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Rhizobacteria isolated from a metal-polluted area enhance plant growth in zinc and cadmium-contaminated soil

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Abstract

In this work, we evaluated the ability of rhizobacteria isolated from a metal-contaminated site to produce plant growth-promoting substances, such as indole-3-acetic acid (IAA), ammonia, hydrogen cyanide, siderophores and extracellular enzymes, to solubilize phosphate and for 1-aminocyclopropane-1-carboxylate (ACC)-deaminase activity, while assessing their capacity to enhance Trifolium repens growth. The rhizobacteria that better performed were used as bioinoculants for plants grown in zinc- and cadmium-spiked soils. Rhizobacteria were inoculated onto white clover seedlings growing in 250 and 500 mg kg−1 of zinc and in 10 and 30 mg kg−1 of cadmium-spiked soils and plant traits determined. The available and exchangeable rhizosphere metal concentrations were analyzed. Twenty rhizobacteria stimulated white clover growth under axenic conditions. Overall, strains Rhodococcus erythropolis EC 34, Achromobacter sp. 1AP2 and Microbacterium sp. 3ZP2 increased clover biomass in the absence and in presence of metals; however, in soils with 250 mg kg−1 of zinc, bacterial inoculation did not enhance plant biomass. Biomass enhancement may be related to the multiple bacterial promoting traits, especially the production of high levels of IAA and siderophores and the activity of ACC-deaminase. To the best of our knowledge, this is the first study reporting the potential of R. erythropolis to increase plant growth in metal-contaminated soils. In general, strains Microbacterium sp. 3ZP2 and Arthrobacter sp. EC 10 enhanced the available and exchangeable metal concentrations in rhizosphere showing their potential to improve phytoremediation efficiency. This work clearly indicates that rhizobacteria are promising for the development of bioinoculants useful for phytoremediation of polluted soils.

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References

  • Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224

    Article  CAS  Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    Article  CAS  Google Scholar 

  • Aina R, Palin L, Citterio S (2006) Molecular evidence for benzo[a]pyrene and naphthalene genotoxicity in Trifolium repens L. Chemosphere 65:666–673

    Article  CAS  Google Scholar 

  • Andreazza R, Okeke BC, Lambais MR, Bortolon L, de Melo GWB, de Oliveira CFA (2010) Bacterial stimulation of copper phytoaccumulation by bioaugmentation with rhizosphere bacteria. Chemosphere 81:1149–1154

    Article  CAS  Google Scholar 

  • Barrutia O, Garbisu C, Hernandez-Allica J, Garcıa-Plazaola JI, Becerril JM (2010) Differences in EDTA-assisted metal phytoextraction between metallicolous and non-metallicolous accessions of Rumex acetosa L. Environ Pollut 158:1710–1715

    Article  CAS  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y (1997) Enhanced accumulation of Pb in Indian mustard by soil applied chelating agents. Environ Sci Technol 31:860–865

    Article  Google Scholar 

  • Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58

    Article  CAS  Google Scholar 

  • Broos K, Uyttebroek M, Mertens J, Smolders E (2004) A survey of symbiotic nitrogen fixation by white clover grown on metal contaminated soils. Soil Biol Biochem 36:633–640

    Article  CAS  Google Scholar 

  • Cappuccino JC, Sherman N (1992) Negative staining. In: Cappuccino JC, Sherman N (eds) Microbiology: a laboratory manual, 3rd edn. Benjamin/Cummings PubCo, Redwood City, pp 125–179

    Google Scholar 

  • Carrillo-Castañeda G, Munoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL (2003) Plant growth-promoting bacteria promote copper and iron translocation from root to shoot in alfalfa seedlings. J Plant Nutr 26:1801–1814

    Article  Google Scholar 

  • Castro IV, Ferreira EM, McGrath SP (2003) Survival and plasmid stability of rhizobial introduced into contaminated soil. Soil Biol Biochem 35:49–54

    Article  CAS  Google Scholar 

  • Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1678

    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 YP, Rekha PD, Arunshen AB, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41

