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Plant and Soil

, Volume 312, Issue 1–2, pp 207–218 | Cite as

Oxygen input controls the spatial and temporal dynamics of arsenic at the surface of a flooded paddy soil and in the rhizosphere of lowland rice (Oryza sativa L.): a microcosm study

  • Matthieu N. Bravin
  • Fanny Travassac
  • Martine Le Floch
  • Philippe Hinsinger
  • Jean-Marie GarnierEmail author
Regular Article

Abstract

The impact of oxygen (O2) input at the soil surface and in the rhizosphere of rice (Oryza sativa L.) on the spatial and temporal dynamics of arsenic (As) was investigated in a flooded paddy soil. A soil microcosm and root-mat technique were designed to mimic submerged conditions of paddy fields. Water-filled containers with (planted) or without (unplanted) 27-day-old rice seedlings were fitted for 20 days on top of microcosms containing an As-affected soil (Bangladesh). After the initial establishment of strongly reduced conditions (−230 mV) in both planted and unplanted soils, the redox potential gradually increased until the day 8 to reach + 50 mV at 2 mm from the surface of unplanted soils only. This oxidation was associated with an accumulation of NH4-oxalate extractable As (25.7 mg kg−1) in the 0.5-mm top layer, i.e. at levels above the initial total content of As in the soil (14 mg kg−1) and a subsequent depletion of As in soil solution at 2 mm from soil surface. Root O2-leakage induced the formation of an iron (Fe) plaque in root apoplast, with no evidence of outer rhizosphere oxidation. Arsenic content reached 173 mg kg−1 in the Fe plaque. This accumulation induced a depletion of As in soil solution over several millimetres in the rhizosphere. Arsenic contents in root symplast and shoots (112 and 2.3 mg kg−1, respectively) were significantly lower than in Fe plaque. Despite a large As concentration in soil solution, Fe plaque appeared highly efficient to sequester As and to restrict As acquisition by rice. The oxidation-mediated accumulation of As in the Fe plaque and in the oxidised layer at the top of the soil mobilised 21 and 3% of the initial amount of As in the planted and unplanted soils, respectively. Soil solution As concentration steadily decreased during the last 16 days of the soil stage, likely indicating a decrease in the ability of the soil to re-supply As from the solid-phase to the solution. The driving force of As dynamic in soil was therefore attributed to the As diffusion from reduced to oxidised soil layers. These results suggest a large mobility of As in the soil during the flooded period, controlled by the setting of oxic/anoxic interfaces at the surface of soil in contact with flooding water and in the rhizosphere of rice.

Keywords

Arsenic Bangladesh Iron coatings Oryza sativa L. Oxidation Rhizosphere 

Notes

Acknowledgments

This research was funded by the ACI “Ecodyn” (French Ministry of Research). We deeply thank Michaël Clairotte and Jean-Louis Aznar for the analyses, Nicole Balsera and Didier Arnal for the technical assistance.

