Biologically-Mediated Weathering of minerals from Nanometre Scale to Environmental Systems.

Lead Research Organisation: University of Sheffield
Department Name: Civil and Structural Engineering

Abstract

In nature, a complex system of physical, chemical and biological processes weather the Earth's surface and transform rock into soil. Because global erosion loss is now much faster (100 times or more) than soil formation, largely as a result of unsustainable cultivation practices, soil has become a finite resource. Despite the importance of soil for sustenance of our planet and it 6 billion human inhabitants, our knowledge of weathering is limited. This is because various scientific approaches are not sufficiently integrated to tackle the many, complex interactions that occur. Therefore a multidisciplinary approach is needed to study soil formation rates and processes. Soil fungi appear to use plant energy to mine nutrients from rock-but the mechanisms involved are uncertain. We want to know if biological weathering is driven by the flow of sugar produced by plant photosynthesis in return for nutrient elements (such as phosphorous, potassium) from the mineral particles. Nearly a third of the total chemical energy (sugar) produced by forest trees passes directly to symbiotic (mutually beneficial) root fungi. These fungi completely cover the tree roots and form extensive networks of living threads through soil. Virtually all nutrients taken up by the trees are absorbed through these fungi. This research programme will identify how fungal cells, and their secretions, interact with mineral surfaces and affect the rates of nutrient transfer from minerals to the organism. Making biological processes central to molecular-level understanding of how minerals dissolve is counter to existing theories. Investigating these fundamental molecular weathering mechanisms in living systems allows us to create new concepts and mathematical models that can describe biological weathering and be used in computer simulations of soil weathering dynamics. We propose to study these biochemical interactions at three levels of observation: 1. At the molecular scale to understand interactions between living cells and minerals and to quantify the chemistry that breaks down the mineral structure, 2. At the soil grain scale to quantify the activity and spatial distribution of the fungi, roots and other organisms (e.g. bacteria) and their effects on the rates at which minerals are dissolved to release nutrients, and 3. At soil profile scale to test models for the spatial distribution of active fungi and carbon energy and their seasonal variability and impact on mineral dissolution rates. We will combine the expertise from many scientific fields. Biologists will work with the fungi and plant cultures in the presence and absence of minerals that are sources of nutrients, and measure carbon energy fluxes in the fungal networks. Surface chemists will use X-Ray and Infrared beams that interact with the cell and mineral surface, and are then measured using sophisticated sensors to provide information on the chemical bonds that can form. Physicists will measure the minuscule forces that operate between fungi cells and minerals surfaces, but determine if fungi actually adhere and form chemical bonds. Materials scientists will use highly specialised visualisation methods to observe the shape and composition of dissolving minerals at almost atomic scale. Geochemists will study how the minerals change over time and how much mineral is dissolved. The data and understanding that is obtained, by working from almost molecular to soil profile scale, will be used by numerical modellers to simulate the complex interactions between higher plants, fungi, minerals, soil organic matter and infiltrating water. A final step is to simulate soil profile weathering under a range of scenarios for changes in climatic conditions and soil management. The anticipated achievement is a much stronger fundamental understanding of soil formation, particularly the role of biological weathering, so that we can improve our management strategies for this important natural resource.

Publications

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Bray A (2014) Biotite surface chemistry as a function of aqueous fluid composition in Geochimica et Cosmochimica Acta

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M.E. Romero-Gonzalez (Author) (2010) Interactions at the cell-mineral interface

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S. Bonneville (Author) (2010) Fungi on the rocks!

