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Microbial Ecology

, Volume 52, Issue 2, pp 322–333 | Cite as

Zinc Phosphate Transformations by the Paxillus involutus/Pine Ectomycorrhizal Association

  • Marina Fomina
  • John M. Charnock
  • Stephen Hillier
  • Ian J. Alexander
  • Geoffrey M. GaddEmail author
Article

Abstract

In this research, we investigate zinc phosphate transformations by Paxillus involutus/pine ectomycorrhizas using zinc-resistant and zinc-sensitive strains of the ectomycorrhizal fungus under high- and low-phosphorus conditions to further understand fungal roles in the transformation of toxic metal minerals in the mycorrhizosphere. Mesocosm experiments with ectomycorrhizas were performed under sterile conditions with zinc phosphate localized in cellophane bags: zinc and phosphorus mobilization and uptake by the ectomycorrhizal biomass were analyzed. In the presence of a phosphorus source, an ectomycorrhizal association with a zinc-resistant strain accumulated the least zinc compared to a zinc-sensitive ectomycorrhizal association and non-mycorrhizal plants. Under low-phosphorus conditions, mycorrhizal seedlings infected with the zinc-resistant strain increased the dissolution of zinc phosphate and zinc accumulation by the plant. Extended X-ray absorption fine structure analysis of both mycorrhizal and nonmycorrhizal roots showed octahedral coordination of zinc by oxygen-containing ligands such as carboxylates or phosphate. We conclude that zinc phosphate solubilization and zinc and phosphorus uptake by the association depend on ectomycorrhizal infection, strain of the mycobiont, and the phosphorus status of the matrix.

Keywords

Mycorrhizal Fungus Ectomycorrhizal Fungus Zinc Phosphate Phosphorus Deficiency Zinc Accumulation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This research was funded by the BBSRC/BIRE program (94/BRE13640), BNFL, and CCLRC Daresbury SRS (SRS user grant 40107). We thank Dr. Jan Colpaert and Miss Kristin Adriaensen (Limburgs University Centre, Belgium) for the provision of fungal strains. We are very grateful to Dr. Lorrie Murphy and Dr. Fred Mosselmans (Stations 7.1, CLRC Daresbury SRS, UK) for their help with X-ray absorption spectroscopy and to Mr. Martin Kierans [Centre for High Resolution Imaging and Processing (CHIPs), School of Life Sciences, University of Dundee, Scotland] for assistance with cryo-scanning electron microscopy. We are also very grateful to Prof. John Raven FRS (School of Life Sciences, University of Dundee) for helpful discussions.