    Article  Google Scholar 

  • Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84

    Article  Google Scholar 

  • El-Tayeb MA, El-Enany AE, Ahmed NL (2006) Salicylic acid induced adaptive response to copper stress in sunflower (Helianthus annuus L.). Plant Growth Regul 50:191–199

    Article  CAS  Google Scholar 

  • Evangelou MWH, Bauer U, Ebel M, Schaeffer A (2007) The influence of EDDS and EDTA on the uptake of heavy metals of Cd and Cu from soil with tobacco Nicotiana tabacum. Chemosphere 68:345–353

    Article  CAS  Google Scholar 

  • Farina R, Beneduzi A, Ambrosini A, Campos SB, Lisboa BB, Wendisch V, Vargas LK, Passaglia LMP (2012) Diversity of plant growth-promoting rhizobacteria communities associated with the stages of canola growth. Appl Soil Ecol 55:44–52

    Article  Google Scholar 

  • Glick BR (2001) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393

    Article  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  CAS  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  Google Scholar 

  • Glick BR, Karaturovic DM, Newell PC (1995) A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can J Microbiol 41:533–536

    Article  CAS  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195

    Article  CAS  Google Scholar 

  • Gupta AK, Sinha S (2006) Chemical fractionation and heavy metals accumulation in the plants of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: selection of single extractants. Chemosphere 64:161–173

    Article  CAS  Google Scholar 

  • Gupta CP, Dubey RC, Maheshwari DK (2002) Plant growth enhancement and suppression of Macrophomina phaseolina causing charcoal root of peanut by fluorescent Pseudomonas. Biol Fert Soils 35:399–405

    Article  CAS  Google Scholar 

  • Gupta P, Samant K, Sahu A (2012) Isolation of cellulose-degrading bacteria and determination of their cellulolytic potential. Int J Microbiol 2012:1–5

  • He LY, Chen ZJ, Ren GD, Zhang YF, Qian M, Sheng XF (2009) Increased cadmium and lead uptake of a cadmium hyperaccumulator tomato by cadmium-resistant bacteria. Eco Environ Saf 72:1343–1348

    Article  CAS  Google Scholar 

  • Kabata Pendias A, Pendias H (1992) Trace elements in soils and plants. CRC Press, Boca Raton

    Google Scholar 

  • Khalid A, Arshad M, Zahir AA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480

    Article  CAS  Google Scholar 

  • Kloepper JW, Schroth MN (1978) Plant growth promoting rhizobacteria on radishes. In: Fourth international conference on plant pathogen bacteria. Angers, pp. 879–882

  • Li K, Ramakrishna W (2011) Effect of multiple metal resistant bacteria from contaminated lake sediments on metal accumulation and plant growth. J Hazard Mater 189:531–539

    Article  CAS  Google Scholar 

  • Luo S, Chen L, Chen J-L, Xiao X, Xu T, Wan Y, Rao C, Liu C, Liu Y, Lai C, Zeng G (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009a) Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manag 90:831–837

    Article  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009b) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75:719–725

    Article  CAS  Google Scholar 

  • Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Manier N, Deram A, Broos K, Denayer F, Van Haluwyn C (2009) White clover nodulation index in heavy metal contaminated soils: a potential bioindicator. J Environ Qual 38:685–692

    Article  CAS  Google Scholar 

  • Marques APGC, Rangel AOSS, Castro PML (2009) Remediation of heavy metal contaminated soils: phytoremediation as a potentially promising clean-up technology. Crit Rev Environ Sci Technol 39:622–654

    Article  CAS  Google Scholar 

  • Marques APGC, Pires C, Moreira H, Rangel AOSS, Castro PML (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235

    Article  CAS  Google Scholar 

  • Marques APGC, Moreira H, Franco AR, Rangel AOSS, Castro PML (2013) Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria: effects on phytoremediation strategies. Chemosphere 92:74–83

    Article  CAS  Google Scholar 

  • Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    Article  CAS  Google Scholar 

  • Oliveira RS, Dodd JC, Castro PML (2001) The mycorrhizal status of Phragmites australis in several polluted soils and sediments of an industrialised region of Northern Portugal. Mycorrhiza 10:241–247

