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The effect of bacteria and fungi on chemical weathering and chemical denudation fluxes in pine growth experiments

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Abstract

Vascular plants and associated microbial communities affect the nutrient resources of terrestrial ecosystems by impacting chemical weathering that transfers elements from primary minerals to other ecosystem pools, and chemical denudation that transports weathered elements out of the system in solution. We performed a year-long replicated flow-through column growth experiment to isolate the effects of vascular plants, ectomycorrhiza-forming fungi and associated bacteria on chemical weathering and chemical denudation. The study focused on Ca2+, K+ and Mg2+, for which the sole sources were biotite and anorthite mixed into silica sand. Concentrations of the cations were measured in input and output solutions, and three times during the year in plant biomass and on exchangeable cation sites of the growth medium. Weathering and denudation fluxes were estimated by mass balance, and mineral surface changes, biofilm and microbial attachments to surfaces were investigated with scanning electron microscopy. Both bacteria and fungi increased weathering fluxes compared to abiotic controls. Without a host plant denudation rates were as large as weathering rates i.e. the weathering to denudation ratio was about one. Based on whole year fluxes, ectomycorrhizal seedlings produced the greatest weathering to denudation ratios (1.5). Non-ectomycorrhizal seedlings also showed a high ratio of 1.3. Both ectomycorrhizal hyphal networks and root hairs of non-ectomycorrhizal trees, embedded in biofilm (microorganisms surrounded by extracellular polymers), transferred nutrients to the host while drainage losses were minimized. These results suggest that biofilms localize both weathering and plant nutrient uptake, isolating the root-hypha-mineral interface from bulk soil solution.

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Abbreviations

EMF:

Ectomycorrhiza-forming fungi

References

  • Aghamiri RR, Schwartzman DW (2002) Weathering rates of bedrock by lichens: a mini watershed study. Chem Geol 188:249–259

    Article  Google Scholar 

  • Ameel J, Ruzycki E, Axler RP (1998) Analytical chemistry and quality assurance procedures for natural water samples, 6th edn. Central Analytical Laboratory, NRRI Tech Rep NRRI/TR-98/03

  • Bain DC, Mellor A, Wilson MJ, Duthie ML (1994) Chemical and mineralogical weathering rates and processes in an upland granitic till catchment in Scotland. Water Air Soil Poll 73:11–27

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Balogh Z (2006) Chemical hydrology of vascular plant growth: role of root–fungus associations. Dissertation. Washington State University, Pullman, WA

  • Balogh-Brunstad Z, Keller CK, Bormann BT, O’Brien R, Wang D, Hawley G (2008) Chemical weathering and chemical denudation dynamics through ecosystem development and disturbance. Global Biogeochem Cycles, 22, GB1007, doi:10.1029/2007GB002957

  • Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. PNAS 96:3404–3411

    Article  Google Scholar 

  • Barker WW, Welch SA, Banfield JF (1997) Biochemical weathering of silicate minerals. In: Banfield JF, Nealson KH (eds) Geomicrobiology: interactions between microbes and minerals. Rev Mineral 35:391–428

  • Barker WW, Welch SA, Chu S, Banfield JF (1998) Experimental observations of the effect of bacteria on aluminosilicate weathering. Am Mineral 83:1551–1563

    Google Scholar 

  • Bormann FH, Likens GE (1979) Pattern and process in a forested ecosystem. Springer-Verlag, New York

    Google Scholar 

  • Bormann FH, Bowden WB, Pierce RS, Hamburg SP, Voigt GK, Ingersoll RC, Likens GE (1987) The Hubbard Brook sandbox experiment. In: Jordan R, Gilpin ME, Aber JD (eds) Restoration ecology. Cambridge University Press, New York, pp 251–256

    Google Scholar 

  • Bormann BT, Wang D, Bormann FH, Benoit G, April R, Snyder MC (1998) Rapid, plant-induced weathering in an aggrading experimental ecosystem. Biogeochemistry 43:129–155

    Article  Google Scholar 

  • Bruneau AH, Lewis B (1995) Algae and moss control in turf. Publication TM-20. North Carolina Cooperative Extension Service, NCSU, Raleigh, NC. Available online. http://www.turffiles.ncsu.edu/pubs/management/tm20.html

