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Rhizobium–Legume Symbiosis: A Model System for the Recovery of Metal-Contaminated Agricultural Land

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Toxicity of Heavy Metals to Legumes and Bioremediation

Abstract

Legumes are considered the appropriate crops for raising the productivity and recovery of marginal lands through symbiosis with nodule-forming bacteria collectively called rhizobia. Cultivated fields around the world including India are often irrigated by metal-contaminated groundwater and surface water. This practice poses a significant risk to both agroecosystems and human health via food chain. Therefore, metal removal from contaminated soils is urgently required. In this context, conventional technologies for metal removal have been employed, but they are expensive and disruptive. The use of biological materials including both plants (phytoremediation) and microbial communities in the remediation of polluted environments, on the contrary, has been found environment friendly and inexpensive. Leguminous plants have been found important in this regard due to their bioremediation potential and ability to provide essential nutrient nitrogen to plants in nitrogen deficient soils through symbiosis with rhizobia. The role of Rhizobium–legume symbiotic association in alleviating metal toxicity is reviewed and highlighted.

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References

  • Adriano DC (1986) Trace elements in the terrestrial environment. Springer, New York

    Google Scholar 

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

    CAS  Google Scholar 

  • Becker BU, Kosch K, Parniske M, Müller P (1998) Exopolysaccharide (EPS) synthesis in Bradyrhizobium japonicum: sequence, operon structure and mutational analysis of an exo gene cluster. Mol Gen Genet 259:161–171

    Article  PubMed  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 wastes site. Environ Toxicol Chem 12:1365–1376

    CAS  Google Scholar 

  • Bordeleau L, Prevost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125

    Article  CAS  Google Scholar 

  • Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180

    Article  CAS  Google Scholar 

  • Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, Lopez 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 Azanalcollar pyrite mine. Soil Biol Biochem 37:1131–1140

    Article  CAS  Google Scholar 

  • Chaterjee A, Das D, Mandal BK (1995) Arsenic in groundwater in six districts of west Bengal, India. The biggest arsenic calamity in the world. Prt 1. Arsenic species in drinking water and urine of affected people. Analyst 120:643–650

    Article  CAS  Google Scholar 

  • Chaudri A, McGrath S, Gibbs P, Chambers B, Carlton-Smith C, Bacon J, Campbell C, Aitken M (2008) Population size of indigenous Rhizobium leguminosarum biovar trifolii in long-term field experiments with sewage sludge cake, metal-amended liquid sludge or metal salts: effects of zinc, copper and cadmium. Soil Biol Biochem 40:1670–1680

    Article  CAS  Google Scholar 

  • Chen WX, Li GS, Qi YL, Wang ET, Yuan HL, Li JL (1991) Rhizobium huakuii sp. nov. isolated from the root nodules of Astragalus sinicus. Int J Syst Bacteriol 41:275–280

    Article  Google Scholar 

  • Chowdhury TR, Basu GK, Mandal BK, Biswas BK, Samanta G, Chowdhury UK, Chanda RK, Lodh D, Roy SL, Saha KC, Roy S, Kabir S, Quamruzzaman Q, Chakraborti D (1999) Arsenic poisoning in Ganges Delta. Nature 401:545–546

    PubMed  CAS  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  PubMed  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  PubMed  CAS  Google Scholar 

  • Cunningham SD, Huang JW, Chen J, Berti WR (1996) Phytoremediation of contaminated soils: progress and promise. Abstr Pap Am Chem Soc 212:87

    Google Scholar 

  • Das HK, Mitra AK, Sengupta PK, Hossain A, Islam F, Rabbani GH (2004) Arsenic concentration in rice, vegetables, and fish in Bangladesh: a preliminary study. Environ Int 30:383–387

    Article  PubMed  CAS  Google Scholar 

  • Downie A (1997) Fixing a symbiotic circle. Nature 387:352–353

    Article  PubMed  CAS  Google Scholar 

  • Franceseoni K, Visoottiviseth P, Sridokchan W, Goessler W (2002) Arsenic species in an arsenic hyperaccumulating fern Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci Total Environ 284:27–35

    Article  Google Scholar 

  • Freiberg C, Fellay R, Bairoch A, Broughton WJA (1997) Rosenthal and X. Perret, molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401

    Article  PubMed  CAS  Google Scholar 

  • Freire JRJ (1984) Important limiting factors in soil for the Rhizobium-legume symbiosis. In: Alexander M (ed) BNF ecology, technology and physiology. Plenum, New York, pp 51–74

