Biogeochemistry

, Volume 49, Issue 1, pp 53–67 | Cite as

Mycorrhizal weathering: A true case of mineral plant nutrition?

  • Nico van Breemen
  • Roger Finlay
  • Ulla Lundström
  • Antoine G. Jongmans
  • Reiner Giesler
  • Mats Olsson
Article

Abstract

Weatherable minerals in all podzol surface soils andshallow granitic rock under European coniferousforests studied hitherto are criss-crossed bynumerous open, tubular pores, 3–10 µm in width. Wehypothesize that these pores were formed bycomplex-forming, low-molecular weight organic acidsexuded by or formed in association with mycorrhizalfungi. It is well known that ectomycorrhizal myceliumrepresents a greatly extended, and better distributed,surface area for the absorption of nutrients. However, there have been few investigations of how thewhereabouts of individual hypha affect nutrientuptake. The results presented here provide directevidence that the mycelium is able to penetrate, andmost probably create, microsites which areinaccessible to plant roots and isolated from bulksoil solution phenomena. Dissolved products could betranslocated to the host plant roots, bypassing thesoil solution with often toxic concentration ofAl3+ from acid rain, and bypassing competitionfor nutrient uptake by other organisms. Furthermore,there is strong evidence that ``rock-eating''mycorrhizal fungi play a role in the formation ofpodzol E horizons. The partly speculativeinterpretations presented here challenge conventionalideas about (1) the importance of nutrient uptakefrom the bulk soil solution (2) criteria for criticalloads of acid atmospheric deposition for forests, and(3) the process of podzolization.