  • Caldwell MM, Camp LB (1974) Belowground productivity [of root systems] of two cool desert communities. Oecologia 17:123–130

    Article  Google Scholar 

  • Calvaruso C, Turpault M-P, Frey-Klett P (2006) Root-associated bacteria contribute to mineral weathering and to mineral nutrition in trees: a budgeting analysis. Appl Environ Microbiol 72:1258–1266

    Article  Google Scholar 

  • Clow DW, Drever JI (1996) Weathering rates as a function of flow through an alpine soil. Chem Geol 132:131–141

    Article  Google Scholar 

  • Colpaert JV, Van Tichelen KK, Van Assche JA, Van Laere A (1999) Short-term phosphorus uptake rates in mycorrhizal and non-mycorrhizal roots of intact Pinus sylvestris seedlings. New Phytol 143:589–597

    Article  Google Scholar 

  • Crawford RH, Floyed M, Li CY (2000) Degradation of serpentine and muscovite rock minerals and immobilization of cations by soil Penicillium Spp. Phyton 40:315–322

    Google Scholar 

  • Deer WA, Howie RA, Zussman J (1992) An introduction to the rock-forming minerals, 2nd edn. Longman, London

    Google Scholar 

  • Douglas LA, Fiessinger F (1971) Degradation of clay minerals by H2O2 treatments to oxidize organic matter. Clays Clay Miner 19:67–68

    Article  Google Scholar 

  • Fernandez OA, Caldwell MM (1975) Phenology and dynamics of root growth of three cool semi-desert shrubs under field conditions. J Ecol 63:703–714

    Article  Google Scholar 

  • Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49

    Article  Google Scholar 

  • Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB (1981) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC, 523 pp

  • Ghannoum M, O’Toole G (2004) Microbial biofilms. ASM Press, Washington, DC

    Google Scholar 

  • Hayat MA (2000) Principles and techniques of electron microscopy: biological applications. Cambridge University Press, New York

    Google Scholar 

  • Hoffland E, Giesler R, Jongmans AG, Van Breemen N (2003) Feldspar tunneling by fungi along natural productivity gradients. Ecosystems 6:739–746

    Article  Google Scholar 

  • Johnson DM, Hooper PR, Conrey RM (1999) XRF analysis of rocks and minerals for major and trace elements on a single low dilution Li-tetraborate fused bead. Adv X-ray Anal 41:843–867

    Google Scholar 

  • Jongmans AG, Van Breemen N, Lundstrom 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 

  • Juhnke ME, Jardiu ED (1989) Selective medium for isolation of Xanthomonas maltophilia from soil and rhizosphere environments. Appl Environ Microbiol 55:747–750

    Google Scholar 

  • Karwowski JP, Sunga GN, Kadam S, McAlpines JB (1996) A method for selective isolation of Myxococcus directly from soil. J Ind Microbiol 16:230–236

    Article  Google Scholar 

  • Keller CK, O’Brien R, Havig JR, Smith JL, Bormann BT, Wang D (2006) Tree harvest in an experimental san ecosystem: hydrogeologic insight into nutrient cycling and solute generation processes. Ecosystems 9:634–646

    Article  Google Scholar 

  • Kelly EF, Chadwick OA, Hilinski TE (1998) The effect of plants on mineral weathering. Biogeochemistry 42:21–53

    Article  Google Scholar 

  • Koide RT, Kabir Z (2001) Nutrient economy of red pine is affected by interactions between Pisolithus tinctorius and other forest-floor microbes. New Phytol 150:179–188

    Article  Google Scholar 

  • Landeweert 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 

  • Leyval C, Berthelin J (1991) Weathering of a mica by roots and rhizospheric microorganisms of pine. Soil Sci Soc Am J 55:1009–1016

    Google Scholar 

  • Marschner H (2002) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenetic infection. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:159–163

    Google Scholar 

  • McIntosh JL (1969) Bray and Morgan soil test extractants modified for testing acid soils from different parent materials. Agronomy J 61:259–265

    Google Scholar 

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

    Google Scholar 

  • Moulton KL, West J, Berner RA (2000) Solute flux and mineral mass balance approaches to the quantification of plant effects on silicate weathering. Am J Sci 300:539–570

