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Interactions between Soil Particles and Microorganisms: Impact on the Terrestrial Ecosystem / Edition 1 available in Hardcover
This definitive guide provides the scientific community with a critical evaluation of the interactions of minerals, organic components and microorganisms in the soil and their importance in the ecosystem.
• Provides a unique insight into the effects of microbes on pollutants in the soil, which is necessary for all environmental scientists working in this area
• Allows further discussion and development to uncover the dynamics and mechanisms of the environmental processes of nature
|Series:||Series on Analytical and Physical Chemistry of Environmental Systems Series , #7|
|Product dimensions:||6.32(w) x 9.15(h) x 1.53(d)|
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Interactions between Soil Particles and MicroorganismsImpact on the Terrestrial Ecosystem
John Wiley & SonsCopyright © 2002 John Wiley & Sons, Ltd.
All right reserved.
Chapter OneInteractions between Microorganisms and Soil Particles: An Overview
C. CHENU Unité de Science du Sol, Versailles, France
G. STOTZKY New York University, USA
1 Introduction 4 2 Surface Interactions between Microorganisms and Soil Particles 9 2.1 Adhesion of Microorganisms to Surfaces 9 2.2 Adsorption of Microbial Metabolites on Soil Particles and its Consequences 13 2.2.1 Adsorption of Extracellular Polysaccharides 13 2.2.2 Adsorption of Biologically Active Macromolecules 14 2.3 Effects of Adsorption of Organic Substrates on their Biodegradation 16 3 Interactions between Soil Particles and Microorganisms at the Microstructure Scale 18 3.1 Accessibility of Substrates to Microorganisms 18 3.2 Geometric Hindrance and Predation 21 3.3 Soil Structure Defines Local Physicochemical Conditions 22 3.4 Arrangement and Aggregation of Soil Particles 24 4 Future Prospects 27 4.1 Extend Studies from Model Systems to Natural Systems 27 4.2 Define the Spatial Distributions of Microorganisms in Soil 28 5 Summary 28 References 29
Understanding how soil characteristics control the activity of microorganisms in soil is essential to predict the occurrence and rate of microbially mediated functions that are of agronomic and environmental importance, such as nitrogen mineralization, denitrification, biological nitrogen fixation, turnover of C and N, stability of soil structure, biodegradation of organic pollutants, soil-borne pathogenicity, etc. Such knowledge is also needed to optimize the success of microorganisms purposely introduced to soil and to improve the bioremediation of pollutants.
Microorganisms in soil live in an ecosystem that is dominated by solid particles, some of which have large surface area (Table 1). Soils have specific surface areas that are variable and depend on the texture and mineralogy of the soils (Table 2). The colloidal fraction of these particles can exhibit permanent (e.g., most clay minerals) or variable charges (e.g., oxyhydroxides, organic matter) (Table 1). These colloids are considered to be surface-active particles. The surface area attributable to a bacterial population of [10.sup.10] cells [g.sup.-1] of soil is small compared with the total specific surface area or the external surface area of soils with different textures (Table 2). If the bacteria were spread as a monolayer on the surface area of soil particles, they would probably cover only a small fraction of it. Moreover, the ratio of the surface area of the solid particles to the volume of the liquid phase is high in soils. Hence, the surfaces of soil particles, especially those of surface-active particles, are likely to act as sinks for microbial metabolites.
The spatial arrangement of the solid particles results in a complex and discontinuous pattern of pore spaces of various sizes and shapes that are more or less filled with water or air (Table 2 and Figure 1). This is the habitat of soil microorganisms. Soil may be best defined as the juxtaposition of a multitude of microenvironments or microhabitats, characterized by a variety of physical and chemical conditions. Some of these microhabitats are represented in Figure 2. Bacteria and unicellular algae are 'aquatic' organisms in the sense that they rely on diffusion of organic and inorganic compounds in water for their nutrition. Bacteria, including actinomycetes, and unicellular algae can be free or attached to surfaces of particles, located in water-filled pores, or surrounded by a film of water on the walls of air-filled pores (Figure 2). When attached to surfaces, bacteria may occur as scattered individual cells, micro-colonies, or as biofilms. Fungi can occupy the same locations; in addition, fungal hyphae can extend through unsaturated pores (Figure 2). Soil microhabitats are discrete, not always accessible to microorganisms, and not always interconnected. However, the accessible pore space, i.e., the pore space that is filled with water and in which microorganisms may enter (pore necks larger than the dimensions of microorganisms), is unlikely to be limiting in soils, because microorganisms occupy only a small volume of soil (Table 2).
