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Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows

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Abstract

A variety of plants growing on metalliferous soils accumulate metals in their harvestable parts and have the potential to be used for phytoremediation of heavy metal polluted land. There is increasing evidence that rhizosphere bacteria contribute to the metal extraction process, but the mechanisms of this plant–microbe interaction are not yet understood. In this study ten rhizosphere isolates obtained from heavy metal accumulating willows affiliating with Pseudomonas, Janthinobacterium, Serratia, Flavobacterium, Streptomyces and Agromyces were analysed for their effect on plant growth, Zn and Cd uptake. In plate assays Zn, Cd and Pb resistances and the ability of the bacteria to produce indole-3-acetic acid (IAA), 1-amino-cyclopropane-1-carboxylic acid deaminase (ACC deaminase) and siderophores were determined. The isolates showed resistance to high Zn concentrations, indicating an adaptation to high concentrations of mobile Zn in the rhizosphere of Salix caprea. Four siderophore producers, two IAA producers and one strain producing both siderophores and IAA were identified. None of the analysed strains produced ACC deaminase. Metal mobilization by bacterial metabolites was assessed by extracting Zn and Cd from soil with supernatants of liquid cultures. Strain Agromyces AR33 almost doubled Zn and Cd extractability, probably by the relase of Zn and Cd specific ligands. The remaining strains, immobilized both metals. When Salix caprea plantlets were grown in γ-sterilized, Zn/Cd/Pb contaminated soil and inoculated with the Zn resistant isolates, Streptomyces AR17 enhanced Zn and Cd uptake. Agromyces AR33 tendentiously promoted plant growth and thereby increased the total amount of Zn and Cd extracted from soil. The IAA producing strains did not affect plant growth, and the siderophore producers did not enhance Zn and Cd accumulation. Apparently other mechanisms than the production of IAA, ACC deaminase and siderophores were involved in the observed plant–microbe interactions.

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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 

  • Amir H, Pineau R (2003) Release of Ni and Co by mircrobial activity in New Caledonian ultramafic soils. Can J Microbiol 49:288–293

    Article  PubMed  CAS  Google Scholar 

  • Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva V, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz K-J, Stepanok VV (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652

    Article  PubMed  CAS  Google Scholar 

  • Brown CM, Dilworth MJ (1975) Ammonia assimilation by Rhizobium cultures and bacteroids. J Gen Microbiol 122:61–67

    Google Scholar 

  • Burd GI, Dixon DG, Glick BR (1998) A plant growth promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668

    PubMed  CAS  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth promoting bacteria that decease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    Article  PubMed  CAS  Google Scholar 

  • Dell’Amico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant grwoth-promoting bacteria. FEMS Microbiol Ecol 52:153–162

    Article  PubMed  CAS  Google Scholar 

  • de Souza MO, Chu D, Zhao M, Zayed AM, Ruzin SE, Schichnes D, Terry N (1999) Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian Mustard. Plant Physiol 199:565–573

    Article  Google Scholar 

  • Dos Santos Utmazian MN, Wenzel WW (2007) Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. J Plant Nutr Soil Sci 170:265–272

    Article  CAS  Google Scholar 

  • Edwards U, Rogall T, Blocker H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853

    Article  PubMed  CAS  Google Scholar 

  • Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393

    Article  PubMed  CAS  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentration by plant growth promoting bacteria. J Theor Biol 190:63–68

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Boyer GL (1996) Siderophore-mediated aluminium uptake by Bacillus megaterium ATCC 19213. Appl Environ Microbiol 62:4044–4048

    PubMed  CAS  Google Scholar 

  • Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of Ni hyperaccumulator Thlaspi goesingense. Appl Envir Microbiol 70:2667–2677

    Article  CAS  Google Scholar 

  • Kalinowski BE, Oskarsson A, Albinsson Y, Arlinger J, Ödegaard-Jensen A, Andlid T, Pedersen K (2004) Microbial leaching of uranium and other trace elements from shale mine tailings at Ranstad. Geoderma 122:177–194

    Article  CAS  Google Scholar 

  • Lasat MM, Baker AJM, Kochain LV (1996) Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiol 112:1715–1722

    PubMed  CAS  Google Scholar 

  • Lodewyckx C, Mergeay M, Vangronsveld J, Clijsters H, Van Der Lelie D (2002) Isolation, characterization and identification of bacteria associated with the zinc hyperaccumulator Thlaspi caerulescens subsp. calaminaria. Int J Phytoremediation 4:101–105

    Article  PubMed  CAS  Google Scholar 

  • McGrath SM, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminates soils. Plant Soil 188:153–159

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao F-J (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:1–6

    Article  CAS  Google Scholar 

  • Milagres AMF, Machuca A, Napoleao D (1999) Detection of siderophore production from several fungi and bacteria by modification of chromeazurol S (CAS) agar plate assay. J Microbiol Methods 37:1–6

    Article  PubMed  CAS  Google Scholar 

  • Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119:736–747

    PubMed  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  PubMed  CAS  Google Scholar 

  • Nriagu JO (1979) Global inventory of natural and anthropogenix emissions of trace metals to the atmosphere. Nature 279:409–411

    Article  PubMed  CAS  Google Scholar 

  • Pattern CL, Glick RB (1996) Bacterial biosynthesis of indole-acetic-acid. Can J Microbiol 42:207–220

    Article  Google Scholar 

  • Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr 6+ on the growth of Indian mustard. Chemosphere 62:741–748

    Article  PubMed  CAS  Google Scholar 

  • Sawar M, Kremer RJ (1995) Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol 20:282–285

    Article  Google Scholar 

  • Sessitsch A, Hardarson G, Akkermans ADL, de Vos WM (1997) Characterization of Rhizobium etli and other Rhizobium spp. that nodulate Phaseolus vulgaris L. in an Austrian soil. Mol Ecol 6:601–608

    Article  CAS  Google Scholar 

  • Sessitsch A, Weilharter A, Gerzabek MH, Kirchmann H, Kandeler E (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67:4215–4224

    Article  PubMed  CAS  Google Scholar 

  • Singh OV, Labana S, Pandley G, Budhiaraja R, Jain RK (2001) Phytoremediation: an overview of metallic ion decontamination from soil. Appl Microbiol Biotechnol 61:405–412

    Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 43:1691–1705

    Google Scholar 

  • Wenzel WW, Jockwer F (1999) Accumulation of heavy metals grown on mineralized soils of the Austrian alps. Environ Pollut 104:145–155

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This project was funded by the Wiener Wissenschafts-, Forschungs- und Technologiefonds. Melanie Kuffner received a DOC fellowship from the Austrian Academy of Sciences (Doktorandenprogramm der Österreichischen Akademie der Wissenschaften).

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Correspondence to Angela Sessitsch.

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Responsible Editor: David E. Crowley.

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Kuffner, M., Puschenreiter, M., Wieshammer, G. et al. Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304, 35–44 (2008). https://doi.org/10.1007/s11104-007-9517-9

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