References

  1. 1.
    Ahonen-Jonnarth, U, Finlay, RD (2001) Effects of elevated nickel and cadmium concentrations on growth and nutrient uptake of mycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Plant Soil 236: 129–138CrossRefGoogle Scholar
  2. 2.
    Ahonen-Jonnarth, U, Goransson, A, Finlay, RD (2003) Growth and nutrient uptake of ectomycorrhizal Pinus sylvestris seedlings in a natural substrate treated with elevated Al concentrations. Tree Physiol 23: 157–167PubMedGoogle Scholar
  3. 3.
    Adriaensen, K, Van der Lelie, D, Van Laere, A, Vangrosveld, J, Colpaert, JV (2003) A zinc-adapted fungus protects pines from zinc stress. New Phytol 161: 549–555CrossRefGoogle Scholar
  4. 4.
    Binsted, N (1998) Daresbury Laboratory EXCURV98 ProgramGoogle Scholar
  5. 5.
    Binsted, N, Strange, RW, Hasnain, SS (1992) Constrained and restrained refinement in EXAFS data analysis with curved wave theory. Biochem 31: 12117–12125CrossRefPubMedGoogle Scholar
  6. 6.
    Brown, MT, Wilkins, DA (1985) Zinc tolerance of mycorrhizal Betula. New Phytol 99: 101–106CrossRefGoogle Scholar
  7. 7.
    Brown, S, Chaney, R, Hallfrisch, J, Ryan, JA, Berti, WR (2004) In situ soil treatments to reduce the phyto- and bioavailability of lead, zinc, and cadmium. J Environ Qual 33: 522–531PubMedCrossRefGoogle Scholar
  8. 8.
    Bu¨cking, H, Heyser, W (1999) Elemental composition and function of polyphosphates in ectomycorrhizal fungi—an X-ray microanalytical study. Mycol Res 103: 31–39CrossRefGoogle Scholar
  9. 9.
    Burford, EP, Fomina, M, Gadd, GM (2003) Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag 67: 1127–1155CrossRefGoogle Scholar
  10. 10.
    Burgstaller, W, Schinner, F (1993) Leaching of metals with fungi. J Biotechnol 27: 91–116CrossRefGoogle Scholar
  11. 11.
    Burleigh, SH, Cavagnaro, T, Jakobsen, I (2002) Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53: 1593–1601CrossRefPubMedGoogle Scholar
  12. 12.
    Chen, X-B, Wright, JV, Conca, JL, Peurrung, LM (1997) Evaluation of heavy metal remediation using mineral apatite. Water Air Soil Pollut 98: 57–78Google Scholar
  13. 13.
    Colpaert, JV, Van Assche, JA (1992) Zinc toxicity in ectomycorrhizal Pinus sylvestris. Plant Soil 143: 201–211CrossRefGoogle Scholar
  14. 14.
    Colpaert, JV, Vandenkoornhuyse, P, Adriaensen, K, Vangronsveld, J (2000) Genetic variation and heavy metal tolerance in the ectomycorrhizal basidiomycete Suillus luteus. New Phytol 147: 367–379CrossRefGoogle Scholar
  15. 15.
    Colpaert, JV, Muller, LAH, Lambaerts, M, Andriaensen, K, Vangronsveld, J (2004) Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytol 162: 549–559CrossRefGoogle Scholar
  16. 16.
    Conca, JL (1997) Phosphate-induced metal stabilization (PIMS). Final report to the U.S. Environmental Protection Agency 68D60023, Res. Triangle Park, NCGoogle Scholar
  17. 17.
    Duff, SMG, Sarath, G, Plaxton, WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90: 791–800CrossRefGoogle Scholar
  18. 18.
    Fomina, M, Alexander, IJ, Hillier, S, Gadd, GM (2004) Zinc phosphate and pyromorphite solubilization by soil plant-symbiotic fungi. Geomicrobiol J 21: 351–366CrossRefGoogle Scholar
  19. 19.
    Fomina, M, Alexander, IJ, Colpaert, JV, Gadd, GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37: 857–866CrossRefGoogle Scholar
  20. 20.
    Gadd, GM (1993) Interactions of fungi with toxic metals. New Phytol 124: 25–60CrossRefGoogle Scholar
  21. 21.
    Gilroy, S, Jones, DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5: 56–60CrossRefPubMedGoogle Scholar
  22. 22.
    Greger, M (1999) Metal availability and bioconcentration in plants. In: Prasad, MNV, Hagemeyer, J (Eds.) Heavy Metal Stress in Plants from Molecules to Ecosystem. Springer-Verlag, Berlin, Heidelberg, Germany, pp 1–27Google Scholar
  23. 23.
    Gurman, SJ, Binsted, N, Ross, I (1984) A rapid, exact, curved-wave theory for EXAFS calculations. J Phys Chem 17: 143–151Google Scholar
  24. 24.
    Gurman, SJ, Binsted, N, Ross, I (1986) A rapid, exact, curved-wave theory for EXAFS calculations. 2. The multiple-scattering contributions. J Phys Chem 19: 1845–1861Google Scholar
  25. 25.
    Hartley-Whitaker, J, Cairney, JWG, Meharg, AA (2000) Sensitivity to Cd and Zn of host and symbiont of ectomycorrhizal Pinus sylvestris L. (Scots pine) seedlings. Plant Soil 218: 31–42CrossRefGoogle Scholar