    Google Scholar 

  • Fu J, Zhou Q, Liu J, Liu W, Wang T, Zhang Q, Jiang G (2008) High levels of heavy metals in rice (Oryza sativa L.) from a typical waste recycling area in southeast China and its potential risk to human health. Chemosphere 71:1269–1275

    Article  PubMed  CAS  Google Scholar 

  • Giller KE, Witter E, Mc Grath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils – a review. Soil Biol Biochem 25:273–278

    Article  Google Scholar 

  • Heckman JR, Angle JS, Chaney RL (1987) Residual effects of sewage sludge on soybean: II. Accumulation of soil and symbiotically fixed nitrogen. J Environ Qual 16:117–124

    Google Scholar 

  • Herawati N, Suzuki S, Hayashi K, Rivai IF, Koyama H (2000) Cadmium, copper, and zinc levels in rice and soil of Japan, Indonesia, and China by soil type. Bull Environ Contam Toxicol 64:33–39

    Article  PubMed  CAS  Google Scholar 

  • Hong SH, Gohya M, Ono H, Murakami H, Yamashita M, Hirayama N, Murooka Y (2000) Molecular design of novel metal binding oligomeric human metallo thioneins. Appl Microbiol Biotechnol 54:84–89

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with the MTL4 and the PCS genes. Chemosphere 66:1670–1676

    Article  PubMed  CAS  Google Scholar 

  • Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2008) Promotion of metal accumulation in nodule of Astragalus sinicus by the expression of the iron-regulated transporter gene in Mesorhizobium huakuii sub sp. rengi B3. J Biosci Bioeng 105:642–648

    Article  PubMed  CAS  Google Scholar 

  • Ji G, Silver S (1995) Bacterial resistance mechanisms for heavy metals of environmental concern. J Ind Microbiol 14:61–75

    Article  PubMed  CAS  Google Scholar 

  • Juste P, Chassin A, Gomez M, Linères B, Mocquot FI, Wiart J (1995) Les micro-polluants métalliques dans les boues résiduaires des stations d’épuration urbaines. ADEME, Angers and INRA, Bordeaux

    Google Scholar 

  • Keyser HH, Munns DN (1979) Tolerance of rhizobia to acidity, aluminium and phosphate. Soil Sci Soc Am J 43:519–523

    Article  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 

  • Kinkle BK, Angle JS, Keysere HH (1987) Long-term effects of metal sewage sludge application on soil population of Bradyrhizobium japonicum. Appl Environ Microbiol 53:315–319

    PubMed  CAS  Google Scholar 

  • Klaassen CD, Watkins JB (2003) Casarett and Doull’s essentials of toxicology. McGraw-Hill, New York, NY

    Google Scholar 

  • Kotrba P, Macek T, Ruml T (1999) Heavy metal-binding peptides and proteins in plants – a review. Collect Czech Chem Commun 64:1057–1086

    Article  CAS  Google Scholar 

  • Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, Kawaguchi M (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51:1381–1397

    Article  PubMed  CAS  Google Scholar 

  • Lima AIG, Pereira SIA, de Almeida Paula Figueira EM, Caldeira GCN, de Matos Caldeira HDQ (2006) 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 

  • Liu XM, Wu JJ, Xu JM (2006) Characterizing the risk assessment of heavy metals and sampling uncertainty analysis in paddy field by geostatistics and GIS. Environ Pollut 141:257–264

    Article  PubMed  CAS  Google Scholar 

  • Ma LQ, Kumar KM, Tu C, Zhang W, Cai Y, Kennelly ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579

    Article  PubMed  CAS  Google Scholar 

  • Mandal BK, Chowdhury TR, Samanta G, Basu GK, Chowdhury PP, Chanda CR, Lodh D, Karan NK, Dhar RK, Tamili DK, Das D, Saha KC, Chakraborti D (1996) Arsenic in groundwater in seven districts in West Bengal, India – the biggest calamity in the World. Curr Sci 70:976–986

    CAS  Google Scholar 

  • Mandal SM, Dey S, Ray B, Pati BR (2007) Production and composition of extracellular polysaccharide synthesized by a Rhizobium isolate of Vigna mungo (L.) Hepper. Biotechnol Lett 29:1271–1275

    Article  PubMed  CAS  Google Scholar 

  • Mandal SM, Pati BR, Das AK, Ghosh AK (2008) Characterization of a symbiotically effective Rhizobium resistant to arsenic: isolated from the root nodules of Vigna mungo (L.) Hepper grown in an arsenic-contaminated field. J Gen Appl Microbiol 54:93–99