 
Description INTRODUCTION
This research project tackled the challenge of quantifying the role of biology in the physical and chemical alternation of rocks and minerals to form and develop soil at Earth's surface and to supply plants with mineral nutrients. In unsaturated soil environments, plant roots normally form symbiotic mycorrhizal associations with fungi. The plants provide energy from photosynthesis to the fungi in return for nutrients absorbed from the soil and released from minerals. A particular focus of this project is the role of ectomycorrhizal fungi (EMF), one of the two major types of mycorrhiza of trees. In EMF associations, roots are sheathed in fungus, and up to 30% of the net photosynthate of the plants passes through these fungi into the soil and virtually all of the water and nutrients taken up by the plants are supplied through the fungi. Fuelled by substantial amounts of recent photosynthate transported from shoots to roots, these fungi form extensive mycelial networks which extend into soil actively foraging for nutrients by altering minerals through the acidification of the immediate root environment. EMF aggressively weather minerals through the additional mechanism of releasing reactive organic compounds such as oxalic acid. Rates of biotic weathering should therefore be conceptualized as fundamentally controlled by the biomass, surface area of contact, and capacity of roots and their mycorrhizal fungal partners to interact physically and chemically with minerals. Furthermore, all of these factors are ultimately controlled by rates of carbon-energy supply from photosynthetic organisms to the fungi.
The aim of the project was to transform our understanding of how biota control mineral weathering and soil formation; through new mechanistic understanding and how this affects weathering processes from the scale of individual mineral grains to the whole planet. Key objectives were:
1. To assess the importance of soil carbon fluxes in controlling biologically-mediated weathering rates;
2. To identify linkages between plants, microbes and mineral reactions focussing on the central role of mycorrhizal fungi;
3. To elucidate the biochemical and biophysical interactions between mineral surfaces and living cells of mycorrhiza;
4. To quantify how these interactions change with climatic and geochemical parameters; and
5. To apply systems models to identify key variables and limiting conditions for the long-term weathering behaviour of soils.

