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Introduction


Rocks are the primary source of all plant nutrients, except nitrogen. These nutrients are bound into a variety of crystalline structures (minerals). Minerals are either formed during rock formation from magma (primary mineral) or formed during soil formation (secondary minerals). Secondary minerals are formed when the local soil solution is saturated in respect to that mineral. In contrast to secondary minerals, for primary minerals are formed in  the soil solution is generally undersaturated, causing earth mantle at high temperature and pressure. At the earth surface  these minerals to dissolve. But this may be thermodynamically unstable. Here, in interaction with water, they either dissolve complete (congruent dissolution) or partly dissolve leaving a solid residue like clay minerals (incongruent dissolution). This  dissolution process is extremely slow for most minerals. It has been estimated that it takes more than 30 million years to dissolve a 1 mm diameter quartz grain under natural soil conditions conditions   class="ltx_cite" data-bib-text="@article{Lasaga_1984, doi = {10.1029/jb089ib06p04009},  url = {http://dx.doi.org/10.1029/jb089ib06p04009},  year = 1984, 

author = {Antonio C. Lasaga},  title = {Chemical kinetics of water-rock interactions},  journal = {J. Geophys. Res.}  }" data-bib-key="Lasaga_1984" contenteditable="false">Lasaga 1984. Nonetheless, soil mineral weathering provides an essential input of plant nutrients into ecosystems, avoiding or delaying nutrient limitations limitations   class="ltx_cite" data-bib-text="@article{Chadwick_1999, doi = {10.1038/17276},  url = {http://dx.doi.org/10.1038/17276},  year = 1999, 

pages = {491--497},  author = {O. A. Chadwick and L. A. Derry and P. M. Vitousek and B. J. Huebert and L. O. Hedin},  journal = {Nature}  }" data-bib-key="Chadwick_1999" contenteditable="false">Chadwick 1999.

In addition, mineral weathering produces cations that counteract soil acidification, thereby improving the availability of most plant nutrients nutrients  class="ltx_cite" data-bib-text="@article{van_Breemen_1983, doi = {10.1007/bf02369968},  url = {http://dx.doi.org/10.1007/bf02369968},  year = 1983, 

author = {N. van Breemen and J. Mulder and C. T. Driscoll},  title = {Acidification and alkalinization of soils},  journal = {Plant Soil}  }" data-bib-key="van_Breemen_1983" contenteditable="false">Breemen 1983. Also clays are formed as a weathering product of feldspars and micas micas  class="ltx_cite" data-bib-text="@article{Oades_1988, doi = {10.1007/bf02180317},  url = {http://dx.doi.org/10.1007/bf02180317},  year = 1988, 

author = {J. M. Oades},  title = {The retention of organic matter in soils},  journal = {Biogeochemistry}  }" data-bib-key="Oades_1988" contenteditable="false">Oades 1988. Clay particles contribute, with their negative charged surfaces, to the cation exchange capacity (CEC) of the soil, reducing the leaching of positively charged nutrients like K+ and NH4+. Clay content correlates positively with water holding capacity and soil organic matter (SOM) content content  class="ltx_cite" data-bib-text="@article{Sollins_1996, doi = {10.1016/s0016-7061(96)00036-5},  url = {http://dx.doi.org/10.1016/s0016-7061(96)00036-5},  year = 1996, 

author = {Phillip Sollins and Peter Homann and Bruce A. Caldwell},  title = {Stabilization and destabilization of soil organic matter: mechanisms and controls},  journal = {Geoderma}  }" data-bib-key="Sollins_1996" contenteditable="false">Sollins 1996.

Moreover, the weathering of Ca- and Mag-silicate minerals play a central role in the global carbon cycle. The Ca and Mg, released by the weathering process, will be locked up as carbonates in marine sediments sediments  class="ltx_cite" data-bib-text="@article{sundquist1985geological, title={Geological perspectives on carbon dioxide and the carbon cycle},  author={Sundquist, Eric T},  journal={The Carbon Cycle and Atmospheric CO: Natural Variations Archean to Present},  pages={55--59},  year={1985},  publisher={Wiley Online Library}  }" data-bib-key="sundquist1985geological" contenteditable="false">Sundquist 1985. On the long-term, atmospheric CO2 is regulated by the weathering rates of these minerals, which is influenced by climate and mountain uplift uplift  class="ltx_cite" data-bib-text="@article{Berner_2003, doi = {10.1038/nature02131},  url = {http://dx.doi.org/10.1038/nature02131},  year = 2003, 

title = {The long-term carbon cycle,  fossil fuels and atmospheric composition},  journal = {Nature}  }" data-bib-key="Berner_2003" contenteditable="false">Berner 2003    class="ltx_cite" data-bib-text="@article{Raymo_1992, doi = {10.1038/359117a0},  url = {http://dx.doi.org/10.1038/359117a0},  year = 1992, 

author = {M. E. Raymo and W. F. Ruddiman},  title = {Tectonic forcing of late Cenozoic climate},  journal = {Nature}  }" data-bib-key="Raymo_1992" contenteditable="false">Raymo 1992.