    Article  PubMed  CAS  Google Scholar 

  • Mandimba GR (1995) Contribution of nodulated legumes on the growth of Zea mays L. under various cropping systems. Symbiosis 19:213–222

    Google Scholar 

  • McGrath SP (1994) Effects of heavy metals from sewage sludge on soil microbes in agricultural ecosystems. In: Ross SM (ed) Toxic metals in soil-plant systems. Wiley, Chichester, pp 242–274

    Google Scholar 

  • Meinhardt LW, Krishnan HB, Balatti PA, Pueppke SG (1993) Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257. Mol Microbiol 9:17–29

    Article  PubMed  CAS  Google Scholar 

  • Moftah JM (2000) Physiological response of lead polluted tomato and egg plant to the antioxidant ethylene diurea. Menufiya Agric Res 25:933–955

    Google Scholar 

  • Murooka Y, Xu Y, Sanada H, Araki M, Morinaga T, Yokota A (1993) Formation of root nodules by Rhizobium huakuii biovar rengei bv. nov. on Astragalus sinicus cv, Japan. J Ferment Bioeng 76:38–44

    Article  CAS  Google Scholar 

  • Nies DH (1992) Resistance to cadmium, cobalt, zinc and nickel in microbes. Plasmid 27:17–28

    Article  PubMed  CAS  Google Scholar 

  • Niu S, Cao S, Shen E (1995) The status of arsenic poisoning in China. In: SEGH second international conference on arsenic exposure and health effects, San Diego, CA

    Google Scholar 

  • Nuswantara S, Fujie M, Yamada T, Malek W, Inaba M, Kaneko Y, Murooka Y (1999) Phylogenic position of Mesorhizobium huakuii subsp. rengei, a symbiont of Astragalus sinicus cv, Japan. J Biosci Bioeng 87:49–55

    Article  PubMed  CAS  Google Scholar 

  • Obbard JP, Sauerbeck D, Jones KC (1994) Dehydrogenase activity of the microbial biomass in soils from a field experiment amended with heavy metal contaminated sewage sludges. Sci Total Environ 142:157–162

    Article  PubMed  CAS  Google Scholar 

  • Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944

    Article  PubMed  CAS  Google Scholar 

  • Ow DW (1993) Phytochelatin-mediated cadmium tolerance in Schizosaccharomyces pombe. In Vitro Cell Dev Biol 29:213–219

    Google Scholar 

  • Paudyal SP, Aryal RR, Chauhan SVS, Maheshwari DK (2007) Effect of heavy metals on growth of Rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World 5:27–32

    Google Scholar 

  • Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production. Plant Soil 174:3–28

    Article  CAS  Google Scholar 

  • Pereira SIA, Lima AIG, de Almeida EM, Figueira P (2006a) Heavy metal toxicity in Rhizobium leguminosarum biovar viciae isolated from soils subjected to different sources of heavy metal contamination: effects on protein expression. Appl Soil Ecol 33:286–293

    Article  Google Scholar 

  • Pereira SIA, Lima AIG, Figueira EMAP (2006b) 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 

  • Perret X, Freiberg C, Rosenthal A, Broughton WJ, Fellay R (1999) High-resolution transcriptional of analysis the symbiotic plasmid of Rhizobium sp. NGR234. Mol Microbiol 32:415–425

    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 

  • Raina S, Missiakas D (1997) Making and breaking disulfide bonds. Annu Rev Microbiol 51:179–202

    Article  PubMed  CAS  Google Scholar 

  • Raskin I, Kumar PBAN, Dushenkov S, Salt D (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5:285–290

    Article  CAS  Google Scholar 

  • Reeve WG, Tiwari RP, Wong CM, Dilworth MJ, Glenn AR (1998) The transcriptional regulator gene phrR in Sinorhizobium meliloti WSM419 is regulated by low pH and other stresses. Microbiology 144:3335–3342

    Article  PubMed  CAS  Google Scholar 

  • Reeve WG, Tiwari RP, Kale NB, Dilworth MJ, Glenn AR (2002) ActP controls copper homeostasis in Rhizobium leguminosarum bv. viciae and Sinorhizobium meliloti preventing low pH-induced copper toxicity. Mol Microbiol 43:981–991

    Article  PubMed  CAS  Google Scholar 

  • Ruvkun GB, Sundaresan V, Ausubel FM (1982) Directed transposon Tn5 mutagenesis and complementation analysis of Rhizobium meliloti symbiotic nitrogen fixation genes. Cell 29:551–559

    Article  PubMed  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  PubMed  CAS  Google Scholar 