acidification Al3+ toxicity coniferous trees ectomycorrhiza microbiological weathering podzolization 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bååth E (1980) Soil fungal biomass after clear-cutting of a pine forest in central Sweden. Soil Biol. & Biochem. 12: 495–500Google Scholar
  2. Bååth E, Lundgren B & Söderström B (1984) Fungal populations in podzolic soil experimentally acidified to simulate acid rain. Microbial. Ecology 10: 197–203Google Scholar
  3. BarkerWW, Welch SA & Banfield JF (1997) Biogeochemical weathering of silicate minerals. In: Banfield JF and Nealson KH (Eds) G Interactions between Microbes and Minerals (pp 391–429). Reviews in Mineralogy, Vol. 35. Mineralogical Soc. America, Washington DC, U.S.A.Google Scholar
  4. Björkman E (1949) The ecological significance of ectotrophic mycorrhizal associations in forest trees. Svensk Botanisk Tidskrift 38: 1–14Google Scholar
  5. Blum AE & Stillings LL (1995) Chemical weathering rates of silicate minerals. In White AF & Brantley SL (Eds) Reviews in Mineralogy, Vol 31(pp 291–551). Mineralogical Soc. Amer., Washington DC, U.S.A.Google Scholar
  6. Boyle JR & Voigt GK (1973) Biological weathering of silicate minerals, implications for tree nutrition and soil genesis. Plant & Soil 38: 191–201Google Scholar
  7. Van Breemen N, Lundström US & Jongmans AG (submitted) Do plants drive podzolization via rock-eating ectomycorrhizal fungi? GeodermaGoogle Scholar
  8. Bruckert S (1970) Influence des composJs organiques solubles sur la pédogénèse en milieu acide. I. Etudes de terrain. Annales Agronomiques 21: 421–452Google Scholar
  9. Callot G, Maurette M, Pottier L & Dubois A (1987) Biogenic etching of microfeatures in amorphous and crystalline silicates. Nature 328: 147–149Google Scholar
  10. Cromack Jr K, Sollins P, Graustein WC, Speidel K, Todd AW, Spycher G, Li CY & Todd, RL (1979) Calcium oxalate accumulations and soil weathering in mats of the hypogeous fungus Hysterangium crassum. Soil Biol. Biochem. 11: 463–468CrossRefGoogle Scholar
  11. Degermark C (1995) Climate and chemistry of water. Reference measurement 1986–1995, SLU, Vindels Expt St., Vindels, Sweden [In Swedish]Google Scholar
  12. Devêvre O, Garbaye J and Botton B (1996) Release of complexing organic acids by rhizosphere fungi as a factor in Norway spruce yellowing in acidic soils. Mycol. Res. 100: 1367–1374Google Scholar
  13. El Gibaly MH, El Reweiny FM, Abdel-Nasser M & El Dahtory TA (1997) Studies of phosphate-solubilizing bacteria in soil rhizosphere of different plants. Occurrence of bacterial acid producers and phosphate dissolvers. Zentralbl. Bakt. Parasit. Infek. Hyg. 132: 233–239Google Scholar
  14. Entry JA, Rose CL & Cromack K Jr (1991) Litter decomposition and nutrient release in ectomycorrhizal mat soils of a Douglas fir ecosystem. Soil Biol. Biochem. 23: 185–290Google Scholar
  15. Falkengren-Grerup U & Eriksson H (1990) Changes in soil, vegetation and forest yield between 1947 and 1988 in beech and oak sites of southern Sweden. For. Ecol. Manege. 38: 37–53Google Scholar
  16. Finlay RD (1993) in Mycorrhiza in Ecosystems. In Read DJ, Lewis DH, Fitter AH & Alexander IJ (Eds) Proceedings 3rd European Symposium on Mycorrhizas, CAB International (pp 91–97)Google Scholar
  17. Fitzpatrick EA (1970) A technique for the preparation of large thin sections of soils and consolidated material. In DA Osmond & P. Bullock (ed.) Micromorphological Techniques and Application (pp 3–13). Tech. Monogr. 2. Soil Survey of England and Wales, Rotthamsted Exp. Stn. HarpendenGoogle Scholar
  18. Frey P, Frey-Klett P, Garbaye J, Berge O and Heulin T (1997) Metabolic and genotypic fingerprinting of fluorescent pseudomonads associated with the Douglas fir Laccaria bicolor mycorrhizosphere. Appl. and Environ. Microbiol. 63: 1852–1860Google Scholar
  19. Frey-Klett P, Pierrat JC & Garbaye J (1997) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Applied and Environmental Microbiology 63: 139–144Google Scholar
  20. Giesler R, Ilvesniemi H, Nyberg L, van Hees P, Starr M, Bishop K, Kareinen T & Lundström US (in press) Distribution and mobilization of Al, Fe and Si in three podzolic soil profiles in relation to the humus layer. GeodermaGoogle Scholar
  21. Giesler R & Lundström US (1993) Soil solution chemistry: effect of bulking soil samples. Soil Sci. Soc. Am. J. 57: 1283–1288Google Scholar
  22. Graustein WC, Cromack K Jr & Sollins P (1977) Calcium oxalate: occurrence in soils and effect on nutrient and geochemical cycles. Science 198: 1252–1254Google Scholar
  23. Griffiths RP, Baham JE & Caldwell BA (1994) Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biol. Biochem. 26: 331–337CrossRefGoogle Scholar
  24. Van Hees PAW, Dahlen J, Lundström US, Borén H & Allard B (in press) Determination of low molecular weight organic acids in soil solution by HPLC. Talanta 48: 173–179Google Scholar
  25. Van Hees PAW, Lundström US & Giesler R (in press) Low molecular weight acids and their Al-complexes in soil solutions-Composition, distribution and seasonal variation in three podzolized soils. GeodermaGoogle Scholar
  26. Jongmans AG, Van Breemen N, Lundström US, Van Hees PAW, Finlay RD, Srinivasan M, Unestam T, Giesler R, Melkerud P-A & Olsson M (1997) Rock-eating fungi. Nature 389: 682–683CrossRefGoogle Scholar
  27. Kauppi PE, Meilikainen K, & Kuusela K (1992). Biomass and carbon budget of European forests. Science 256: 70–74Google Scholar
