiol 64:453–458

    PubMed  CAS  Google Scholar 

  • Pereira SIA, Lima AIG, Figueira EMAP (2006) Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv. viciae isolated from contaminated Portuguese soils. Microb Ecol 52:176–186

    Article  PubMed  CAS  Google Scholar 

  • Purchase D, Miles RJ (2001) Survival and nodulating ability of indigenous and inoculated Rhizobium leguminosarum biovar trifolii in sterilized and unsterilized soil treated with sewage sludge. Curr Microbiol 42:59–64

    Article  PubMed  CAS  Google Scholar 

  • Purchase D, Miles RJ, Young TWK (1997) Cadmium uptake and nitrogen fixing ability in heavy-metal-resistant laboratory and field strains of Rhizobium leguminosarum biovar trifolii. FEMS Microbiol Ecol 22:85–93

    Article  CAS  Google Scholar 

  • Rehman A, Nautiyal CS (2002) Effect of drought on the growth and survival of the stress-tolerant bacterium Rhizobium sp. NBRI2505 sesbania and its drought-sensitive transposon Tn5 mutant. Curr Microbiol 45:368–377

    Article  PubMed  CAS  Google Scholar 

  • Riccillo PM, Muglia CI, De Bruijn FJ, Roe AJ, Booth IR, Aguilar OM (2000) Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J Bacteriol 182:1748–1753

    Article  PubMed  CAS  Google Scholar 

  • Robinson B, Russell C, Hedley M, Clothier B (2001) Cadmium adsorption by rhizobacteria: implications for New Zealand pastureland. Agric Ecosyst Environ 87:315–321

    Article  CAS  Google Scholar 

  • Saltikov CW, Olson BH (2002) Homology of Escherichia coli R773 arsA, arsB, and arsC genes in arsenic-resistant bacteria isolated from raw sewage and arsenic-enriched creek waters. Appl Environ Microbiol 68:280–288

    Article  PubMed  CAS  Google Scholar 

  • Saxena PK, KrishnaRaj S, Dan T, Perras MR, Vettakkorumakankav NN (1999) Phytoremediation of metal contaminated and polluted soils. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants – from molecules to ecosystems. Springer, Berlin

    Google Scholar 

  • Silver S, Misra TK (1988) Plasmid-mediated heavy metal resistances. Annu Rev Microbiol 42:717–743

    Article  PubMed  CAS  Google Scholar 

  • Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789

    Article  PubMed  CAS  Google Scholar 

  • Somasegaran P, Hoben HJ (1994) Handbook for rhizobia. Springer, Berlin

    Book  Google Scholar 

  • Trajanovska S, Britz ML, Bhave M (1997) Detection of heavy metal ion resistance genes in Gram-positive and Gram-negative bacteria isolated from a lead-contaminated site. Biodegradation 8:113–124

    Article  PubMed  CAS  Google Scholar 

  • Wagner GJ (1993) Accumulation of cadmium in crop plants and it consequences to human health. Adv Agron 51:173–212

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007a) Cadmium, chromium and copper in greengram plants. Agron Sustain Dev 27:145–153

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007b) Impact of heavy metal toxicity on plant growth, symbiosis, seed yield and nitrogen and metal uptake in chickpea. Aust J Exp Agric 47:712–720

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007c) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70:36–45

    Article  PubMed  CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Centre for Cell Biology, Department of Biology, University of Aveiro, 3810-193, Aveiro, Portugal

    Corticeiro Sofia, Pereira Sofia, Lima Ana & Figueira Etelvina

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  1. Corticeiro Sofia
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  2. Pereira Sofia
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  3. Lima Ana
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  4. Figueira Etelvina
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Corresponding author

Correspondence to Figueira Etelvina .

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Editors and Affiliations

  1. Fac. Agricultural Sciences, Dept. Agricultural Microbiology, Aligarh Muslim University, Aligarh, 202002, India

    Almas Zaidi

  2. , Department of Biological Sciences, Crescent University, College of Natural, Abeokuta, Ogun, Nigeria

    Parvaze Ahmad Wani

  3. Fac. Agricultural Sciences, Dept. Agricultural Microbiology, Aligarh Muslim University, Aligarh, 202002, India

    Mohammad Saghir Khan

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Sofia, C., Sofia, P., Ana, L., Etelvina, F. (2012). The Influence of Glutathione on the Tolerance of Rhizobium leguminosarum to Cadmium. In: Zaidi, A., Wani, P., Khan, M. (eds) Toxicity of Heavy Metals to Legumes and Bioremediation. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0730-0_5

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