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

Biogeochemistry

Volumn 111, Issue 1-3, 2012, Pages 411-425

  Saccone, Loredana ^a,c   Gazzè, Salvatore A ^a   Duran, Adele L ^b   Leake, Jonathan R ^b   Banwart, Steven A ^b   Ragnarsdóttir, Kristín Vala ^c   Smits, Mark M ^d   McMaster, Terence J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF ICELAND   (Iceland)

^d HASSELT UNIVERSITY   (Belgium)

Author keywords

AFM; Biolayer; Ectomycorrhizal fungi; Force mapping; Hyphae; Mineral weathering

Indexed keywords

ADHESION; COLONIZATION; COMPARATIVE STUDY; ECTOMYCORRHIZA; EXPERIMENTAL STUDY; FUNGUS; HYDROPHOBICITY; IMAGE ANALYSIS; SEEDLING; SYMBIOSIS;

FUNGI; PAXILLUS INVOLUTUS; PINUS SYLVESTRIS;

EID: 84873196665     PISSN: 01682563     EISSN: 1573515X     Source Type: Journal    
DOI: 10.1007/s10533-011-9667-y     Document Type: Article

References (54)

1. Alessandrini A, Facci P (2005) AFM: a versatile tool in biophysics. Meas Sci Technol 16: 65-92.
2. 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.
3. 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.
4. 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.
5. 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.
6. 2. Science 276: 544-545.
7. 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.
8. 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.
9. 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.
10. Buss HL, Brantley SL, Liermann LJ (2003) Non-destructive methods for removal of bacteria from silicate surfaces. Geomicrobiol J 20: 25-42.
11. Buss HL, Lüttge A, Brantley SL (2007) Etch pit formation on iron silicates surfaces during siderophore-promoted dissolution. Chem Geol 240: 326-342.
12. 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.
13. Deer WA, Howie RA, Zussmann J (1992) The rock-forming minerals, 2nd edn. Longman Group (FE) Limited, Hong Kong, p 696.
14. Dufrêne YF (2000) Direct characterization of the physicochemical properties of fungal spores using functionalized AFM probes. Biophys J 78: 3286-3291.
15. 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.
16. Elliot MA, Talbot NJ (2004) Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr Opin Microbiol 7: 594-601.
17. Harding MW, Marques LLR, Howard RJ, Olson ME (2009) Can filamentous fungi form biofilms? Trends Microbiol 17: 475-480.
18. 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.
19. 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.
20. 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.
21. Kaminskyj SGW, Dahms TES (2008) High spatial resolution surface imaging and analysis of fungal cells using SEM and AFM. Micron 39: 349-361.
22. 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.
23. Le Quere A, Wright DP, Soderstrom 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29: 877-896.
30. 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.
31. 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.
32. Ma H, Snook LA, Tian C, Kaminskyj SGW, Dahms TES (2006) Fungal surface remodelling visualized by atomic force microscopy. Mycol Res 110: 879-886.
33. 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.
34. 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.
35. +. Plant Soil 179: 141-150.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego.
43. Smits MM, Hoffland E, van Breemen N (2004) Contribution of mineral tunnelling to total feldspar weathering. Geoderma 125: 59-69.
44. 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.
45. Tortonese M, Kirk M (1997) Characterization of application specific probes for SPMs. P Soc Photo-Opt Ins Proc 3009: 53-60.
46. van der Aa BC, Dufrêne YF (2002) In situ characterization of bacterial extracellular polymeric substances by AFM. Colloid Surf B 23: 173-182.
47. 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.
48. 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.
49. van Schöll L, Smits MM, Hoffland E (2006) Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171: 805-814.
50. Wallander H (2000) Uptake of P from apatite by Pinus sylvestris seedlings colonized by different ectomycorrhizal fungi. Plant Soil 218: 249-256.
51. Wessels JGH (1993) Wall growth, protein excretion and morphogenesis in fungi. New Phytol 123: 397-413.
52. Wösten HAB (2001) Hydrophobins: multipurpose proteins. Ann Rev Microbiol 55: 625-646.
53. 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.
54. 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.