Skip to main content
SpringerLink
Log in

High resolution characterization of ectomycorrhizal fungal-mineral interactions in axenic microcosm experiments

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Microcosms with Pinus sylvestris seedlings in symbiosis with the fungus mycorrhizal Paxillus involutus were established, and atomic force microscopy (AFM) was used to characterise plant photosynthate-driven fungal interactions with mineral surfaces. Comparison of images of the same area of the minerals before and after mycorrhizal fungal colonization showed extensive growth of hyphae on three different mineral surfaces – hornblende, biotite and chlorite. A layer of biological exudate, or biolayer, covered the entire mineral surface and was composed of globular features of diameter 10–80 nm, and the morphology of the biolayer differed among mineral types. Similar-sized components were found on the fungal hyphae, but with a more elongated profile. Biolayer and hyphae surfaces both appeared to be hydrophobic with the hyphal surfaces yielding higher maximal adhesive interactions and a wider range of values: the mean (± SE) adhesive forces were 2.63 ± 0.03 and 3.46 ± 0.18 nN for biolayer and hypha, respectively. The highest adhesion forces are preferentially localized at the hyphal surface above the Spitzenkörper region and close to the tip, with a mean interaction force in this locality of 5.24 ± 0.49 nN. Biolayer thickness was between 10 and 40 nm. The underlying mineral was easily broken up by the tip, in contrast to the native mineral. These observations of mineral surfaces colonised by mycorrhizal fungus demonstrate how fungal hyphae are able to form a layer of organic exudates, or biolayer, and its role in hyphal attachment and potential weathering of ferromagnesian silicates, which may supply nutrients to the plant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Alessandrini A, Facci P (2005) AFM: a versatile tool in biophysics. Meas Sci Technol 16:65–92

    Article  Google Scholar 

  • Bakker MR, George E, Turpault MP, Zhang JL, Zeller B (2004) Impact of Douglas-fir and scots pine seedlings on plagioclase weathering under acidic conditions. Plant Soil 266:247–259

    Article  Google Scholar 

  • Balogh-Brunstad Z, Keller CK, Dickinson JT, Stevens F, Li CY, Bormann BT (2008a) Biotite weathering and nutrient uptake by ectomycorrhizal fungus Suillus tomentosus, in liquid-culture experiments. Geochim Cosmochim Acta 72:2601–2618

    Article  Google Scholar 

  • Balogh-Brunstad Z, Keller CK, Gill RA, Bormann BT, Li CY (2008b) The effect of bacteria and fungi on chemical weathering and chemical denudation fluxes in pine growth experiments. Biogeochemistry 88:153–167

    Article  Google Scholar 

  • Beech IB, Smith JR, Steele AA, Penegar I, Campbell SA (2002) The use of atomic force microscopy for studying interactions of bacterial biofilms with surfaces. Colloid Surf B 23:231–247

    Article  Google Scholar 

  • Berner RA (1997) Paleoclimate–The rise of plants and their effect on weathering and atmospheric CO2. Science 276:544–545

    Article  Google Scholar 

  • Blum JD, Klaue A, Nezat CA, Driscoll CT, Johnson CE, Siccama TG, Eagar C, Fahey TJ, Likens GE (2002) Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature 417:729–731

    Article  Google Scholar 

  • Bonneville S, Smits MM, Brown A, Harrington J, Leake JR, Brydson R, Benning LG (2009) Plant-driven fungal weathering: early stages of mineral alteration at the nanometer scale. Geology 37:615–618

    Article  Google Scholar 

  • Bremer PJ, Geesey GG, Drake B (1992) Atomic force microscopy of the topography of a hydrated bacterial biofilm on a copper surface. Curr Microbiol 24:223–230

    Article  Google Scholar 

  • Buss HL, Brantley SL, Liermann LJ (2003) Non-destructive methods for removal of bacteria from silicate surfaces. Geomicrobiol J 20:25–42

    Article  Google Scholar 

  • Buss HL, Lüttge A, Brantley SL (2007) Etch pit formation on iron silicates surfaces during siderophore-promoted dissolution. Chem Geol 240:326–342

    Article  Google Scholar 

  • Callow JA, Crawford SA, Higgins MJ, Mulvaney P, Wetherbee R (2000) The application of atomic force microscopy to topographical studies and force measurements on the secreted adhesive of the green alga Enteromorpha. Planta 211:641–647

    Article  Google Scholar 

  • Deer WA, Howie RA, Zussmann J (1992) The rock-forming minerals, 2nd edn. Longman Group (FE) Limited, Hong Kong, p 696

    Google Scholar 

  • Dufrêne YF (2000) Direct characterization of the physicochemical properties of fungal spores using functionalized AFM probes. Biophys J 78:3286–3291

    Article  Google Scholar 

  • Dufrêne YF, Boonaert CJP, Gerin PA, Asther M, Rouxhet PG (1999) Direct probing of the surface ultrastructure and molecular interactions of dormant and germinating spores of Phanerochaete chrysosporium. J Bacteriol 181:5350–5354