1. CARBON FLOWS FROM PLANTS TO SOIL FUNGI CONTROL THE RELEASE RATES OF NUTRIENTS FROM SOIL MINERALS
Our project shows for the first time that the amount of carbon that is fixed by plant photosynthesis and directed through plant roots into the mycorrhizal fungi directly affects the rate of nutrient transfer from soil minerals into the plant. This was shown in studies involving growing tree seedlings with their roots inoculated with a single mycorrhizal fungus in sterile Petri dish 'microcosms' from which we excluded all other microorganisms, and in experiments using non-sterile soil in 8 litre 'mesocosms' in which we grew tree saplings inoculated with fungi and root-associated microbial communities of the adult trees collected from the field.
In both the microcosm and mesocosm experiments we supplied 14C carbon dioxide gas to the shoots of the plants, and traced and measured the fixation of this carbon by photosynthesis, and its subsequent allocation to roots, to the symbiotic mycorrhizal fungi extending from roots into the substrates, and into patches of different mineral grains. In the microcosm experiments we put small wells containing grains or chips of specific types of rocks and minerals inside the Petri dishes and the fungal symbionts grew from the roots into the wells where they then colonised the surfaces of the mineral grains. By comparing the amount of 14C allocated by the fungal partner from the host tree into wells containing quartz (a chemically resistant mineral that lacks nutrient elements required by plants and fungi) or containing apatite (the primary mineral source of the essential nutrient phosphorus, in the form of calcium phosphate) we found seventeen-fold higher carbon allocation by the fungus to interact with apatite rather than quartz grains.
This carbon allocation was accompanied by enhanced fungal exudation of oxalic acid, an important organic compound that binds to calcium to form crystalline calcium oxalate and accelerates the dissolution of calcium bearing minerals such as apatite. Rates of mineral weathering of apatite were shown to be increased by the mycorrhizal fungus, and where the fungal partner was supplied with phosphorus in solution the carbon allocation to the fungus was reduced, and the amount of apatite weathering was lower than when the main source of phosphorus was provided by apatite grains. In the latter case this increased the relative biomass of the fungus compared to the plant roots and greatly increased rates of weathering. This demonstrates that mycorrhiza both direct plant carbon energy towards the nutrient-rich phosphorus minerals but also that this flow of carbon energy accelerates mineral dissolution and uptake of the nutrient by the plant. These experiments were carried out without flowing water around the minerals or roots; the only way the phosphorus could enter the plant tissue was through the mycorrhizal fungi in contact with the mineral.
We carried out similar experiments using many different types of mineral and rock grains placed in separate wells within Petri dishes. We found that the dissolution rates of all the grains correlated with the amount of carbon flowing from the plant to the different wells.
Our experiments for the first time provide quantitative evidence of the importance of organic carbon allocation from recent photosynthate to mycorrhizal fungal hyphae in soil as a major pathway of chemical energy used to dissolve and alter minerals leading to nutrient release and fungal and plant uptake of these nutrients.
2. MYCORRHIZAL FUNGI ARE A CENTRAL LINK BETWEEN PLANT TYPE AND BIOLOGICAL WEATHERING OF SOIL MINERALS
One of the PhD students who completed their thesis as part of the project studied the biological dissolution of minerals buried beneath different tree types in an arboretum setting. Trees of similar size but known to have different fungal associations of their roots with specific types of mycorrhiza were selected. Mesh bags containing specific grains and fragments of mineral and rock were buried under the trees. The mesh material of the bags allowed mycorrhizal fungi to penetrate the bags, but excluded roots.
Two major classes of trees were selected including conifers (gymnosperms) and broadleaved l (angiosperms). The earliest gymnosperms to evolve are known to have established mycorrhizal associations with a particular type of fungi called arbuscular mycorrhiza- which co-evolved with the first land plants over 400 million years ago. These kinds of mycorrhiza are also common in angiosperm trees, which diversified much later than the earliest gymnosperms. However, a subset of relatively recently evolved gymnosperm and angiosperm trees support ectomycorrhiza, a root-fungal association in which the fine roots are entirely sheathed by advanced groups of fungi that often produce toadstools in forests. The ectomycorrhizal fungal partnerships have been shown to play a significant role in mineral weathering in many previous studies, and our work as described above, but the role of arbuscular mycorrhizal weathering under trees has previously been overlooked. In the arboretum experiment, both types of fungal associations were studied in four species of angiosperm and four species of gymnosperm trees.