    Article  CAS  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indole-acetic acid in development of the host plant root system. Appl Environ Microbiol 8:3795–3801

    Article  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  CAS  Google Scholar 

  • Pires C (2010) Bacteria in heavy metal contaminated soil: diversity, tolerance and use in remediation systems. Ph.D. dissertation, Cranfield University

  • Rajkumar M, Freitas H (2008) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Bioresour Technol 99:3491–3498

    Article  CAS  Google Scholar 

  • Rajkumar M, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    Article  CAS  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30

    Google Scholar 

  • Sahu GK, Sindhu SS (2011) Disease control and plant growth promotion of green gram by siderophore producing Pseudomonas sp. Res J Microbiol 6:735–749

    Article  Google Scholar 

  • Saleh SS, Glick BR (2001) Involvement of gasS and pros in enhancement of the plant growth-promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can J Microbiol 47:698–705

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  Google Scholar 

  • Shahzad SM, Khalid A, Arshad M, Rehman K (2010) Screening rhizobacteria containing ACC-deaminase for growth promotion of chickpea seedlings under axenic conditions. Soil Environ 29:38–46

    CAS  Google Scholar 

  • Sheng XF, Xia JJ (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64:1036–1042

    Article  CAS  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 611–651

    Google Scholar 

  • Tsezos M (2009) Metal–microbes interactions: beyond environmental protection. Adv Mater Res 71–73:527–532

    Article  Google Scholar 

  • Ultra VU, Yano A, Iwasaki K, Tanaka S, Kang YM, Sakurai K (2005) Influence of chelating agent addition on copper distribution and microbial activity in soil and copper uptake by brown mustard (Brassica juncea). Soil Sci Plant Nutr 51:193–202

    Article  CAS  Google Scholar 

  • van Loon LC (2007) Plant responses to plant growth promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  Google Scholar 

  • Vasseur L, Fortin MJ, Cyr J (1998) Clover and cress as indicator species of impacts from limed sewage sludge and landfill wastewater land application. Sci Total Environ 217:231–239

    Article  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Vivas A, Biro B, Ruíz-Lozanoa JM, Azcon R (2006) Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn toxicity. Chemosphere 52:1523–1533

    Article  Google Scholar 

  • Wallinga I, Vark W, Houba VJG, Lee JJ (1989) Plant analysis procedures. Syllabus, Department of Soil Science and Plant Nutrition, Wageningen Agricultural University, Wageningen

    Google Scholar 

  • Whiting NS, de Souza PM, Terry N (2001) Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ Sci Technol 35:3144–3150

    Article  CAS  Google Scholar 

  • Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR-122 that overproduce indole acetic acid. Curr Microbiol 32:67–71

    Article  CAS  Google Scholar 

  • Zaidi A, Khan MS (2007) Stimulatory effect of dual inoculation with phosphate solubilizing microorganisms and arbuscular mycorrhizal fungus on chickpea. Aust J Exp Agric 47:1014–1022

    Article  Google Scholar 

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Acknowledgments

This work was supported by National Funds from FCT—Fundação para a Ciência e a Tecnologia through projects PTDC/AGR/CFL/111583/2009 and PEst-OE/EQB/LA0016/2013. S.I.A. Pereira wish to acknowledge a research grant from FCT (Ref. SFRH/BPD/65134/2009) and Fundo Social Europeu (Programa Operacional Potencial Humano (POPH), Quadro de Referência Estratégico Nacional (QREN)).

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  1. CBQF - Centro de Biotecnologia e Química Fina - Laboratório Associado, Escola Superior de Biotecnologia, Universidade Católica Portuguesa/Porto, Rua Dr. António Bernardino Almeida, 4200-072, Porto, Portugal

    S. I. A. Pereira, L. Barbosa & P. M. L. Castro

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  1. S. I. A. Pereira
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  2. L. Barbosa
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Pereira, S.I.A., Barbosa, L. & Castro, P.M.L. Rhizobacteria isolated from a metal-polluted area enhance plant growth in zinc and cadmium-contaminated soil. Int. J. Environ. Sci. Technol. 12, 2127–2142 (2015). https://doi.org/10.1007/s13762-014-0614-z

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