References

  1. Ando T, Yoshida S, Nishiyama I (1983) Nature of oxidizing power of rice roots. Plant Soil 72:57–71CrossRefGoogle Scholar
  2. Bacha RE, Hossner LR (1977) Characteristics of coatings formed on rice roots as affected by iron and manganese additions. Soil Sci Soc Am J 41:931–935CrossRefGoogle Scholar
  3. Begg MCB, Kirk GJD, Mackenzie AF, Neue HU (1994) Root-induced iron oxidation and pH changes in the lowland rice rhizosphere. New Phytol 128:469–477CrossRefGoogle Scholar
  4. Calba H, Firdaus, Cazevieille P, Thée C, Poss R, Jaillard B (2004) The dynamics of protons, aluminium, and calcium of maize cultivated in tropical acid soils: experimental study and modelling. Plant Soil 260:33–46CrossRefGoogle Scholar
  5. Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97PubMedCrossRefGoogle Scholar
  6. Cheng Y, Howieson JG, O’Hara GW, Watkin ELJ, Souche G, Jaillard B, Hinsinger P (2004) proton release by roots of Medicago murex and Medicago sativa growing in acidic conditions, and implications for rhizosphere pH changes and nodulation at low pH. Soil Biol Biochem 36:1357–1365CrossRefGoogle Scholar
  7. Cornell RM, Schwertmann U (2003) The iron oxides, 2ndnd edn. Wiley, Weinheim, New YorkGoogle Scholar
  8. Cornu JY, Staunton S, Hinsinger P (2007) Copper concentration in plants and in the rhizosphere as influenced by the iron status of tomato (Lycopersicon esculentum L.). Plant Soil 292:63–77CrossRefGoogle Scholar
  9. FAO (1999) World reference base for soil resources. FAO, Roma, p 96Google Scholar
  10. Fitz WJ, Wenzel WW, Zhang H, Nurmi J, Stipek K, Fischerova Z, Schweiger P, Kollensperger G, Ma LQ, Stingeder G (2003) Rhizosphere characteristics of the Arsenic hyperaccumulator Pteris vittata L. and monitoring of phytoremoval efficiency. Environ Sci Technol 37:5008–5014PubMedCrossRefGoogle Scholar
  11. Flessa H, Fischer WR (1992) Plant-induced changes in the redox potentials of rice rhizospheres. Plant Soil 143:55–60CrossRefGoogle Scholar
  12. Frenzel P, Bosse U, Janssen PH (1999) Rice roots and methanogenesis in a paddy soil: ferric iron as an alternative electron acceptor in the rooted soil. Soil Biol Biochem 31:421–430CrossRefGoogle Scholar
  13. Hansel CM, Fendorf S, Sutton S, Newville M (2001) Characterization of Fe plaque and associated metals on the roots of mine-wasted impacted aquatic plants. Environ Sci Technol 35:3863–3868PubMedCrossRefGoogle Scholar
  14. Hinsinger P, Gilkes RJ (1995) Root-induced dissolution of phosphate rock in the rhizosphere of lupins grown in alkaline soil. Aust J Soil Res 33:477–489CrossRefGoogle Scholar
  15. Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59CrossRefGoogle Scholar
  16. Kirk GJD, Bajita JB (1995) Root-induced iron oxidation, pH changes and zinc solubilization in the rhizosphere of lowland rice. New Phytol 131:129–137CrossRefGoogle Scholar
  17. Liesack W, Schnell S, Revsbech NP (2000) Microbiology of flooded rice paddies. FEMS Microbiol Rev 24:625–645PubMedCrossRefGoogle Scholar
  18. Liu WJ, Zhu YG, Smith FA, Smith SE (2004a) Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oryza sativa L.) grown in solution culture? J Exp Bot 55:1707–1713PubMedCrossRefGoogle Scholar
  19. Liu WJ, Zhu YG, Smith FA, Smith SE (2004b) Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture? New Phytol 162:481–488CrossRefGoogle Scholar
  20. Liu WJ, Zhu YG, Smith FA (2005) Effects of iron and manganese plaques on arsenic uptake by rice seedlings (Oryza sativa L.) grown in solution culture supplied with arsenate and arsenite. Plant Soil 277:127–138CrossRefGoogle Scholar
  21. Liu WJ, Zhu YG, Hu Y, Williams PN, Gault AG, Meharg AA, Charnock JM, Smith FA (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L.). Environ Sci Technol 40:5730–5736PubMedCrossRefGoogle Scholar
  22. Lüdemann H, Arth I, Liesack W (2000) Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Appl Environ Microb 66:754–762CrossRefGoogle Scholar
  23. Masscheleyn PH, Delaune RD, Patrick WH Jr (1991) Effect of redox potential and pH on arsenic speciation and solubility in a contaminated soil. Environ Sci Technol 25:1414–1419CrossRefGoogle Scholar
  24. Meharg AA, Rahman M (2003) Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ Sci Technol 37:229–234PubMedCrossRefGoogle Scholar
  25. Meng X, Korfiatis GP, Bang S, Bang KW (2002) Combined effects of anions on arsenic removal by iron hydroxides. Toxicol Lett 133:103–111PubMedCrossRefGoogle Scholar
  26. Pansu M, Gautheyrou J (2003) L’analyse du sol minéralogique, organique et minérale. Springer, France, p 1012Google Scholar
  27. Ratering S, Schnell S (2000) Localization of iron-reducing activity in paddy soil by profile studies. Biogeochemistry 48:341–365CrossRefGoogle Scholar
  28. Revsbech NP, Pedersen O, Reichardt W, Briones A (1999) Microsensor analysis of oxygen and pH in the rice rhizosphere under field and laboratory conditions. Biol Fertil Soils 29:379–385CrossRefGoogle Scholar
  29. Saleque MA, Kirk GJD (1995) Root-induced solubilization of phosphate in the rhizosphere of lowland rice. New Phytol 129:325–336CrossRefGoogle Scholar
  30. Takahashi Y, Minamikawa R, Hattori KH, Kurishima K, Kihou N, Yuita K (2004) Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol 38:1038–1044PubMedCrossRefGoogle Scholar
  31. Taylor GJ, Crowder AA (1983) Use of DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70:1254–1257CrossRefGoogle Scholar
  32. Ultra Jr VU, Tanaka S, Sakurai K, Iwasaki K (2007) Effects of arbuscular mycorrhiza and phosphorus application on arsenic toxicity in sunflower (Helianthus annuus L.) and on the transformation of arsenic in the rhizosphere. Plant Soil 290:29–41CrossRefGoogle Scholar
  33. van Geen A, Rose J, Thoral S, Garnier JM, Zheng Y, Bottero JY (2004) Decoupling of As and Fe release to Bangladesh groundwater under reducing conditions. Part II: evidence from sediment incubation. Geochim Cosmochim Acta 68:3475–3486CrossRefGoogle Scholar
  34. van Geen A, Zheng Y, Cheng Z, He Y, Dhar RK, Garnier JM, Rose J, Seddique A, Hoque MA, Ahmed KM (2006) Impact of irrigating rice paddies with groundwater containing arsenic in Bangladesh. Sci Total Environ 367:769–777PubMedCrossRefGoogle Scholar
  35. Wenzel WW, Kirchbaumer N, Prohaska T, Stingeder G, Lombi E, Adriano CD (2001a) Arsenic fractionation in soils using an improved sequential extraction procedure. Anal Chim Acta 436:309–323CrossRefGoogle Scholar
  36. Wenzel WW, Wieshammer G, Fitz WJ, Puschenreiter M (2001b) Novel rhizobox design to assess rhizosphere characteristics at high spatial resolution. Plant Soil 237:37–45CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Matthieu N. Bravin
    • 1
  • Fanny Travassac
    • 2
  • Martine Le Floch
    • 2
  • Philippe Hinsinger
    • 1
  • Jean-Marie Garnier
    • 2
    Email author
  1. 1.INRA – SupAgro, UMR 1222 Biogéochimie du Sol et de la RhizosphèreMontpellier Cedex 1France
  2. 2.CNRS – Université Paul Cézanne, UMR 6635 CEREGE, Pôle d’activité de l’ArboisAix-en-ProvenceFrance

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