Iain M. Young

Rhizosphere: biophysics, biogeochemistry and ecological relevance

Life on Earth is sustained by a small volume of soil surrounding roots, called the rhizosphere. The soil is where most of the biodiversity on Earth exists, and the rhizosphere probably represents the most dynamic habitat on Earth; and certainly is the most important zone in terms of defining the quality and quantity of the Human terrestrial food resource. Despite its central importance to all life, we know very little about rhizosphere functioning, and have an extraordinary ignorance about how best we can manipulate it to our advantage. A major issue in research on rhizosphere processes is the intimate connection between the biology, physics and chemistry of the system which exhibits astonishing spatial and temporal heterogeneities. This review considers the unique biophysical and biogeochemical properties of the rhizosphere and draws some connections between them. Particular emphasis is put on how underlying processes affect rhizosphere ecology, to generate highly heterogeneous microenvironments. Rhizosphere ecology is driven by a combination of the physical architecture of the soil matrix, coupled with the spatial and temporal distribution of rhizodeposits, protons, gases, and the role of roots as sinks for water and nutrients. Consequences for plant growth and whole-system ecology are considered. The first sections address the physical architecture and soil strength of the rhizosphere, drawing their relationship with key functions such as the movement and storage of elements and water as well as the ability of roots to explore the soil and the definition of diverse habitats for soil microorganisms. The distribution of water and its accessibility in the rhizosphere is considered in detail, with a special emphasis on spatial and temporal dynamics and heterogeneities. The physical architecture and water content play a key role in determining the biogeochemical ambience of the rhizosphere, via their effect on partial pressures of O2 and CO2, and thereby on redox potential and pH of the rhizosphere, respectively. We address the various mechanisms by which roots and associated microorganisms alter these major drivers of soil biogeochemistry. Finally, we consider the distribution of nutrients, their accessibility in the rhizosphere, and their functional relevance for plant and microbial ecology. Gradients of nutrients in the rhizosphere, and their spatial patterns or temporal dynamics are discussed in the light of current knowledge of rhizosphere biophysics and biogeochemistry. Priorities for future research are identified as well as new methodological developments which might help to advance a comprehensive understanding of the co-occurring processes in the rhizosphere.

Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil

Biological soil thin-sections and a combination of image analysis and geostatistical tools were used to conduct a detailed investigation into the distribution of bacteria in soil and their relationship with pores. The presence of spatial patterns in the distribution of bacteria was demonstrated at the microscale, with ranges of spatial autocorrelation of 1 mm and below. Bacterial density gradients were found within bacterial patches in topsoil samples and also in one subsoil sample. Bacterial density patches displayed a mosaic of high and low values in the remaining subsoil samples. Anisotropy was detected in the spatial structure of pores, but was not detected in relation to the distribution of bacteria. No marked trend as a function of distance to the nearest pore was observed in bacterial density values in the topsoil, but in the subsoil bacterial density was greatest close to pores and decreased thereafter. Bacterial aggregation was greatest in the cropped topsoil, though no consistent trends were found in the degree of bacterial aggregation as a function of distance to the nearest pore. The implications of the results presented for modelling and predicting bacterial activity in soil are discussed.

In Situ Spatial Patterns of Soil Bacterial Populations, Mapped at Multiple Scales, in an Arable Soil

Very little is known about the spatial organization of soil microbes across scales that are relevant both to microbial function and to field-based processes. The spatial distributions of microbes and microbially mediated activity have a high intrinsic variability. This can present problems when trying to quantify the effects of disturbance, management practices, or climate change on soil microbial systems and attendant function. A spatial sampling regime was implemented in an arable field. Cores of undisturbed soil were sampled from a 3 × 3 × 0.9 m volume of soil (topsoil and subsoil) and a biological thin section, in which the in situ distribution of bacteria could be quantified, prepared from each core. Geostatistical analysis was used to quantify the nature of spatial structure from micrometers to meters and spatial point pattern analysis to test for deviations from complete spatial randomness of mapped bacteria. Spatial structure in the topsoil was only found at the microscale (micrometers), whereas evidence for nested scales of spatial structure was found in the subsoil (at the microscale, and at the centimeter to meter scale). Geostatistical ranges of spatial structure at the micro scale were greater in the topsoil and tended to decrease with depth in the subsoil. Evidence for spatial aggregation in bacteria was stronger in the topsoil and also decreased with depth in the subsoil, though extremely high degrees of aggregation were found at very short distances in the deep subsoil. The data suggest that factors that regulate the distribution of bacteria in the subsoil operate at two scales, in contrast to one scale in the topsoil, and that bacterial patches are larger and more prevalent in the topsoil.