The vast amounts of nutrients locked in soil minerals has triggered, nearly 100 years ago, the question if plants actively enter this potential nutrient source    class="ltx_cite" data-bib-text="@article{HALEY_1923, doi = {10.1097/00010694-192303000-00002},  url = {http://dx.doi.org/10.1097/00010694-192303000-00002},  year = 1923, 

author = {DENNIS EDWARD HALEY},  title = {{AVAILABILITY} {OF} {POTASSIUM} {IN} {ORTHOCLASE} {FOR} {PLANT} {NUTRITION}},  journal = {Soil Science}  }" data-bib-key="HALEY_1923" contenteditable="false">HALEY 1923    class="ltx_cite" data-bib-text="@article{TURK_1919, doi = {10.1097/00010694-191910000-00001},  url = {http://dx.doi.org/10.1097/00010694-191910000-00001},  year = 1919, 

author = {ERNEST DE TURK},  title = {{POTASSIUM}-{BEARING} {MINERALS} {AS} A {SOURCE} {OF} {POTASSIUM} {FOR} {PLANT} {GROWTH}},  journal = {Soil Science}  }" data-bib-key="TURK_1919" contenteditable="false">TURK 1919. Five decennia later, studies appear on the role of microorganisms, including mycorrhizal fungi, in mineral weathering    class="ltx_cite" data-bib-text="@article{WEBLEY_1963, doi = {10.1111/j.1365-2389.1963.tb00935.x},  url = {http://dx.doi.org/10.1111/j.1365-2389.1963.tb00935.x},  year = 1963, 

author = {R. B. DUFF and D. M. WEBLEY and R. O. SCOTT},  title = {{SOLUBILIZATION} {OF} {MINERALS} {AND} {RELATED} {MATERIALS} {BY} 2-{KETOGLUCONIC} {ACID}-{PRODUCING} {BACTERIA}},  journal = {Soil Science}  }" data-bib-key="DUFF_1963" contenteditable="false">DUFF 1963    class="ltx_cite" data-bib-text="@article{Sperber_1958, doi = {10.1071/ar9580778},  url = {http://dx.doi.org/10.1071/ar9580778},  year = 1958, 

author = {JI Sperber},  title = {The incidence of apatite-solubilizing organisms in the rhizosphere and soil},  journal = {Aust. J. Agric. Res.}  }" data-bib-key="Sperber_1958" contenteditable="false">Sperber 1958    class="ltx_cite" data-bib-text="@article{Boyle_1967, doi = {10.1126/science.155.3759.193},  url = {http://dx.doi.org/10.1126/science.155.3759.193},  year = 1967, 

author = {J. R. Boyle and G. K. Voigt and B. L. Sawhney},  title = {Biotite Flakes: Alteration by Chemical and Biological Treatment},  journal = {Science}  }" data-bib-key="Boyle_1967" contenteditable="false">Boyle 1967    class="ltx_cite" data-bib-text="@article{Boyle_1973, doi = {10.1007/bf00011226},  url = {http://dx.doi.org/10.1007/bf00011226},  year = 1973, 

author = {J. R. Boyle and G. K. Voigt},  title = {Biological weathering of silicate minerals},  journal = {Plant Soil}  }" data-bib-key="Boyle_1973" contenteditable="false">Boyle 1973. More recently, a publication with the provocative title Rock eating fungi appeared in Nature    class="ltx_cite" data-bib-text="@article{Jongmans_1997, doi = {10.1038/39493},  url = {http://dx.doi.org/10.1038/39493},  year = 1997, 

pages = {682--683},  author = {A. G. Jongmans and N. van Breemen and U. Lundström and P. A. W. van Hees and R. D. Finlay and M. Srinivasan and T. Unestam and R. Giesler and P.-A. Melkerud and M. Olsson},  journal = {Nature}  }" data-bib-key="Jongmans_1997" contenteditable="false">Jongmans 1997. This publication presented evidence of, presumably mycorrhizal, fungal hyphae drilling their way (chemically and/or physically) into feldspar grains. This paper initiated renewed interest into the topic. A series of reviews has been published since then, covering the research up to 2009    class="ltx_cite" data-bib-text="@article{Finlay_2009, doi = {10.1016/j.fbr.2010.03.002},  url = {http://dx.doi.org/10.1016/j.fbr.2010.03.002},  year = 2009, 

author = {Roger Finlay and Hakan Wallander and Mark Smits and Sara Holmstrom and Patrick van Hees and Bin Lian and Anna Rosling},  title = {The role of fungi in biogenic weathering in boreal forest soils},  journal = {Fungal Biology Reviews}  }" data-bib-key="Finlay_2009" contenteditable="false">Finlay 2009    class="ltx_cite" data-bib-text="@article{Hoffland_2004, doi = {10.1890/1540-9295(2004)002[0258:trofiw]2.0.co;2},  url = {http://dx.doi.org/10.1890/1540-9295(2004)002[0258:trofiw]2.0.co;2},  year = 2004, 

