Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi.

Phosphorus (P) is essential for plant growth. Arbuscular mycorrhizal fungi (AMF) aid its uptake by acquiring P from sources distant from roots in return for carbon. Little is known about how AMF colonise soil pore-space, and models of AMF-enhanced P-uptake are poorly validated. We used synchrotron X-ray computed tomography to visualize mycorrhizas in soil and synchrotron X-ray fluorescence/X-ray absorption near edge structure (XRF/XANES) elemental mapping for P, sulphur (S) and aluminium (Al) in combination with modelling. We found that AMF inoculation had a suppressive effect on colonisation by other soil fungi and identified differences in structure and growth rate between hyphae of AMF and nonmycorrhizal fungi. Our results showed that AMF co-locate with areas of high P and low Al, and preferentially associate with organic-type P species over Al-rich inorganic P. We discovered that AMF avoid Al-rich areas as a source of P. Sulphur-rich regions were found to be correlated with higher hyphal density and an increased organic-associated P-pool, whilst oxidized S-species were found close to AMF hyphae. Increased S oxidation close to AMF suggested the observed changes were microbiome-related. Our experimentally-validated model led to an estimate of P-uptake by AMF hyphae that is an order of magnitude lower than rates previously estimated - a result with significant implications for the modelling of plant-soil-AMF interactions.

Space and time-resolved monitoring of phosphorus release from a fertilizer pellet and its mobility in soil using microdialysis and X-ray computed tomography.

Phosphorus is an essential nutrient for crops. Precise spatiotemporal application of P fertilizer can improve plant P acquisition and reduce run-off losses of P. Optimizing application would benefit from understanding the dynamics of P release from a fertilizer pellet into bulk soil, which requires space- and time-resolved measurements of P concentration in soil solutions. In this study, we combined microdialysis and X-ray computed tomography to investigate P transport in soil. Microdialysis probes enabled repeated solute sampling from one location with minimal physical disturbance, and their small dimensions permitted spatially resolved monitoring. We observed a rapid initial release of P from the source, producing high dissolved P concentrations within the first 24 h, followed by a decrease in dissolved P over time compatible with adsorption onto soil particles. Soils with greater bulk density (i.e., reduced soil porosity) impeded the P pulse movement, which resulted in a less homogeneous distribution of total P in the soil column at the end of the experiment. The model fit to the data showed that the observed phenomena can be explained by diffusion and adsorption. The results showed that compared with conventional measurement techniques (e.g., suction cups), microdialysis measurements present a less invasive alternative. The time-resolved measurements ultimately highlighted rapid P dynamics that require more attention for improving P use efficiency.

Linking root structure to functionality: the impact of root system architecture on citrate-enhanced phosphate uptake.

Root citrate exudation is thought to be important for phosphate solubilization. Previous research has concluded that cluster-like roots benefit most from this exudation in terms of increased phosphate uptake, suggesting that root structure plays an important role in citrate-enhanced uptake (additional phosphate uptake due to citrate exudation). Time-resolved computed tomography images of wheat root systems were used as the geometry for 3D citrate-phosphate solubilization models. Citrate-enhanced uptake was correlated with morphological measures of the root systems to determine which had the most benefit. A large variation of citrate-enhanced uptake over 11 root structures was observed. Root surface area dominated absolute phosphate uptake, but did not explain citrate-enhanced uptake. Number of exuding root tips correlated well with citrate-enhanced uptake. Root tips in close proximity could collectively exude high amounts of citrate, resulting in a delayed spike in citrate-enhanced uptake. Root system architecture plays an important role in citrate-enhanced uptake. Singular morphological measurements of the root systems cannot entirely explain variations in citrate-enhanced uptake. Root systems with many tips would benefit greatly from citrate exudation. Quantifying citrate-enhanced uptake experimentally is difficult as variations in root surface area would overwhelm citrate benefits.

Multiple Scale Homogenisation of Nutrient Movement and Crop Growth in Partially Saturated Soil.

In this paper, we use multiple scale homogenisation to derive a set of averaged macroscale equations that describe the movement of nutrients in partially saturated soil that contains growing potato tubers. The soil is modelled as a poroelastic material, which is deformed by the growth of the tubers, where the growth of each tuber is dependent on the uptake of nutrients via a sink term within the soil representing root nutrient uptake. Special attention is paid to the reduction in void space, resulting change in local water content and the impact on nutrient diffusion within the soil as the tubers increase in size. To validate the multiple scale homogenisation procedure, we compare the system of homogenised equations to the original set of equations and find that the solutions between the two models differ by [Formula: see text]. However, we find that the computation time between the two sets of equations differs by several orders of magnitude. This is due to the combined effects of the complex three-dimensional geometry and the implementation of a moving boundary condition to capture tuber growth.