Three-dimensional microorganization of the soil-root-microbe system.

Soils contain the greatest reservoir of biodiversity on Earth, and the functionality of the soil ecosystem sustains the rest of the terrestrial biosphere. This functionality results from complex interactions between biological and physical processes that are strongly modulated by the soil physical structure. Using a novel combination of biochemical and biophysical indicators and synchrotron microtomography, we have discovered that soil microbes and plant roots microengineer their habitats by changing the porosity and clustering properties (i.e., spatial correlation) of the soil pores. Our results indicate that biota act to significantly alter their habitat toward a more porous, ordered, and aggregated structure that has important consequences for functional properties, including transport processes. These observations support the hypothesis that the soil–plant–microbe complex is self-organized.

Interactions between soil structure and fungi

The spatial organisation of soils is crucially important in affecting belowground function, and the associated delivery of ecosystem services. Fungi constitute an important part of the soil biomass. As well as playing key roles in nutrient cycling and biotic interactions, they are also intimately involved in soil structural dynamics. Fungi mediate the formation of soil structure at a variety of spatial scales via charge, adhesive and enmeshment mechanisms. They also produce large quantities of hydrophobic compounds that affect water infiltration properties of soils. Fungi can also destroy soil structure via decomposition of organic matter that affects soil aggregation. In turn, soil structure affects fungi. The filamentous growth-form of fungi is a very efficient space-filling structure well adapted for life in a spatially heterogeneous environment such as soil, but the labyrinthine pore network ultimately regulates how fungal mycelia grow through and function within the soil. The distribution of water within soils plays a crucial role in governing fungal development and activity, as does the spatial distribution of nutrient resources. This article reviews the continual interplay that occurs between soil structure and fungi, and discusses how self-organisation mechanisms may operate in the soil system.

New methods and models for characterising structural heterogeneity of soil

The dual cause of quantifying and modelling soil structure is a regular irritant to most soil scientists, whatever their discipline. All know of the importance of placing soil processes in the context of the physical framework of the soil. It is the habitat for all soil biota, and plant roots; it acts as a reservoir for solutes, and is composed of the main conduits that transfer gases to the atmosphere, and potential pollutants to the waterways. Unfortunately, an explicit account of the heterogeneity inherent in the soil physical architecture has, until recently, been beyond experimental and theoretical insight. This discussion aims to draw together some current methods and models for characterising the soil structural heterogeneity. We question the use of aggregates as indicators of structure, assess possible alternatives, and discuss several theoretical approaches that promise to capture the ubiquitous heterogeneity in soil structures. The key question that is examined is, can we functionally quantify soil structure and causally relate that quantification to specific processes?