    Article  Google Scholar 

  • Nezat CA, Blum JD, Klaue A, Johnson CE, Siccama TG (2004) Influence of landscape position and vegetation on long-term weathering rates at Hubbard Brook Experimental Forest, New Hampshire, USA. Geochim Cosmochim Acta 68:3065–3078

    Article  Google Scholar 

  • O’Brien R, Keller CK, Strobridge DM (2004) Plant-cover effects on hydrology and pedogenesis in a sandy vadose zone. Geoderma 118:63–76

    Article  Google Scholar 

  • Paris F, Bonnaud P, Ranger J, Lapeyrie F (1995) In vitro weathering of phlogopite by ectomycorrhizal fungi I. Effect of K+ and Mg2+ deficiency on phyllosilicate evolution. Plant Soil 177:191–201

    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 

  • Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, CABI Publishing, Ottawa, Canada

    Google Scholar 

  • Richter DL, Bruhn JN (1986) Pure culture synthesis of Pinus resinosa ectomycorrhizae with Scleroderma aurantium. Mycologia 78:139–142

    Article  Google Scholar 

  • Rogers JR, Bennett PC, Choi WJ (1998) Feldspars as a source of nutrients for microorganisms. Am Mineral 83:1532–1540

    Google Scholar 

  • Rosling A, Lindahl BD, Taylor AFS, Finlay RD (2004) Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals. FEMS Microbiol Ecol 47:31–37

    Article  Google Scholar 

  • SAS Institute Inc (2004) SAS/STAT® 9.1 User’s Guide. SAS Institute Inc, Cary, NC, 5121 pp

  • Smith SE, Read DJ (1997) Mycorrhizal symbioses, 2nd edn. Academic press, San Diego, CA

    Google Scholar 

  • SW-846 EPA Method 3050B (1995) Acid digestion of sediments, sludges, and soils. In: Test methods for evaluating solid waste, 3rd edn, 3rd update. U.S. EPA, Washington, DC

  • Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (1999) Principles and applications of soil microbiology. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

  • Wallander H, Wickman T (1999) Biotite and microcline as potassium sources in ectomycorrhizal and non-ectomycorrhizal Pinus sylvestris seedlings. Mycorrhiza 9:25–32

    Article  Google Scholar 

  • White AF, Brantley SL (1995) Chemical weathering rates of silicate minerals. Reviews in mineralogy 31. Mineralogical Society of America, Washington, DC

    Google Scholar 

  • White AF, Brantley SL (2003) The effect of time on the weathering of silicate minerals: why do weathering rates differ in the laboratory and field? Chem Geol 202:479–506

    Article  Google Scholar 

  • Yamanaka T, Li CY, Bormann BT, Okabe H (2003) Tripartite associations in alder: effects of Frankia and Alpova diplophloeus and the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. Plant Soil 254:179–186

    Article  Google Scholar 

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Acknowledgments

This work was supported by NSF grant EAR-03-12011 to C. K. Keller and collaborators. We also acknowledge financial and logistical support by the Department of Crop and Soil Sciences, Electron Microscopy Center and the School of Earth and Environmental Sciences at Washington State University, the Pacific Northwest National Laboratory—Environmental Microbiological Science Laboratory in Richland, WA, and the USDA Forest Service Research, Long-Term Ecosystem Productivity program at Corvallis, OR. We are greatly thankful for the help, advice and discussions of M. Fauci, D. F. Bezdicek, E. Harwood, R. Bolton, M. Davis, J. Boyle, J. Young, B. W. Arey, C. Davitt and V. Lynch-Holm to make the experiments and analytical work possible. We are also thankful for the help of statistician Pat Cunningham. We thank the associate editor and two anonymous reviewers for their constructive comments.

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Correspondence to Z. Balogh-Brunstad.

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Balogh-Brunstad, Z., Keller, C.K., Gill, R.A. et al. The effect of bacteria and fungi on chemical weathering and chemical denudation fluxes in pine growth experiments. Biogeochemistry 88, 153–167 (2008). https://doi.org/10.1007/s10533-008-9202-y

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