Statistical Effective Diffusivity Estimation in Porous Media Using an Integrated On-site Imaging Workflow for Synchrotron Users.

Transport in porous media plays an essential role for many physical, engineering, biological and environmental processes. Novel synchrotron imaging techniques and image-based models have enabled more robust quantification of geometric structures that influence transport through the pore space. However, image-based modelling is computationally expensive, and end users often require, while conducting imaging campaign, fast and agile bulk-scale effective parameter estimates that account for the pore-scale details. In this manuscript we enhance a pre-existing image-based model solver known as OpenImpala to estimate bulk-scale effective transport parameters. In particular, the boundary conditions and equations in OpenImpala were modified in order to estimate the effective diffusivity in an imaged system/geometry via a formal multi-scale homogenisation expansion. Estimates of effective pore space diffusivity were generated for a range of elementary volume sizes to estimate when the effective diffusivity values begin to converge to a single value. Results from OpenImpala were validated against a commercial finite element method package COMSOL Multiphysics (abbreviated as COMSOL). Results showed that the effective diffusivity values determined with OpenImpala were similar to those estimated by COMSOL. Tests on larger domains comparing a full image-based model to a homogenised (geometrically uniform) domain that used the effective diffusivity parameters showed differences below 2 % error, thus verifying the accuracy of the effective diffusivity estimates. Finally, we compared OpenImpala's parallel computing speeds to COMSOL. OpenImpala consistently ran simulations within fractions of minutes, which was two orders of magnitude faster than COMSOL providing identical supercomputing specifications. In conclusion, we demonstrated OpenImpala's utility as part of an on-site tomography processing pipeline allowing for fast and agile assessment of porous media processes and to guide imaging campaigns while they are happening at synchrotron beamlines. Supplementary Information: The online version contains supplementary material available at 10.1007/s11242-023-01993-7.

Projected Increases in Precipitation Are Expected To Reduce Nitrogen Use Efficiency and Alter Optimal Fertilization Timings in Agriculture in the South East of England.

Nitrogen fertilization is vital for productive agriculture and efficient land use. However, globally, approximately 50% of the nitrogen applied is lost to the environment, causing inefficiencies, pollution, and greenhouse gas emissions. Rainfall and its effect on soil moisture are the major components controlling nitrogen losses in agriculture. Thus, changing rainfall patterns could accelerate nitrogen inefficiencies. We used a mechanistic modeling platform to determine how precipitation-optimal nitrogen fertilization timings and resulting crop nitrogen uptake have changed historically (1950-2020) and how they are predicted to change under the RCP8.5 climate scenario (2021-2069) in the South East of England. We found that historically, neither precipitation-optimal fertilization timings nor resulting plant uptake changed significantly. However, there were large year-to-year variations in both. In the 2030s, where it is projected to get wetter, precipitation-optimal fertilization timings are predicted to be later in the season and the resulting plant uptake noticeably lower. After 2040, the precipitation-optimal uptakes are projected to increase with earlier precipitation-optimal timings closer to historical values, corresponding to the projected mean daily rainfall rates decreasing to the historical values in these growing seasons. It seems that the interannual variation in precipitation-optimal uptake is projected to increase. Ultimately, projected changes in precipitation patterns will affect nitrogen uptake and precipitation-optimal fertilization timings. We argue that the use of bespoke fertilization timings in each year can help recuperate the reduced N uptake due to changing precipitation.

Global earthworm distribution and activity windows based on soil hydromechanical constraints.

Earthworm activity modifies soil structure and promotes important hydrological ecosystem functions for agricultural systems. Earthworms use their flexible hydroskeleton to burrow and expand biopores. Hence, their activity is constrained by soil hydromechanical conditions that permit deformation at earthworm's maximal hydroskeletal pressure (≈200kPa). A mechanistic biophysical model is developed here to link the biomechanical limits of earthworm burrowing with soil moisture and texture to predict soil conditions that permit bioturbation across biomes. We include additional constraints that exclude earthworm activity such as freezing temperatures, low soil pH, and high sand content to develop the first predictive global map of earthworm habitats in good agreement with observed earthworm occurrence patterns. Earthworm activity is strongly constrained by seasonal dynamics that vary across latitudes largely due to soil hydromechanical status. The mechanistic model delineates the potential for earthworm migration via connectivity of hospitable sites and highlights regions sensitive to climate.

Stabilizing gold nanoparticles for use in X-ray computed tomography imaging of soil systems.