Microbial Distribution in Soils: Physics and Scaling

In a handful of fertile soil there are billions of microorganisms and yet, even with a conservative estimate, the surface area covered by these organisms is considerably less than 1%. What does this tell us about the function of the physical structure in which soil organisms reside and function, collecting, and separating micropopulations from each other and from resources? It would seem that most of the soil is akin to desert regions with little life been supported on its terrains, yet with vast communities of individuals, from an amazing array of species, supported in small-scale habitats, connected or disconnected by saturated or unsaturated pore space over relatively short time-scales. The biodiversity of these communities remains impressive yet overall functionally illusive, bar some considerations of inbuilt redundancy. What is far more impressive is the range of habitats on offer to populations with short-term evolutionary time frames. The availability of spatially and temporally diverse habitats probably gives rise to the biodiversity that we seeAbstract In a handful of fertile soil there are billions of microorganisms and yet, even with a conservative estimate, the surface area covered by these organisms is considerably less than 1%. What does this tell us about the function of the physical structure in which soil organisms reside and function, collecting, and separating micropopulations from each other and from resources? It would seem that most of the soil is akin to desert regions with little life been supported on its terrains, yet with vast communities of individuals, from an amazing array of species, supported in small-scale habitats, connected or disconnected by saturated or unsaturated pore space over relatively short time-scales. The biodiversity of these communities remains impressive yet overall functionally illusive, bar some considerations of inbuilt redundancy. What is far more impressive is the range of habitats on offer to populations with short-term evolutionary time frames. The availability of spatially and temporally diverse habitats probably gives rise to the biodiversity that we see in soil. It is not too far fetched to state that the majority of habitats on Earth (and indeed extraterrestrial) are revealed in that handful of soil. The key question is what is the functional consequence of such habitat heterogeneity? To answer this it is clear that we need to bring together a new discipline that combines the biology and physics of the soil ecosystem. This biophysical approach, combined, where required, with important mineral-microbe knowledge is needed to help us understand the mechanisms by which soils remain productive, and to identify the tipping-points at which there may be no return to sustainability. This review aims to highlight the importance of addressing the soil ecosystem as a dynamic heterogeneous system focusing on microbiota–habitat interactions.

Root phenomics of crops: opportunities and challenges

Reliable techniques for screening large numbers of plants for root traits are still being developed, but include aeroponic, hydroponic and agar plate systems. Coupled with digital cameras and image analysis software, these systems permit the rapid measurement of root numbers, length and diameter in moderate (typically <1000) numbers of plants. Usually such systems are employed with relatively small seedlings, and information is recorded in 2D. Recent developments in X-ray microtomography have facilitated 3D non-invasive measurement of small root systems grown in solid media, allowing angular distributions to be obtained in addition to numbers and length. However, because of the time taken to scan samples, only a small number can be screened (typically <10 per day, not including analysis time of the large spatial datasets generated) and, depending on sample size, limited resolution may mean that fine roots remain unresolved. Although agar plates allow differences between lines and genotypes to be discerned in young seedlings, the rank order may not be the same when the same materials are grown in solid media. For example, root length of dwarfing wheat (Triticum aestivum L.) lines grown on agar plates was increased by ~40% relative to wild-type and semi-dwarfing lines, but in a sandy loam soil under well watered conditions it was decreased by 24-33%. Such differences in ranking suggest that significant soil environment-genotype interactions are occurring. Developments in instruments and software mean that a combination of high-throughput simple screens and more in-depth examination of root-soil interactions is becoming viable.

Visualization, modelling and prediction in soil microbiology

The introduction of new approaches for characterizing microbial communities and imaging soil environments has benefited soil microbiology by providing new ways of detecting and locating microorganisms. Consequently, soil microbiology is poised to progress from simply cataloguing microbial complexity to becoming a systems science. A systems approach will enable the structures of microbial communities to be characterized and will inform how microbial communities affect soil function. Systems approaches require accurate analyses of the spatio–temporal properties of the different microenvironments present in soil. In this Review we advocate the need for the convergence of the experimental and theoretical approaches that are used to characterize and model the development of microbial communities in soils.

A lattice BGK model for advection and anisotropic dispersion equation

This paper presents a lattice Boltzmann model (LBM) for 2-D advection and anisotropic dispersion equation (AADE) based on the Bhatnagar, Gross and Krook (BGK) model. In the proposed model, the particle speed space is discretized using a rectangular lattice that has four speeds in nine directions, and the single relaxation time is assumed to be directionally dependent. To ensure that the collision is mass-invariant when the relaxation time is directionally dependent, the concentration is calculated from a weighted summation of the particle distribution functions. The proposed model was verified against benchmark problems and the finite difference solution of solute transport with spatially variable dispersion coefficients and non-uniform velocity field. The significant results are that it conserves mass perfectly and offers accurate and efficient solutions for both dispersion-dominated and advection-dominated problems.