The survival of microorganisms and the rate of their biological functions have been shown to vary widely with soil type and soil management. However, despite the many studies that have been performed and the statistical relations that have been established between soil characteristics and biological functions, they do not enable sufficient prediction and control of most functions (e.g., [1,2]). The precise nature of the interactions between soil constituents and microorganisms must be known to identify the soil characteristics that actually control survival and activity of microorganisms. This should enable relevant descriptive parameters (e.g., pore size distribution, abundance of montmorillonite) to be defined and, then, to allow realistic predictions of the overall phenomena, especially in simulation models.
The interactions between microorganisms and soil particles can be broadly classified into biological and abiological. Biological interactions involve the growth and multiplication of cells and the secretion of organic substances, such as enzymes and other biopolymers. Abiotic interactions involve physical and physicochemical interactions. Physical interactions relate to the geometry and cohesion of the soil matrix. They include, for example, pore size distribution, water retention, aggregate stability, and mechanical properties of soil. Physical interactions are highly dependent on the size, shape, and spatial arrangement of soil particles, as well as on their surface properties. Physicochemical interactions include processes at interfaces or in the soil solution, e.g., sorption, dissolution, hydrolysis, oxidation, and parameters such as pH. Characteristics of the surface of particles, i.e., surface area, electrostatic charge, surface free energy, and functional groups, are important here. Interactions between microorganisms and the soil environment often simultaneously involve biological, physical, and physicochemical processes.
Interactions between soil microorganisms and soil particles are bidirectional. Soil particles influence the survival and biological activity of microorganisms, partly by controlling the geometry of pores in which microorganisms live and the local physicochemical conditions. Microorganisms, despite being minor soil constituents, affect soil particles by modifying their arrangement or aggregating them, weathering mineral particles or contributing to the precipitation and formation of new mineral particles, and degrading organic particles.
This chapter provides an overview of the interactions between soil microorganisms and mineral and organic particles in soil. The overview is not exhaustive, and its main purpose is to emphasize recent developments as well as important gaps in knowledge. Possible interactions between microorganisms and soil particles are summarized in Figure 3, of which only some will be discussed. The reader is referred to other reviews for further information, e.g., 3-7]. Surface interactions will be discussed before interactions that are related to the spatial arrangement of soil particles.
2 SURFACE INTERACTIONS BETWEEN MICROORGANISMS AND SOIL PARTICLES
Surface interactions between microorganisms and soil particles can be indirect, as the surface properties of soil particles can affect the composition of the soil solution (e.g., the cation-exchange capacity (CEC) of soil particles controls, to a great extent, the cation concentration of cations in the soil solution). Adsorption, which is the concentration of adsorbates (microbial cells, organic molecules) at the interface between the soil solution or atmosphere and a solid particle, the adsorbent, is a direct surface interaction between microorganisms and soil particles. Such concentration at the interface is the result of physical or chemical forces between the adsorbate and the adsorbent. The term adhesion is generally used when the adsorbate is also a solid particle, e.g., a bacterium. The term binding will be used herein to describe nonreversible adsorption. The term sorption is often used in a more general sense to describe situations where a molecule or biological entity is absent from the soil solution, as the result of adsorption, entrapment in soil aggregates, dissolution in the hydrophobic portions of soil organic matter, or even absorption by living organisms.
2.1 ADHESION OF MICROORGANISMS TO SURFACES
Surface interactions of microorganisms with soil particles involve several steps: (i) transport to the surface, (ii) contact and initial adhesion, (iii) firmer attachment, and then (iv) growth, to form adhering microcolonies or biofilms. The initial adhesion is rapid (seconds, minutes) and can be reversible or nonreversible. It is a physicochemical process, which is described and reasonably well predicted by theories of colloid chemistry, such as the Derjaguin-Landau-Verwey-Overbeek (DLVO) theory for electrostatic interactions (e.g., ) and Lewis-acid/base hydrophobic interactions. Most data on microbial adhesion have been obtained with bacteria and have shown that adhesion depends on the surface properties of the cells and on their physiological state. Bacteria and fungi may, in a second step with a time scale of hours or days, synthesize extracellular polymers, such as polysaccharides or proteins, which have been shown to anchor the cells more firmly.
Data exist on the extent and mechanisms of adhesion of microbial cells to pure solid surfaces, such as those of polymers, anion exchange resins, quartz, or mica, from studies with model systems. However, polymeric materials differ from soil particles in their composition and properties. Quartz and mica particles are present in soil, but they have surface electrostatic charges and reactivity very different from those of clay minerals (Table 1). Few studies have focused on the adhesion of bacteria and fungi to clay minerals, because of experimental difficulties. Measuring adhesion between particles of different nature and of similar small size is particularly difficult because these particles cannot easily be distinguished and separated. The adhesion of bacteria to clay particles also poses a conceptual problem as both constituents are usually net negatively charged. According to the diffuse double layer theory, bacterial cells have to overcome a potential energy barrier to come into contact with clay surfaces. Possible ways to overcome this barrier are cation bridging, water bridging, polymer bridging through extracellular polymers, or high ionic strength of the soil solution. Furthermore, many of the surfaces of soil particles are not clean but are coated with mineral or organic compounds that may change the overall surface properties of the particles.