  28. Kubin E (1983) Nutrients in the soil, ground vegetation and tree layer in an old spruce forest in Northern Finland. Ann. Bot. Finn. 20: 361–390Google Scholar
  29. Lawrence GB & David MB (1996) Chemical evaluation of soil-solution in acid forest soils. Soil Science 161: 298–313Google Scholar
  30. Leyval C & Berthelin J (1991) Weathering of a mica by roots and rhizospheric microorganisms of pine Soil Sci. Soc. Am. J. 55: 1009–1016Google Scholar
  31. Lundström US (1993) The role of organic acids in the solution chemistry of a podzolized soil. J. Soil Sci. 41: 359–369Google Scholar
  32. Lundström US, Van Breemen N & Jongmans AG (1995) Evidence for microbial decomposition of organic acids during podzolization. Eur. J. Soil Sci. 46: 489–496Google Scholar
  33. Markewitz D & Richter DD (1997) The bio in aluminium and silicon geochemistry. Biogeochemistry 42: 235–252Google Scholar
  34. Melkerud P-A (1989) Weathering; its products and deposits. In Augustithis SS (Ed.) (pp 307–305). Theoophrastus Publ., S.A. Athens, GreeceGoogle Scholar
  35. Mikola P, Hahl J & Torniainen E (1966) Vertical distribution of mycorrhizae in pine forests with spruce undergrowth. Ann. Bot. Fenn. 3: 406–409Google Scholar
  36. Mulder J, Van Breemen N & van Eijck HC (1989) Depletion of soil aluminium by acid deposition and implications for acid neutralization. Nature 337: 247–249Google Scholar
  37. Nickel E (1973) Experimental dissolution of light and heavy minerals in comparison with weathering and intrastitial solution. Contrib. Sediment 1: 1–68Google Scholar
  38. Posch M, Hettelingh J-P, de Smet PAM & Downing RJ (1997) Calculation and mapping of critical thresholds in Europe. CCE Status Report 1997 RIVMN, National Institute of Public Health and the Environment, Bilthoven, the NetherlandsGoogle Scholar
  39. Van Reeuwijk LP (1995) Procedures for soil analysis. Techn. Paper 7. International Soil Reference and Information Centre, Wageningen, The NetherlandsGoogle Scholar
  40. Robert M & Berthelin J (1986) Role of biological and biochemical factors in soil mineral weathering. In Huang PM & Schnitzer M (Eds) Interactions of Soil Minerals with Natural Organics and Microbes (pp 453–495). SSSA Special Publ. No. 17, Soil Sci. Soc. Amer., Inc., Madison, WisconsinGoogle Scholar
  41. Rost-Siebert K (1985) Untersuchungen zur H-und Al Ionentoxizität an Keimpflanzen von Fichte (Picea abies, Karst.) und Buche (Fagus sylvatica L.) in Lösungskultur. Berichte Forschungszentrum Waldökosysteme/ Waldsterben, Göttingen, Germany, Vol. 12Google Scholar
  42. Rustad LE & Cronan CS (1995) Biogeochemical controls on aluminum chemistry in the O horizon of a red spruce (Picea rubens Sarg.) stand in central Maine, U.S.A. Biogeochemistry 29: 107–129Google Scholar
  43. Schützel H, Kutschke D & Wildner G (1963) Zur Problematik der Genese Grauen Gneise des Sächsischen Erzgebirges (Zirkonstatistische Untersuchungen) (pp 1–65). Freiberger Forschungshefte C159, MineralogieGoogle Scholar
  44. Smith SE & Read DJ (1997) Mycorrhizal Symbiosis, 2nd edn. Academic PressGoogle Scholar
  45. Söderström B (1977) Vital staining of fungi in pure cultures and in soil with fluorescein diacetate. Soil Biol. Biochem. 9: 59–63Google Scholar
  46. Söderström BE (1979) Seasonal fluctuations of active fungal biomass in horizons of a podzolized pine-forest soil in central Sweden. Soil Biol. Biochem. 11: 149–154Google Scholar
  47. Staaf H, Persson T & Bertills U (ed) (1996) Skogsmarkskalkning Report No. 4559, Swedish Environmental Protection Agency, StockholmGoogle Scholar
  48. Sun Y-P, Unestam T, Lucas SD, Johanson KJ, Kenne KJ & Finlay R (1999) Exudationreabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and other microorganisms. Mycorrhiza 00: 000–000Google Scholar
  49. Sverdrup H & de Vries W (1994) Calculating critical loads for acidity with the simple mass balance method. Water Air and Soil Pollution 72: 143–162Google Scholar
  50. De Vries, W, Reinds GL & Posch M (1994) Assessment of critical loads and their exceedance on European forests using a one-layer steady-state model. Water Air and Soil Poll. 72: 357–394Google Scholar
  51. Wallander H, Wickman T & Jacks G (1997) Apatite as a source of mycorrhizal and nonmycorrhizal Pinus sylvestris. Plant & Soil 196: 123–131Google Scholar
  52. Wesselink LG (1994) Time Trends and Mechanisms of Soil Acidification. PhD Dissertation, Wageningen Agricultural University, The NetherlandsGoogle Scholar
  53. Wickman T & Wallander H (1996) Biotite or microcline as a potassium source in ectomycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. In “Weathering assessment and nutrient availability in coniferous forests”, PhD Thesis, Royal Inst Techn.Google Scholar
  54. Zak DR and Pregitzer KS (1998) Integration of ecophysiological and biogeochemical approaches to ecosystem dynamics. In Pace ML & Groffman PM (Eds) Successes, Limitations and Frontiers in Ecosystem Science (pp 372–403). Springer, New YorkGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Nico van Breemen
    • 1
  • Roger Finlay
    • 2
  • Ulla Lundström
    • 3
  • Antoine G. Jongmans
    • 1
  • Reiner Giesler
    • 4
  • Mats Olsson
    • 5
  1. 1.Department of Soil Science and GeologyWAUWageningenThe Netherlands
  2. 2.Department of Forest Mycology and PathologySLUUppsalaSweden
  3. 3.Department of Chemistry and Process TechnologyMid Sweden UniversitySundsvallSweden
  4. 4.Department of Forest EcologySLUUmeåSweden
  5. 5.Department of Forest SoilsSLUUppsalaSweden

Personalised recommendations