This investigation establishes a system of gold nanoparticles that show good colloidal stability as an X-ray computed tomography (XCT) contrast agent under soil conditions. Gold nanoparticles offer numerous beneficial traits for experiments in biology including: comparatively minimal phytotoxicity, X-ray attenuation of the material and the capacity for functionalization. However, soil salinity, acidity and surface charges can induce aggregation and destabilize gold nanoparticles, hence in biomedical applications polymer coatings are commonly applied to gold nanoparticles to enhance stability in the in vivo environment. Here we first demonstrate non-coated nanoparticles aggregate in soil-water solutions. We then show coating with a polyethylene glycol (PEG) layer prevents this aggregation. To demonstrate this, PEG-coated nanoparticles were drawn through flow columns containing soil and were shown to be stable; this is in contrast with control experiments using silica and alumina-packed columns. We further determined that a suspension of coated gold nanoparticles which fully saturated soil maintained stability over at least 5 days. Finally, we used time resolved XCT imaging and image based models to approximate nanoparticle diffusion as similar to that of other typical plant nutrients diffusing in water. Together, these results establish the PEGylated gold nanoparticles as potential contrast agents for XCT imaging in soil.

Biomechanical limits to soil penetration by earthworms: direct measurements of hydroskeletal pressures and peristaltic motions.

Burrows resulting from earthworm activity are important for supporting various physical and ecological soil processes. Earthworm burrowing activity is quantified using models for earthworm penetration and cavity expansion that consider soil moisture and mechanical properties. Key parameters in these models are the maximal pressures exerted by the earthworm's hydroskeleton (estimated at 200 kPa). We designed a special pressure chamber that directly measures the pressures exerted by moving earthworms under different confining pressures to delineate the limits of earthworm activity in soils at different mechanical and hydration states. The chamber consists of a Plexiglas prism fitted with inner flexible tubing that hosts the earthworm. The gap around the tubing is pressurized using water, and the earthworm's peristaltic motion and concurrent pressure fluctuations were recorded by a camera and pressure transducer. A model that links the earthworm's kinematics with measured pressure fluctuations was developed. Resulting maximal values of radial pressures for anecic and endogeic earthworms were 130 kPa and 195 kPa, respectively. Mean earthworm peristaltic frequencies were used to quantify burrowing rates that were in agreement with previous results. The study delineates mechanical constraints to soil bioturbation by earthworms by mapping the elastic behaviour in the measurement chamber onto the expected elasto-viscoplastic environment of natural soils.

Listening to earthworms burrowing and roots growing - acoustic signatures of soil biological activity.

We report observations of acoustic emissions (AE) from growing plant roots and burrowing earthworms in soil, as a noninvasive method for monitoring biophysical processes that modify soil structure. AE emanating from earthworm and plants root activity were linked with time-lapse imaging in glass cells. Acoustic waveguides where installed in soil columns to monitor root growth in real time (mimicking field application). The cumulative AE events were in correlation with earthworm burrow lengths and with root growth. The number of AE events recorded from the soil columns with growing maize roots were several orders of magnitude larger than AE emanating from bare soil under similar conditions. The results suggest that AE monitoring may offer a window into largely unobservable dynamics of soil biomechanical processes such as root growth or patterns of earthworm activity - both important soil structure forming processes.

Soil Penetration by Earthworms and Plant Roots--Mechanical Energetics of Bioturbation of Compacted Soils.

We quantify mechanical processes common to soil penetration by earthworms and growing plant roots, including the energetic requirements for soil plastic displacement. The basic mechanical model considers cavity expansion into a plastic wet soil involving wedging by root tips or earthworms via cone-like penetration followed by cavity expansion due to pressurized earthworm hydroskeleton or root radial growth. The mechanical stresses and resulting soil strains determine the mechanical energy required for bioturbation under different soil hydro-mechanical conditions for a realistic range of root/earthworm geometries. Modeling results suggest that higher soil water content and reduced clay content reduce the strain energy required for soil penetration. The critical earthworm or root pressure increases with increased diameter of root or earthworm, however, results are insensitive to the cone apex (shape of the tip). The invested mechanical energy per unit length increase with increasing earthworm and plant root diameters, whereas mechanical energy per unit of displaced soil volume decreases with larger diameters. The study provides a quantitative framework for estimating energy requirements for soil penetration work done by earthworms and plant roots, and delineates intrinsic and external mechanical limits for bioturbation processes. Estimated energy requirements for earthworm biopore networks are linked to consumption of soil organic matter and suggest that earthworm populations are likely to consume a significant fraction of ecosystem net primary production to sustain their subterranean activities.