  26. 26.
    Hedin, L, Lundqvist, S (1969) Effects of electron–electron and electron–phonon interactions on the one-electron states of solids. Solid State Phys 23: 1–181CrossRefGoogle Scholar
  27. 27.
    Heuwinkel, H, Kirkby, EA, Bot, J Le, Marschner, H (1992) Phosphorus deficiency enhances molybdenum uptake by tomato plants. J Plant Nutr 15: 549–568CrossRefGoogle Scholar
  28. 28.
    Horst, WJ, Kamh, M, Jibrin, JM, Chude, VA (2001) Agronomic measures for increasing P availability to crops. Plant Soil 237: 211–233CrossRefGoogle Scholar
  29. 29.
    Huang, C, Barker, SJ, Langridge, P, Smith, FW, Graham, D (2000) Zinc deficiency up-regulates expression of high-affinity phosphatetransporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol 124: 415–422CrossRefPubMedGoogle Scholar
  30. 30.
    Ingestad, T (1979) Mineral nutrient requirements of Pinus sylvestris and Picea abies seedlings. Physiol Plant Pathol 45: 373–380CrossRefGoogle Scholar
  31. 31.
    Jentschke, G, Godbold, DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109: 107–116CrossRefGoogle Scholar
  32. 32.
    Jones, MD, Hutchinson, TC (1988) Nickel toxicity in mycorrhizal birch seedlings infected with Lactarius rufus or Scleroderma flavidum. II Uptake of nickel, calcium, magnesium, phosphorus and iron. New Phytol 108: 461–470CrossRefGoogle Scholar
  33. 33.
    Jongmans, AG, Van Breemen, N, Lundstrom, U, Van Hees, PAW, Finlay, RD, Srinivasan, M, Unestam, T, Giesler, R, Melkerud, PA, Olsson, M (1997) Rock-eating fungi. Nature 389: 682–683CrossRefGoogle Scholar
  34. 34.
    Koide, RT, Kabir, Z (2001) Nutrient economy of red pine affected by interactions between Pisolithus tinctorius and other forest-floor microbes. New Phytol 105: 179–188CrossRefGoogle Scholar
  35. 35.
    Lajtha, K, Harrison, AF (1995) Strategies of phosphorus acquisition and conservation by plant species and communities. In: Tiessen, H (Ed.) Phosphorus in the Global Environment. John Wiley Sons Ltd, Chichester, UK, pp 140–147Google Scholar
  36. 36.
    Lapeyrie, F, Ranger, J, Vairelles, D (1991) Phosphate-solubilizing activity of ectomycorrhizal fungi in vitro. Can J Bot 69: 342–346CrossRefGoogle Scholar
  37. 37.
    Lapeyrie, F, Ranger, J, Vairelles, D (1991) Phosphate-solubilizing activity of ectomycorrhizal fungi in vitro. Can J Bot 69: 342–346Google Scholar
  38. 38.
    Lundstrom, US, Van Breemen, N, Bain, D (2000) The podzolization process. A review. Geoderma 94: 91–107CrossRefGoogle Scholar
  39. 39.
    Lynch, JP, Brown, KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus. Plant Soil 237: 225–237CrossRefGoogle Scholar
  40. 40.
    Macfall, J, Slack, SA, Iyer, J (1991) Effects of Hebeloma arenosa and phosphorus fertility on growth of red pine (Pinus resinosa) seedlings. Can J Bot 69: 372–379CrossRefGoogle Scholar
  41. 41.
    Marschner, H, Römheld, V, Horst, WJ, Martin, P (1986) Root induced changes in the rhizosphere: importance for mineral nutrition of plants. Z Pflanzenernähr Bodenkd 149: 441–456CrossRefGoogle Scholar
  42. 42.
    Martino, E, Perotto, S, Parsons, R, Gadd, GM (2003) Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biochem 35: 133–141CrossRefGoogle Scholar
  43. 43.
    Meharg, AA (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107: 1253–1265CrossRefPubMedGoogle Scholar
  44. 44.
    Meharg, AA, Cairney, JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30: 69–112CrossRefGoogle Scholar
  45. 45.
    Olsen, SR, Sommers, LE (1982) Phosphorus. In: Page, AL, Miller, RH, Keeney, DR (Eds.) Methods of Soil Analysis. Part 2, Chemical and Microbiological Properties. American Society of Agronomy, Madison, USA, pp 403–429Google Scholar
  46. 46.
    Perotto, S, Martino, E (2001) Molecular and cellular mechanisms of heavy metal tolerance in mycorrhizal fungi: what perspectives for bioremediation? Minerva Biotechnol 13: 55–63Google Scholar
  47. 47.
    Peterson, RL, Chakravarty, P (1991) In: Norris, JR, Read, DJ, Varma, AK (Eds.) Techniques for Mycorrhizal Research. Academic Press, London, pp 75–105CrossRefGoogle Scholar
  48. 48.