The results showed conclusively that ectomycorrhizal gymnosperms and angiosperms caused approximately double the rock dissolution rate than arbuscular mycorrhizal trees of both types. These results provide fascinating new evidence that co-evolution of land plants and arbuscular mycorrhizal fungi is likely to have played a pivotal role in the acceleration of global terrestrial mineral weathering rates that accompanied the rise of land plants over 400 million years ago. This suggests that mycorrhiza-accelerated weathering and soil formation processes driven by these plant-fungal partnerships extend back 100s of millions of years earlier than previously recognized. It further suggested that a consequence of the more recent evolution of ectomycorrhizal fungi led to more rapid biological weathering over the past 120 million years, and that the increase in weathering over this period currently represented in global biogeochemical carbon cycling models and attributed to the rise of angiosperm forests is actually the combined result of the rise of ectomycorrhiza and angiosperm forests. These results have important implications for the evolution of Earth's climate over 100s of millions of years. This is because more rapid weathering consumes atmospheric CO2 and provides a biological thermostat - warmer climate drives biological productivity which in turn drives weathering and lowers CO2 levels thereby causing Earth cooling.
These helped drive an entirely new research project that was led by an expert on paleobotony - in which the co-evolution of trees and mycorrhizal fungi and their capacity to weather minerals in response to the changes in atmospheric CO2 concentrations that have occurred over the past 400 million years were studied as a control on Earth's climate through geological time.
3. MYCORRHIZAL FUNGI DRIVE SOIL WEATHERING THROUGH NANOSCALE INTERACTIONS WITH MINERAL SURFACES
Detailed observations at scales approaching single-atom resolution showed that the nutrient element potassium and other elements in the mineral biotite were depleted underneath ectomycorrhizal fungal hyphae extending from tree seedling roots and growing over the mineral surface under sterile conditions. The element concentration profiles showed a depletion layer of about one hundred nanometres thickness that can be explained by diffusion of elements, within the mineral, outward towards the hyphae where they are removed by uptake into the fungi- which can supply nutrient elements on to the plants.
These remarkable observations were carried out by imaging and analysing the thin interface of contact where mycorrhiza hyphae grow on mineral surfaces. Thin flakes of the sheet mineral biotite, which contains the important plant nutrient element potassium, were used in the microcosm experiments with tree seedling that are described above. A single hyphae was tracked across the biotite surface where it had grown for a period of about 4 months. The hyphae tip represented initial contact while hyphae sections located sequentially back along the hyphae represented progressively longer periods of contact between the hyphae and the mineral.
Using the technique of focussed ion beam milling, thin mineral sections underneath each of the hyphae locations were excavated to a depth of a few hundred nanometres. The extracted sections were removed and the element concentration profiles analysed. Elements were progressively removed in greater amounts for increasingly longer contact times. The profile patterns for a number of elements within biotite were used to calculate element dissolution and diffusion rates. The equations are based on established theories for how mineral elements dissolve and diffuse in solids and liquids. The calculated rates show that the biological dissolution caused by the hyphae is up to 30 times faster on the surface of contact, than is expected for dissolution in the absence of contact with growing fungi.
Using atomic-force microscopy we were able to show that a common ectomycorrhizal fungus growing from the roots of a pine seedling was able to physically alter silicate minerals, weakening the structure so that it was more easily removed and also led to 'trenching' of mineral surfaces leaving fungal-altered tracks. This is clear evidence of directed biogenic weathering of the minerals, involving both exudation of chemicals and physical forcing.
In detailed experiments involving cooperation between biologists and physicists within the consortium, samples were pre-imaged before insertion in the microcosms, were then colonised in the sterile microcosm environment, and then re-imaged after removal from the microcosms. Detailed re-inspection of the same nanoscale areas showed that fungal growth on the surface was accompanied by exudation of organic materials that attached to the mineral surface. Detailed characterisation of the effect of oxalic acid, a major component of the fungal exudate, on the weathering of silicate mineral showed the importance of this compound in accelerating the removal of atoms from the outer surface of a sheet silicate, exposing the more easily dissolvable atoms below leading to progressive etch-pitting of the surfaces.
Additional results showed that fungi in direct contact with biotite surfaces produced a more acidic environment, with pH of 4 or lower, compared to hyphae that were growing further above the mineral surface without direct contact. One of the PhD students, working on the mechanisms of dissolution for biotite, tackled the problem of understanding how pH at the surface influenced the susceptibility of the mineral to break down and dissolve. Small particles of biotite were immersed in solutions to which strong acid or base was added incrementally. With each addition, the difference between the acid or base added, and the amount of hydrogen ion measured in the solution (which reflects the solution pH) allowed the gain or loss of hydrogen ions by the surface to be determined. Dissolution experiments were carried out in parallel where the amount of elements dissolved from the surface at different solution pH values was measured. Taken together, the results indicate that the composition of the biotite surface varies dramatically at different solution pH values. Before dissolving, the biotite mineral contains significant amounts of the chemical elements potassium, aluminium, silicon, iron and magnesium, and oxygen. After reacting in solutions at basic conditions, the biotite surface is highly depleted in potassium. Around neutral conditions, the biotite mineral surface is almost only composed of remaining Si and Al, and the Fe, with extensive removal of potassium and magnesium. Finally, at acidic conditions, the reacted biotite surface is comprised almost exclusively of a remaining network of silicon and oxygen and hydrogen ions. These results are important because they demonstrate how elements are lost from the mineral and become available to solution or through biouptake to fungal hyphae. This shows the important role of the low pH that is induced by the direct fungal contact to influence the extent of mineral dissolution and the selectivity of element release from the mineral.