    Google Scholar 

  • Elliot MA, Talbot NJ (2004) Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr Opin Microbiol 7:594–601

    Article  Google Scholar 

  • Harding MW, Marques LLR, Howard RJ, Olson ME (2009) Can filamentous fungi form biofilms? Trends Microbiol 17:475–480

    Article  Google Scholar 

  • Higgins MJ, Crawford SA, Mulvaney P, Wetherbee R (2002) Characterization of the adhesive mucilages secreted by live diatom cells using atomic force microscopy. Protist 153:25–38

    Article  Google Scholar 

  • Hoffland E, Giesler R, Jongmans AG, van Breemen N (2002) Increasing feldspar tunnelling by fungi across a Mid-Sweden podzol chronosequence. Ecosystems 5:11–22

    Article  Google Scholar 

  • Jongmans AG, Van Breemen N, Lundström U, Van Hees PAW, Finlay RD, Srinivasan M, Unestam T, Giesler R, Melkerud P-A, Olsson M (1997) Rock-eating fungi. Nature 389:682–683

    Article  Google Scholar 

  • Kaminskyj SGW, Dahms TES (2008) High spatial resolution surface imaging and analysis of fungal cells using SEM and AFM. Micron 39:349–361

    Article  Google Scholar 

  • Landerweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254

    Article  Google Scholar 

  • Le Quéré A, Wright DP, Söderström B, Tunlid A, Johansson T (2005) Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula Roth.) and P. involutus (Batsch) Fr APS 18:659–673

  • Leake JR, Read DJ (1997) Mycorrhizal fungi in terrestrial habitats. In: Wicklow DT, Söderström B (eds) The mycota. Environmental and microbial relationships. Springer Verlag, Berlin, pp 281–301

    Google Scholar 

  • Leake JR, Johnson D, Donnelly D, Muckle GE, Boddy L, Read DJ (2004) Networks of power and influence: The role of mycorrhizal mycelium in controlling plant communities and agro-ecosystem functioning. Can J Botany 82:1016–1045

    Article  Google Scholar 

  • Leake JR, Duran AL, Hardy KE, Johnson I, Beerling DJ, Banwart SA, Smits MM (2008) Biological weathering in soil: the role of symbiotic root-associated fungi biosensing minerals and directing photosynthate-energy into grain-scale mineral weathering. Mineral Mag 72:85–89

    Article  Google Scholar 

  • Leake JR, Duran AL, Johnson I, Bonneville S, Smits MM (2009) Hydroxyapatite weathering by pine mycorrhizas – the role of oxalic acid. Geochim Cosmochim Acta 73:A732

    Google Scholar 

  • Lee CK, Wang YM, Huang LS, Lin S (2007) Atomic force microscopy: determination of unbinding force, off-rate and energy barrier for protein–ligand interaction. Micron 38:446–461

    Article  Google Scholar 

  • Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877–896

    Article  Google Scholar 

  • Lo Y-S, Huefner ND, Chan WS, Dryden P, Hagenhoff B, Beebe TP (1999) Organic and inorganic contamination on commercial AFM cantilevers. Langmuir 15:6522–6526

    Article  Google Scholar 

  • Ma H, Snook LA, Kaminskyj SGW, Dahms TES (2005) Surface ultrastructure and elasticity in growing tips and mature regions of Aspergillus hyphae describe wall maturation. Microbiol-SMG 151:3679–3688

    Article  Google Scholar 

  • Ma H, Snook LA, Tian C, Kaminskyj SGW, Dahms TES (2006) Fungal surface remodelling visualized by atomic force microscopy. Mycol Res 110:879–886

    Article  Google Scholar 

  • McMaster TJ, Smits MM, Harvard SJ, Leake JR, Banwart SA, Ragnarsdottir KV (2008) High-resolution imaging of biotite dissolution and measurement of activation energy. Mineral Mag 72:115–120

    Article  Google Scholar 

  • Mikutta R, Kleber M, Kaiser K, Jahn R (2005) Review: organic matter removal from soils using hydrogen peroxide, sodium hypochlorite, and disodium peroxodisulfate. Soil Sci Soc Am J 69:120–135

    Article  Google Scholar 

  • Paris F, Botton B, Lapeyrie F (1996) In vitro weathering of phlogopite by ectomycorrhizal fungi.II. Effect of K+ and Mg2+ deficiency and N sources on accumulation of oxalate and H+. Plant Soil 179:141–150

    Article  Google Scholar 

  • Rajashekar B, Samson P, Johansson T, Tunlid A (2007) Evolution of nucleotide sequences and expression patterns of hydrophobin genes in the ectomycorrhizal fungus P. involutus. New Phytol 174:399–411

