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Effect of Pseudomonas fluorescens and pyoverdine on the phytoextraction of cesium by red clover in soil pots and hydroponics

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Abstract

With the aim of improving the phytoextraction rate of cesium (Cs), the effect of Pseudomonas fluorescens ATCC 17400 and its siderophore pyoverdine (PVD) on the uptake of Cs by red clover was studied in soil pots. This work also provides a mechanistic understanding of the Cs-bacteria (or PVD)-illite-plant interactions by using a simplified experimental design, i.e., hydroponics with either Cs in solution or Cs-spiked illite in suspension. For soil spiked with 11.2 mmol kg−1 (1480 mg kg−1) of Cs, 0.43% of total Cs was taken up by red clover in 12 days (119 μmol g−1 (16 mg g−1) of Cs dry matter in roots and 40 μmol g−1 (5 mg g−1) in shoots). In hydroponics with Cs in solution (0.1 mmol L−1 or 13 mg L−1), 75% of Cs was taken up vs. only 0.86% with Cs-spiked illite suspension. P. fluorescens and PVD did not increase Cs concentrations in aboveground parts and roots of red clover and even decreased them. The damaging effect of PVD on red clover growth was demonstrated with the biomass yielding 66% of the control in soil pots (and 100% mortality after 12 days of exposition) and only 56% in hydroponics (78% with illite in suspension). Nonetheless, PVD and, to a lesser extent, P. fluorescens increased the translocation factor up to a factor of 2.8. This study clearly showed a direct damaging effect of PVD and to a lower extent the retention of Cs by biofilm covering both the roots and illite, both resulting in the lower phytoextraction efficiency.

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References

  • Azmat R (2014) The impact of siderophore secretion by Pseudomonas stutzeri to chelatin Cu metal in solution culture. Pak J Bot 46:383–387

    CAS  Google Scholar 

  • Bradbury MH, Baeyens B (2000) A generalised sorption model for the concentration dependent uptake of caesium by argillaceous rocks. J Contam Hydrol 42:141–163

    Article  CAS  Google Scholar 

  • Broadley MR, Willey NJ (1997) Differences in root uptake of radiocaesium by 30 plant taxa. Environ Pollut 97:11–15

    Article  CAS  Google Scholar 

  • Brookshaw DR, Pattrick RAD, Lloyd JR, Vaughan DJ (2012) Microbial effects on mineral–radionuclide interactions and radionuclide solid-phase capture processes. Mineral Mag 76:777–806

    Article  CAS  Google Scholar 

  • Chen JC, Wang KS, Chen H, Chang SH (2010) Phytoremediation of Cr(III) by Ipomonea aquatica (water spinach) from water in the presence of EDTA and chloride: effects of Cr speciation. Bioresour Technol 101:3033–3039

    Article  CAS  Google Scholar 

  • Chen Z, Montavon G, Ribet S, Guo Z, Robinet JC, David K, Tournassat C, Grambow B, Landesman C (2014) Key factors to understand in-situ behavior of Cs in Callovo–Oxfordian clay-rock (France). Chem Geol 387:47–58

    Article  CAS  Google Scholar 

  • Cornell RM (1993) Adsorption of cesium on minerals: a review. J Radioanal Nucl Chem Artic 171:483–500

    Article  CAS  Google Scholar 

  • Cornu JY, Elhabiri M, Ferret C, Geoffroy VA, Jezequel K, Leva Y, Lollier M, Schalk IJ, Lebeau T (2014) Contrasting effects of pyoverdine on the phytoextraction of Cu and Cd in a calcareous soil. Chemosphere 103:212–219

    Article  CAS  Google Scholar 

  • Cremers A, Elsen A, De Preter P, Maes A (1988) Quantitative analysis of radiocaesium retention in soils. Nature 335:247–249

    Article  CAS  Google Scholar 

  • Dimkpa CO (2016) Microbial siderophores: production, detection and application in agriculture and environment. Endocyt Cell Res 27:7–16

    Google Scholar 

  • Ding D, Zhang Z, Lei Z, Yang Y, Cai T (2016) Remediation of radiocesium-contaminated liquid waste, soil,and ash: a mini review since the Fukushima Daiichi Nuclear Power Plant accident. Environ Sci Pollut Res 23:2249–2263