  • Sá-Pereira P, Rodrigues M, Videira e Castro I, Simões F (2007) Identification of an arsenic resistance mechanism in rhizobial strains. World J Microbiol Biotechnol 23:1351–1356

    Article  Google Scholar 

  • Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195

    Article  PubMed  CAS  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  PubMed  CAS  Google Scholar 

  • Sellstedt A, Staahl L, Mattsson M, Jonsson K, Hoegberg P (1993) Can the 15N dilution technique be used to study N2 fixation in tropical tree symbioses as affected by water deficit? J Exp Bot 44:1749–1755

    Article  Google Scholar 

  • Silver S, Walderhaug M (1992) Gene regulation of plasmid- and chromosomal-determined inorganic ion transport in bacteria. Microbiol Rev 56:195–228

    PubMed  CAS  Google Scholar 

  • Singh S, Kayastha AM, Asthana RK, Srivastava PK, Singh SP (2001) Response of Rhizobium leguminosarum to nickel stress. World J Microbiol Biotechnol 17:667–672

    Article  CAS  Google Scholar 

  • Sinha S, Gupta AK, Bhatt K, Pandey K, Rai UN, Singh KP (2006) Distribution of metals in the edible plants grown at Jajman, Kanpur (Indian) receiving treated tannery wastewater: relation with physico-chemical properties of the soil. Environ Monit Assess 115:1–22

    Article  PubMed  CAS  Google Scholar 

  • Sprent JI (1997) Coevolution of legume-rhizobial symbioses: is it essential for either partner? In: Legocki A, Bothe H, Puhler A (eds) Biological fixation of nitrogen for ecology and sustainable agriculture. NATO ASI series. G. Ecological sciences, vol 39. Springer, Berlin, pp 313–316

    Google Scholar 

  • Sprent JI, Sutherland J, de Faria SM (1987) Some aspects of the biology of nitrogen fixing organisms. Philos Trans R Soc Lond B317:111–119

    Article  Google Scholar 

  • Sriprang R, Hayashi M, Yamashita M, Ono H, Saeki K, Murooka Y (2002) A novel bioremediation system for heavy metals using the symbiosis between leguminous plant and genetically engineered rhizobia. J Biotechnol 99:279–293

    Article  PubMed  CAS  Google Scholar 

  • Sriprang R, Hayashi M, Ono H, Takagai M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791–1796

    Article  PubMed  Google Scholar 

  • Stan V, Gament E, Cornea CP, Voaideş C, Duşa M, Plopeanu G (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Hort Agrobot Cluj 39:88–95

    Google Scholar 

  • Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation). Wiley, New York, NY, pp 307–333

    Google Scholar 

  • Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR (1996a) An essential role for actA in acid tolerance of Rhizobium meliloti. Microbiology 142:601–610

    Article  PubMed  CAS  Google Scholar 

  • Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR (1996b) Acid tolerance in Rhizobium meliloti strain WSM419 involves a two component sensor regulator system. Microbiology 142:1693–1704

    Article  PubMed  CAS  Google Scholar 

  • Vašák M (2005) Advances in metallothionein structure and functions. J Trace Elem Med Biol 19:13–17

    Article  PubMed  Google Scholar 

  • Wang C, Shen Z, Li X, Luo C, Chen Y, Yang H (2004) Heavy metal contamination of agricultural soils and stream sediments near a copper mine in Tongling, People’s Republic of China. Bull Environ Contam Toxicol 73:862–869

    Article  PubMed  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) 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 (2008a) Impact of zinc-tolerant plant growth promoting rhizobacteria on lentil grown in zinc-amended soil. Agron Sustain Dev 28:449–455

    Article  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008b) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163

    Article  PubMed  CAS  Google Scholar 

  • Williams PN, Lei M et al (2009) Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice-Hunan, China. Environ Sci Technol 43:637–642

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Cheng J, Finan TM, Rosen BP, Bhattacharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187:6691–6697

    Article  Google Scholar 

  • Yates RJ, Howieson JG, Reeve WG, Brau L, Speijers J, Nandasena K, Real D, Sezmis E, O’Hara GW (2008) Host-strain mediated selection for an effective nitrogen-fixing symbiosis between Trifolium spp. and Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 40:822–833

    Article  CAS  Google Scholar 

  • Younis M (2007) Response of Lablab purpurens-Rhizobium symbiosis to heavy metals in pot and field experiment. World J Agric Sci 3:111–122

    Google Scholar 

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Mandal, S.M., Bhattacharyya, R. (2012). Rhizobium–Legume Symbiosis: A Model System for the Recovery of Metal-Contaminated Agricultural Land. 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_7

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