4. MATHEMATICAL MODELS UNITE THEORY AND EXPERIMENTS ON CLIMATE AND GEOCHEMICAL EFFECTS ON SOIL WEATHERING
In research from another PhD project affiliated with the project, the effects of climate and mineralogy and mineral chemistry on soil weathering rates are calculated with equations that combine the laboratory results described above, with well-established knowledge on plant productivity and plant-ectomycorrhiza associations. A chain of effects describes how plant productivity is affected by climatic conditions and also delivers carbon into the soil environment via plant roots to mycorrhizal fungi biomass. The amount of fungal biomass provides a physical description of the volume of soil that is pervaded by fungi and where fungal-driven, intensive biological weathering occurs.
The equations that describe element diffusion and dissolution rates provide the quantitative link to specific types of minerals - their resistance and susceptibility to chemical attach by the hyphae surfaces. With these series of calculations, the project has established a new, mechanistic description of biological weathering. This weathering process model quantifies biological weathering rates for soil profiles as a function of soil mineralogy and climatic conditions. The process weathering model allows generalisation of experimental findings to a far wider range of minerals and conditions of climate and plant type that is possible through experimentation alone. The model also allows the differences in weathering rates in soil profiles to be compared between different locations with different soil mineralogy and vegetation, and the impact of changes in climate on vegetation, water availability and flow, and the related biological weathering to be calculated.
5. MECHANISTIC BIOLOGICAL WEATHERING RATES ARE CALCULATED AT GLOBAL SCALE THROUGH GEOLOGICAL TIME
The mechanistic weathering process model successfully describes global weathering rates over geological time scales. Although direct observations of soil weathering rates and climatic conditions are not possible for the geological past, proxy variables such as geochemical isotopes and sedimentary rock records do provide well-established information to test Earth systems models. The process model can be run over time by incorporating the historical distribution of continental lithology (rock types) and how it has changed over 100s of millions of years. Also, from initial conditions of atmospheric CO2, the evolution of climate and its effect on vegetation, plant productivity and the impact on weathering rates is incorporated as well. The mechanistic soil profile model is run over discrete zones of the continental surface, for the conditions within that zone, and the results are added up at each time step. The result is a successful description of the interactions of climate and vegetation evolution, and biological soil weathering, over the past several 100 million years. Some of the most fascinating results are those that support the project view of co-evolution of plants and their mycorrhizal associations over geological history, as a major driver of continental weathering, soil formation, and the atmospheric CO2 draw-down effect of continental weathering. This picture of Earth history, biological evolution, and feedback to climate, provides evidence of how biology has helped shape the Earth habitat and helps stabilise Earth's climate within its current range.
CONCLUDING OVERVIEW
This project and the programmes of research that have followed from it are transformative in our understanding of the processes of biological weathering driven by tree roots and their associated mycorrhizal fungi. Our work establishes a direct link between allocation of photosynthate by trees to their roots and associated mycorrhizal symbionts as pivotal in driving mineral weathering and resulting soil formation. Our work has for the first time developed an Earth systems understanding of the links between plant and fungal evolution, mineral weathering processes, and feedbacks between these factors and global climate and atmospheric CO2 concentrations over the past 400 million years. We have quantified the importance of the active and targeted secretion of organic compounds by mycorrhizal fungal hyphae in response to contact with specific mineral grains containing calcium and other readily weatherable elements. Our results reveal a previously unknown process of element dissolution from silicates involving element removal through multiple layers of the crystals by a diffusion-depletion driven process that alters minerals immediately under fungal hyphae. Additionally, the nanoscale microscopy provided the first nanoscale topographic evidence of biogenic weathering by mycorrhiza. Our findings have advanced our understanding of plant-driven fungal weathering from the scale of atoms to global biogeochemical cycles over hundreds of millions of years and have developed a whole new field of research in experimental paleobiology linking the evolution of plants and their fungal partners to earth system science and biogeochemistry.
Exploitation Route The project was featured as the cover story in the September 2013 issue of the NERC poplar science magazine Planet Earth.
Sectors Environment