    Article  Google Scholar 

  • Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Botany 82:1243–1263

    Article  Google Scholar 

  • Saccone L, Gazze SA, Ragnarsdottir KV, Leake JR, Duran AL, Hallam KR, McMaster TJ (2009) P. involutus hyphae: imaging their structure and interaction with mineral surfaces using AFM. Geochim Cosmochim Acta 73:A1140

    Google Scholar 

  • Schmalenberger A, Duran AL, Leake JR, Romero-Gonzales ME, Banwart SA (2009) Mineralogy controls oxalic acid release in mycorrhizal weathering. Geochim Cosmochim Acta 73:A1177

    Google Scholar 

  • Schmitz I, Schreiner M, Friedbacher G, Grasserbauer M (1997) Phase imaging as an extension to tapping mode AFM for the identification of material properties on humidity-sensitive surfaces. Appl Surf Sci 115:190–198

    Article  Google Scholar 

  • Sirghi L, Kylián O, Gilliland D, Ceccone G, Rossi F (2006) Cleaning and hydrophilization of atomic force microscopy silicon probes. J Phys Chem 110:25975–25981

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Smits MM, Hoffland E, van Breemen N (2004) Contribution of mineral tunnelling to total feldspar weathering. Geoderma 125:59–69

    Article  Google Scholar 

  • Taylor LL, Leake JR, Quirk J, Hardy K, Banwart SA, Beerling DJ (2009) Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiol 7:171–191

    Article  Google Scholar 

  • Tortonese M, Kirk M (1997) Characterization of application specific probes for SPMs. P Soc Photo-Opt Ins Proc 3009:53–60

    Google Scholar 

  • Van der Aa BC, Dufrêne YF (2002) In situ characterization of bacterial extracellular polymeric substances by AFM. Colloid Surf B 23:173–182

    Article  Google Scholar 

  • Van Hees PAW, Godbold DL, Jentschke G, Jones DL (2003) Impact of ectomycorrhizas on the concentration and biodegradation of simple organic acids in a forest soil. Eur J Soil Sci 54:697–706

    Article  Google Scholar 

  • Van Hees PAW, Jones DL, Jentschke G, Godbold DL (2004) Mobilization of aluminium, iron and silicon by Picea abies and ectomycorrhizas in a forest soil. Eur J Soil Sci 55:101–111

    Article  Google Scholar 

  • Van Schöll L, Smits MM, Hoffland E (2006) Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171:805–814

    Article  Google Scholar 

  • Wallander H (2000) Uptake of P from apatite by Pinus sylvestris seedlings colonized by different ectomycorrhizal fungi. Plant Soil 218:249–256

    Article  Google Scholar 

  • Wessels JGH (1993) Wall growth, protein excretion and morphogenesis in fungi. New Phytol 123:397–413

    Article  Google Scholar 

  • Wösten HAB (2001) Hydrophobins: multipurpose proteins. Ann Rev Microbiol 55:625–646

    Article  Google Scholar 

  • Wösten HAB, de Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5:1567–1574

    Google Scholar 

  • Zhong Q, Inniss D, Kjoller K, Elings VB (1993) Fractured polymer silica fibre surface studied by tapping mode atomic force microscopy. Surf Sci 290:688–692

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the Natural Environment Research Council (NERC), consortium grant no NE/C521044/1, and is part of the Weathering Science Consortium (WSC) project on mineral weathering. This research project closely collaborates with MISSION ‘Mineral Surface Science for Nanotechnology’, a Marie Curie Early Stage Training Scheme (MEST-CT-2005-020828).

Author information

Authors and Affiliations

  1. H.H. Wills Physics Laboratory, University of Bristol, Tyndall Avenue, Bristol, BS8 1TL, UK

    Loredana Saccone, Salvatore A. Gazzè & Terence J. McMaster

  2. Department of Animal and Plant Sciences, Alfred Denny Building, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK

    Adele L. Duran & Jonathan R. Leake

  3. Department of Civil and Structural Engineering, Kroto Research Institute, North Campus, University of Sheffield, Broad Lane, Sheffield, S3 7HQ, UK

    Steven A. Banwart

  4. Faculty of Earth Sciences, School of Engineering and Natural Sciences, University of Iceland, Askja, 107, Reykjavik, Iceland

    Loredana Saccone & Kristín Vala Ragnarsdóttir

  5. Environmental Biology, Hasselt University, Campus Diepenbeek, Agoralaan – Gebouw D, 3590, Diepenbeek, Belgium

    Mark M. Smits

Authors
  1. Loredana Saccone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Salvatore A. Gazzè
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adele L. Duran
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan R. Leake
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Steven A. Banwart
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kristín Vala Ragnarsdóttir
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mark M. Smits
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Terence J. McMaster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Terence J. McMaster.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saccone, L., Gazzè, S.A., Duran, A.L. et al. High resolution characterization of ectomycorrhizal fungal-mineral interactions in axenic microcosm experiments. Biogeochemistry 111, 411–425 (2012). https://doi.org/10.1007/s10533-011-9667-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-011-9667-y

Keywords

Search

Navigation