    Article  CAS  Google Scholar 

  • Dong H, Jaisi DP, Kim J, Zhang G (2009) Microbe-clay mineral interactions. Am Mineral 94:1505–1519

    Article  CAS  Google Scholar 

  • Dorjey S, Dolkar D, Sharma R (2017) Plant growth promoting rhizobacteria pseudomonas: a review. Int J Curr Microbiol App Sci 6:1335–1344

    Article  Google Scholar 

  • Environmental Protection Agency (EPA)(2007) 3051A - 1 Revision 1 February Method 3051A Microwave assisted acid digestion of sediments, sludges, soils, and oils. https://www.epa.gov/sites/production/files/2015-12/documents/3051a.pdf accessed 25 september 2017

  • Flemming H-C (1995) Sorption sites in biofilms. Water Sci Technol 32:27–33

    Article  CAS  Google Scholar 

  • Forsberg S, Strandmark M (2001) Migration and chemical availability of 137Cs and 90Sr in Swedish long-term experimental pastures. Water Air Soil Pollut 127:157–171

    Article  CAS  Google Scholar 

  • Fulekar MH, Singh A, Thorat V, Kaushik CP, Eapen S (2010) Phytoremediation of 137Cs using Catharanthus roseus. Indian J Pure Appl Phys 48:516–519

    CAS  Google Scholar 

  • Fuller AJ, Shaw S, Ward MB, Haigh SJ, Mosselmans JFW, Peacock CL, Stackhouse S, Dent AJ, Trivedi D, Burke IT (2015) Caesium incorporation and retention in illite interlayers. App. Clay Sci 108:128–134

    Article  CAS  Google Scholar 

  • Gadd GM (2010) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279

    Article  Google Scholar 

  • Georgias H, Taraz K, Budzikiewicz H, Geoffroy V, Meyer J (1999) The structure of the pyoverdin from Pseudomonas fluorescens 1.3. Structural and biological relationships of pyoverdins from different strains. ZEITSCHRIFT FUR Naturforsch. C-A. J Biosci 54:301–308

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hazotte AA (2016) Rôle de métabolites bactériens dans la mobilisation du césium d’une illite dopée: étude mécaniste et application à la phytoextraction. Thesis, University of Nantes (in French)

  • Hazotte AA, Péron O, Abdelouas A, Montavon G, Lebeau T (2016) Microbial mobilization of cesium from illite: the role of organic acids and siderophores. Chem Geol 428:8–14

    Article  CAS  Google Scholar 

  • Hoflich G, Metz R (1997) Interactions of plant-microorganism-associations in heavy metal containing soils from sewage farms. Bodenkultur 48:239–247

    Google Scholar 

  • IRSN (2011) Bilan des conséqences de l’accident de Fukushima sur l’environnement au Japon, un an après l’accident. http://www.irsn.fr/FR/connaissances/Installations_nucleaires/Les-accidents-nucleaires/accident-fukushima-2011/fukushima-1-an/Documents/IRSN_Fukushima_Synthese-Environnement_28022012.pdf (accessed July 7, 2016) (in French)

  • Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal-contaminated soils: a review. Environ Pollut 153:497–522

    Article  CAS  Google Scholar 

  • Neugschwandtner RW, Tlustos P, Komárek M, Száková J, Jakoubková L (2012) Chemically enhanced phytoextraction of risk elements from a contaminated agricultural soil using Zea mays and Triticum aestivum: performance and metal mobilization over a three year period. Int J Phytoremediation 14:754–771

    Article  CAS  Google Scholar 

  • Patra M, Niladri B, Bulbul B, Archana S (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plants systems and the development of genetic tolerance. Environ Exp Bot 52:199–223

    Article  CAS  Google Scholar 

  • Poinssot C, Baeyens B, Bradbury MH (1999) Experimental and modelling studies of caesium sorption on illite. Geochim Cosmochim Acta 63:3217–3227

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Riise G, Bjørnstad H, Lien H, Oughton D, Salbu B (2005) A study on radionuclide association with soil components using a sequential extraction procedure. J Radioanal Nucl Chem 142:531–538

    Article  Google Scholar 

  • Sawhney B (1972) Selective sorption and fixation of cations by clay-minerals—review. 20:93–100

  • Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194

    Article  CAS  Google Scholar 

  • Shahid M, Austruy A, Echevarria G, Arshad M, Sanaullah M, Aslam M, Nadeem M, Nasim W, Dumat C (2013) EDTA-enhanced phytoremediation of heavy metals: a review. Soil Sediment Contam. An. Int J 23:389–416

    Google Scholar 

  • Sharma S, Singh B, Manchanda VK (2015) 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

    Article  CAS  Google Scholar 

  • Singh S, Thorat V, Kaushik CP, Raj K, Eapen S, D’Souza SF (2009) Potential of Chromolaena odorata for phytoremediation of 137Cs from solution and low level nuclear waste. J Hazard Mater 162:743–745

    Article  CAS  Google Scholar 

  • Staunton S, Roubaud M (1997) Adsorption of 137Cs on montmorillonite and illite: effect of charge compensating cation, ionic strength, concentration of Cs, K and fulvic acid. Clay Clay Miner 45:251–260

    Article  CAS  Google Scholar 

  • Takeda A, Tsukada H, Nakao A, Takaku Y, Hisamatsu S (2013) Time-dependent changes of phytoavailability of Cs added to allophanic andosols in laboratory cultivations and extraction tests. J Environ Radioact 122:29–36

    Article  CAS  Google Scholar 

  • Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387

    Article  CAS  Google Scholar 

  • Veresoglou DS, Tsialtas JT, Barbayiannis N, Zalidis GC (1995) Caesium and strontium uptake by two pasture plant species grown in organic and inorganic soils. Agric Ecosyst Environ 56:37–42

    Article  CAS  Google Scholar 

  • Vinichuk MM, Johanson KJ, Rosén K, Nilsson I (2005) Role of the fungal mycelium in the retention of radiocaesium in forest soils. J Environ Radioact 78:77–92

    Article  CAS  Google Scholar 

  • Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent pseudomonas. BMC Microbiol 9:174

    Article  CAS  Google Scholar 

  • Wendling LA, Harsh JB, Ward TE, Palmer CD, Hamilton MA, Boyle JS, Flury M (2005a) Cesium desorption from illite as affected by exudates from rhizosphere bacteria. Environ Sci Technol 39:4505–4512

    Article  CAS  Google Scholar 

  • Wendling LA, Harsh JB, Palmer CD, Hamilton MA, Dion HM, Boyle JS, Flury M (2005b) Rhizosphere effects on cesium fixation sites of soil containing micaceous clays. Soil Sci Soc Am J 69:1652

    Article  CAS  Google Scholar 

  • White PJ, Broadley MR (2000) Mechanisms of caesium uptake by plants. New Phytol 147:241–256

    Article  CAS  Google Scholar 

  • Wu H, Tang S, Zhang X, Guo J, Song Z, Tian S, Smith DL (2009) Using elevated CO2 to increase the biomass of a Sorghum vulgare×Sorghum vulgare var. sudanense hybrid and Trifolium pratense L. and to trigger hyperaccumulation of cesium. J Hazard Mater 170: 861–870.

  • Xu W, Li W, He J, Singh B, Xiong Z (2009) Effects of insoluble Zn, Cd, and EDTA on the growth, activities of antioxidant enzymes and uptake of Zn and Cd in Vetiveria zizanioides. J Environ Sci 21:186–192

    Article  CAS  Google Scholar 

  • Zhu YG, Shaw G (2000) Soil contamination with radionuclides and potential remediation. Chemosphere 41:121–128

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are most grateful to Dr. Christophe Tournassat (with BRGM, France) for supplying the illite powder.

Funding

This work was financed by France’s Pays de la Loire Regional Council (under the RS2E-OSUNA Project).

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Correspondence to Thierry Lebeau.

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Responsible editor: Georg Steinhauser

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Hazotte, A., Péron, O., Gaudin, P. et al. Effect of Pseudomonas fluorescens and pyoverdine on the phytoextraction of cesium by red clover in soil pots and hydroponics. Environ Sci Pollut Res 25, 20680–20690 (2018). https://doi.org/10.1007/s11356-018-1974-6

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  • DOI: https://doi.org/10.1007/s11356-018-1974-6

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