URL http://external.wun.ac.uk/wsc/index.html
 
Description Two impact routes are used and continue to be pursued with substantial input from the new knowledge created during this NERC project. These are 1. Developing priority areas for translational research with the private sector and government agencies, and 2. Providing science evidence for environmental policy and science at national, EU and intergovernmental levels. SCIENCE AND TECHNOLOGY EXPLOITATION THROUGH INDUSTRY AND GOVERNMENT AGENCIES Knowledge Exchange for the NERC Consortium Grant on Biological Weathering was delivered by an industry-academic-government workshop on Optimising Soil Chemistry for Agricultural Resource Efficiency (OSCAR). This was attended by 41 participants from all 3 sectors, 28th-29th November 2011, hosted by the Royal Society of Chemistry. The workshop report was prepared from the results of 4 working groups established during the meeting. The report was published in March 2013 as an RSC publication Securing Soils for Sustainable Agriculture, a science-led strategy. This authoritative UK R&D strategy document identified 4 priority areas of translational research that should be pursued through industry-government-academic partnerships. The 4 areas are: 1. Creation of closed loop systems for recovery of major nutrients, water and micronutrients from low-grade farm and food wastes to reduce dependence on primary stocks and global markets; 2. Development and application of high sensitivity, high resolution biosignalling and sensor technologies to support precision agriculture and more sophisticated regulatory testing; 3. Detailed and robust understanding of molecular-scale biogeochemical processes associated with phosphorus uptake at and around plant roots, to stimulate the development of target-specific, 'smart' agrochemical agents; 4. Integrated models of plant-soil-water interactions and development of methodologies to upscale from laboratory to field and landscape to inform soil management policies, climate change mitigation and adaptation to environmental change. The report contributed to science evidence that helped inform the BBSRC/NERC research strategy for soils and food production, the Defra Sustainable Intensification (of agriculture) Research Platform, the Technology Strategy Board Sustainable Agri-Food Innovation Platform, and the UK Agritechnology Strategy. SCIENCE EVIDENCE EXPLOITATION AT THE POLICY INTERFACE New knowledge from the NERC Consortium grant on biological weathering contributed to the United Nations Environment Programme (UNEP) Yearbook 2012 where the PI Banwart was co-author of a foresight chapter Benefits of Soil Carbon. The UNEP Yearbook target audience is the International Council of Environment Ministers, The UNEP Council and the general public. Hence, this is an influential impact route for public policy and public understanding. The UNEP chapter authors successfully submitted a proposal to SCOPE (Scientific Committee on Problems of the Environment) for an international Rapid Assessment Process (RAP) project (www.soilcarbon.org.uk). The proposing team compose the core of the project Scientific Advisory Committee which is chaired by the NERC project Principal Investigator. This project, reported in the UNEP Year Book 2014, Chapter 9: Securing soil carbon benefits, has produced 'SCOPE Volume 71: Soil Carbon - science, management and policy for multiple benefits'; comprising 27 background chapters and 4 cross-cut chapters of scientific evidence to inform new policy approaches to support soil science, land management and environmental resources. Prepared by 72 expert authors from 19 countries around the world with the cross-cut chapters drafted by 40 participants at an integrating workshop hosted by the European Commission Directorate General Joint Research Centre in March 2013, this volume is a timely contribution that supports the 5 pillars of the Global Soil Partnership and the related activities of the 2015 International Year of Soils. The new knowledge from this NERC research project helped seed a subsequent successful award of an EC Large Integrating Project on Soil Transformations in European Catchments (www.soiltrec.eu). The project is led by U. Sheffield with 16 partners in Europe, USA and China. The overarching aim of the project is to provide methodology to upscale soil process rates to national and EU scale in order to assess soil threats and mitigation strategies for the EU. 3. Potential use in non-academic contexts: describe how this research could be used in a non-academic context. The project was featured as the cover story in the September 2013 issue of the NERC poplar science magazine Planet Earth. The project outputs and expertise could be used for the following additional non-academic uses: 1. Provide content and design advice for a public display demonstrating how soil functions and its vulnerability to environmental changes such as land use and climate, 2. Provide expert views and popular science accounts of the amazing role of mycorrhiza to help form soil and nourish vegetation - for audio, video or print content. 3. News dissemination to the public of the issues addressed in the Sustainable Agriculture and Soils Innovation (SASI) event held at the Royal Society of Chemistry, 31 March - 1 April 2014, London: www.rsc.org/events/detail/10676/Sustainable Agriculture and Soils Innovation.
First Year Of Impact 2011
Sector Agriculture, Food and Drink,Environment
Impact Types Cultural,Societal,Economic