author = {Ellis Hoffland and Thomas W. Kuyper and H{\aa}kan Wallander and Claude Plassard and Anna A. Gorbushina and Kurt Haselwandter and Sara Holmström and Renske Landeweert and Ulla S. Lundström and Anna Rosling and Robin Sen and Mark M. Smits and Patrick AW van Hees and Nico van Breemen},  title = {The role of fungi in weathering},  journal = {Frontiers in Ecology and the Environment}  }" data-bib-key="Hoffland_2004" contenteditable="false">Hoffland 2004    class="ltx_cite" data-bib-text="@article{Landeweert_2001, doi = {10.1016/s0169-5347(01)02122-x},  url = {http://dx.doi.org/10.1016/s0169-5347(01)02122-x},  year = 2001, 

author = {Renske Landeweert and Ellis Hoffland and Roger D. Finlay and Thom W. Kuyper and Nico van Breemen},  title = {Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals},  journal = {Trends in Ecology {\&} Evolution}  }" data-bib-key="Landeweert_2001" contenteditable="false">Landeweert 2001.

Since 2009, more evidence of mycorrhizal weathering has been published, based on in vitro and microcosm based research. A new aspect is the effect of the arise of different types of mycorrhizal fungi during the evolution of land plants on mineral weathering rates, and thus the global carbon cycle. The gap between laboratory based studies and the real world has been bridged by a number of field based studied and mathematical modeling. So far, evidence of a substantial role of mycorrhizal fungi on soil mineral weathering has been missing, while modeling studies show contrasting results.

In this book chapter we briefly introduce the basics of physical and chemical weathering mechanisms, as insight in these mechanisms is of vital importance in the interpretation of results from laboratory based experiments and modeling studies. Next, we give an overview of the recent literature on this topic, and set their results in perspective with the current knowledge on mineral dissolution kinetics.

Mechanisms of mineral weathering

The most visible aspect of weathering is the break up of rocks and minerals into smaller fragments. This so called physical weathering acts on all scales, from the erosion of complete mountain tops to micrometer scale cracks in mineral crystals. Well known mechanisms of physical weathering are thermal stress and mechanical force by freezing water and penetrating tree roots. but also fungal hyphae, colonizing cracks and voids in mineral grains, can produce mechanical force. They can build up high osmotic pressure in their tissues (up to 20 &microN &microm⁻¹). This is enough pressure to penetrate bullet proof material    class="ltx_cite" data-bib-text="@article{Howard_1991, doi = {10.1073/pnas.88.24.11281},  url = {http://dx.doi.org/10.1073/pnas.88.24.11281},  year = 1991, 

author = {R. J. Howard and M. A. Ferrari and D. H. Roach and N. P. Money},  title = {Penetration of hard substrates by a fungus employing enormous turgor pressures.},  journal = {Proceedings of the National Academy of Sciences}  }" data-bib-key="Howard_1991" contenteditable="false">Howard 1991, and also to widen existing cracks in mineral grains and rock fragments. The results of physical weathering is an increase in mineral surface area exposed to the soil solution.

Less visible is the chemical alteration or dissolution of minerals. Although in principle most primary minerals dissolve in soil solution, certain compounds accelerate the process. The most common, and by far quantitatively most important weathering agents are protons. Protons, and also hydroxide under alkaline conditions, attack the ion bindings in the mineral crystal lattice. This process is called hydrolysis (or carbonation when carbonic acid is the main proton donor). Biotic processes have a strong influence on the soil solution pH via the exudation of protons in exchange of positively charges nutrients as NH4+ and K+, the exudation of organic acids and the release of CO2 into the soil solution.

Organic acids like oxalic acid and citric acid, not only contribute to proton-driven weathering. Their deprotonated anions (in this case oxalate and citrate) interact in a similar way as protons and hydroxide with the mineral crystal lattice. In fact, many of the deprotonated anions of organic acids are stronger weathering agents than protons and hydroxide. They behave as strong complexants with metals including Al3+, a central element in most mineral crystal lattices.

Another set of organic compounds with metal-complexing properties are siderophores. This type of molecules form strong bindings with especially Fe3+.

To They play a key role in the release and uptake of Fe into bacteria, fungi and plants Kraemer 2014 Ahmed 2014. Primary minerals containing substantial amounts of iron, like hornblende and biotite, show enhanced dissolution rates in the presence of microbial or fungal siderophores Kalinowski 2000 Sokolova 2010.

To  understand the impact of mycorrhizal fungi, we first need to determine what is the limiting step in the dissolution process. Generally, the soil solution After decades of research it  is well established that under normal,  far from equilibrium conditions, the rate limiting step is the formation of so called activated surface complexes. That is the complexation of weathering agents as protons or organic ligands with metals  inrespect to  the primary minerals. mineral crystal lattice Furrer 1986 Wieland 1988. The kinetics of this step can be described by the Transition State Theory (TST)  Lasaga 1984. For a single weathering agents, its effect on the weathering rate can be described with:

Application of the TST in mineral dissolution studies including organic complexants, show that the
 
Close to equilibrium: saprolith, big rock fragments.




 fragments.





  class="ltx_title_section">Fungal weathering in the lab

From lab to field


Conclusions