    Sarret, G, Manceau, A, Cuny, D, Van Haluwyn, C, Deruelle, S, Hazemann, J-L, Soldo, Y, Eybert-Berard, L, Menthonnex, J-J (1998) Mechanisms of lichen resistance to metallic pollution. Environ Sci Technol 32: 3325–3330CrossRefGoogle Scholar
  49. 49.
    Sarret, G, Saumitou-Laprade, P, Bert, V, Proux, O, Hazemann, J-L, Traverse, A, Marcus, MA, Manceau, A (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130: 1815–1826CrossRefPubMedGoogle Scholar
  50. 50.
    Sarret, G, Balesdent, J, Bouziri, L, Garnier, J-M, Marcus, MA, Geoffroy, N, Panfili, F, Manceau, A (2004) Zn speciation in the organic horizon of a contaminated soil by micro-X-ray fluorescence, micro- and powder-EXAFS spectroscopy, and isotopic dilution. Environ Sci Technol 38: 2792–2801PubMedCrossRefGoogle Scholar
  51. 51.
    Sayer, JA, Raggett, SL, Gadd, GM (1995) Solubilization of insoluble compounds by soil fungi: development of a screening method for solubilizing ability and metal tolerance. Mycol Res 99: 987–993CrossRefGoogle Scholar
  52. 52.
    Sayer, JA, Cotter-Howells, JD, Watson, C, Hillier, S, Gadd, GM (1999) Lead mineral transformation by fungi. Curr Biol 9: 691–694CrossRefPubMedGoogle Scholar
  53. 53.
    Setala, H, Rissanen, J, Markkola, AM (1997) Conditional outcomes in the relationship between pine and ectomycorrhizal fungi in relation to biotic and abiotic environment. Oikos 80: 112–122CrossRefGoogle Scholar
  54. 54.
    Schwamberger, EC, Sims, JL (1991) Effect of soil pH, nitrogen source, phosphorus, and molybdenum on early growth and mineral nutrition of burley tobacco. Commun Soil Sci Plant Anal 22: 641–657CrossRefGoogle Scholar
  55. 55.
    Schachtman, DP, Reid, RJ, Ayling, SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116: 447–453CrossRefPubMedGoogle Scholar
  56. 56.
    Shetty, KG, Hetrick, BAD, Schwab, AP (1995) Effects of mycorrhizae and fertilizer amendments on zinc tolerance of plants. Environ Pollut 88: 307–314CrossRefPubMedGoogle Scholar
  57. 57.
    Sjöström, E (1993) Wood chemistry. Fundamentals and Applications. 2nd ed. Academic Press Inc. Orlando, FL, USAGoogle Scholar
  58. 58.
    Smith, FW, Rae, AL, Hawkesford, MJ (2000) Molecular mechanisms of phosphate and sulfate transport in plants. Biochim Biophys Acta 1465: 236–245PubMedCrossRefGoogle Scholar
  59. 59.
    Sundén, A, Brelid, H, Rindby, A, Engström, P (2000) Spatial distribution and modes of chemical attachment of metal ions in spruce wood. J Pulp Paper Sci 26: 352–357Google Scholar
  60. 60.
    Tibbett, M, Sanders, FE (2002) Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Ann Bot 89: 783–789CrossRefPubMedGoogle Scholar
  61. 61.
    Van Tichelen, KK, Colpaert, JV, Vangronsveld, J (2001) Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytol 150: 203–213CrossRefGoogle Scholar
  62. 62.
    Topa, MA, Cheeseman, JM (1992) Carbon and phosphorus partitioning in Pinus serotina seedlings growing under hypoxic and low-phosphorus conditions. Tree Physiol 10: 195–207PubMedGoogle Scholar
  63. 63.
    Vance, CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Plant Physiol 127: 390–397CrossRefPubMedGoogle Scholar
  64. 64.
    Vance, CP, Uhde-Stone, C, Allan, DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytol 157: 423–447CrossRefGoogle Scholar
  65. 65.
    Vodnik, D, Jentschke, G, Fritz, E, Gogala, N, Godbold, DL (1999) Root-applied cytokinin reduces lead uptake and affects its distribution in Norway spruce seedlings. Plant Physiol 106: 75–81CrossRefGoogle Scholar
  66. 66.
    Wallander, H, Wickman, T, Jacks, G (1997) Apatite as a P source in mycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Plant Soil 196: 123–131CrossRefGoogle Scholar
  67. 67.
    Whitelaw, MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69: 99–151CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Marina Fomina
    • 1
  • John M. Charnock
    • 2
  • Stephen Hillier
    • 3
  • Ian J. Alexander
    • 4
  • Geoffrey M. Gadd
    • 1
    Email author
  1. 1.Division of Environmental and Applied Biology, Biological Sciences Institute, School of Life SciencesUniversity of DundeeDundeeUK
  2. 2.SRS Daresbury Laboratory, DaresburyWarringtonUK
  3. 3.Department of Plant and Soil Science, School of Biological SciencesUniversity of AberdeenAberdeenUK
  4. 4.Macaulay Institute, CraigiebucklerAberdeenUK

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