In soils, microorganisms are observed to adhere to particles larger than their cells, such as sand grains (Figure 4a) or plant residues (Figure 4b and c). Adhesion of bacteria to smaller-sized particles results in mineral coatings of the cell envelope, often described as 'bacterial microaggregates' (Figure 4d). Biofilms are also observed adhering to the surface of soil aggregates (Figure 4e). Other than such morphological evidence, scant direct quantification exists of adhesion of microorganisms to mineral surfaces in soils. It is often suggested that the limited extent of leaching of bacteria from soils and the difficulty in separating microorganisms from soils are the result of adhesion. However, in all experiments where the retention of microorganisms by soils was quantified, no clear distinction was made between adhesion to surfaces and entrapment in soil aggregates or narrow pores (e.g., ).
There is relative agreement in the literature that solid surfaces can influence microbial activities, but experimental observations are often contradictory, and most data are restricted to model systems and to particles other than clays. Positive and negative effects of adhesion on substrate utilization, nitrification, respiration, and growth have been demonstrated and extensively reviewed by Stotzky. These effects were, or could be, interpreted by an indirect action of surfaces, as most observed effects were the result of a modification of the composition of the soil solution through the adsorption or desorption of protons, substrates, nutrients, or enzymes on the mineral surfaces. For example, montmorillonite affected bacterial metabolism in part by buffering the pH of the suspension and maintaining it within the optimal range for growth. The decreased rate of growth of microcolonies of Pseudomonas fluorescens when adhering to glass was explained by limitations in diffusion of the substrates in the immediate vicinity of the cell. Similarly, Harms and Zehnder found that the degradation of polychlorinated dibenzofuran by Sphingomonas cells was lower for cells attached to glass beads than for free ones. Specific cell activities were unchanged, but substrate transport was limited for adhering cells because less liquid medium surrounded attached than free cells. In addition, the diffusion zones of adjacent adhering cells overlapped. There has been much debate on the idea that bacteria at surfaces are at an advantage because of the concentration of mineral nutrients and organic substrates at the interface. Experimental studies on substrate utilization by free and attached bacteria have shown variable results, confirming this hypothesis in a few cases (e.g. [26,27]) but not in general.
In soils or sediments, adhesion of cells to solid surfaces may result in the creation of a new microenvironment for microbes, consisting of extracellular slime, clay coatings, or both. In these microenvironments, diffusion of substrates or [O.sub.2] is likely to be limited (see next section).
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Table of Contents
List of Contributors.
PART I: FUNDAMENTALS OF SOIL PARTICLE-MICROORGANISM INTERACTIONS.
Interactions between Microorganisms and Soil Particles: An Overview (C. Chenu and G. Stotzky).
A Fractal Approach for Interactions between Soil Particles and Microorganisms (N. Senesi and L. Boddy).
Interactions of Organic Materials and Microorganisms with Minerals in the Stabilization of Structure (J. A. Baldock).
Impact of Organic Substances on the Formation and Transformation of the Metal Oxides in Soil Environments (A. Violante, G. S. R. Krishnamurti and P. M. Huang).
Microbial Mobilization of Metals from Soil Minerals under Aerobic Conditions (E. Kurek).
Interactions of Bacteria and Environmental Metals, Fine-grained Mineral Development and Bioremediation Strategies (J. S. McLean, J.-U. Lee and T. J. Beveridge).
PART II: IMPACT OF SOIL PARTICLE-MICROORGANISM INTERACTIONS ON THE TERRESTRIAL ENVIRONMENT.
(A) ION CYCLING AND ORGANIC POLLUTANT TRANSFORMATION.
Effect of Mineral Colloids on Biogeochemical Cycling of C, N, P and S in Soil (G. Guggenberger and K. M. Haider).
Impact of Interactions between Microorganisms and Soil Colloids on the Transformation of Organic Pollutants (J. Dec, J.-M. Bollag, P. M. Huang, and N. Senesi).
(B) RHIZOSPHERE CHEMISTRY AND BIOLOGY.
Chemical and Biological Processes in the Rhizosphere: Metal Pollutants (P. M. Huang and J. J. Germida).
Biotic and Abiotic Interactions in the Rhizosphere: Organic Pollutants (T. A. Anderson, D. P. Shupack and H. Awata).
(C) ANAEROBIC AND TRANSPORT PROCESSES, AND THE SUBSURFACE TERRESTRIAL ENVIRONMENT.
Interactions between Microorganisms and Minerals under Anaerobic Conditions (H. L. Ehrlich).
The Role of Mineral Colloids in the Facilitated Transport of Contaminants in Saturated Porous media (M. Elimelech and J. N. Ryan).