SOIL MICROBIOLOGY, ECOLOGY, AND BIOCHEMISTRY



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SOIL MICROBIOLOGY, ECOLOGY, AND BIOCHEMISTRY T H I R D E D I T I O N EDITOR ELDOR A. PAUL Universitats- und Landesbibliothek Darmstadt Bibliothek Biologie AMSTERDAM. BOSTON HEIDELBERG LONDON NEW YORK OXFORD PARIS SAN DIEGO SAN FRANCISCO SINGAPORE SYDNEY TOKYO ELSEVIER Academic Press is an imprint of Elsevier

CONTRIBUTORS XVII PREFACE XIX PART I BACKGROUND SOIL MICROBIOLOGY, ECOLOGY AND BIOCHEMISTRY IN PERSPECTIVE E. A. PAUL General History and Scope 3 Soil Microbiology 5 Soil Ecology, 10 Soil Biochemistry 13 In Perspective 19 References and Suggested Reading 21

VI CONTENTS THE SOIL HABITAT R. P. VORONEY Introduction 25 Soil Genesis and Formation of the Soil Habitat 26 Soil Profile 29 Physical Aspects of Soil 29 Soil Texture 30 Soil Structure 32 Soil Habitat Scale and Observation 33 Scale of Soil Habitat 33 Pore Space 35 Soil Solution Chemistry 39 SoilpH 43 Soil Temperature 43 Soil Water Content 45 Environmental Factors, Temperature and Moisture Interactions 48 References and Suggested Reading 49 PART II SOIL BIOTA PHYSIOLOGICAL AND BIOCHEMICAL METHODS FOR STUDYING SOIL BIOTA AND THEIR FUNCTION E. KANDELER Introduction 53 Scale of Investigations and Collection of Samples 54 Storage and Pretreatment of Samples 56 Microbial Biomass 57 Chloroform Fumigation Incubation and Extraction Methods 57 Substrate-Induced Respiration 58 Isotopic Composition of Microbial Biomass 58 Signature Molecules as a Measure of Microbial Biomass and Microbial Community Structure 59

VII ATP as a Measure of Active Microbial Biomass 59 Microbial Membrane Components and Fatty Acids 60 Respiratory Quinones as a Measure of Structural Diversity 62 Ergosterol as a Measure of Fungal Biomass 63 Lipopolysaccharides, Glycoproteins, and Cell Walls 64 Growth Rates from Signature Molecules 65 Physiological Analyses 65 - Culture-Based Studies 65 Isolation and Characterization of Specific Organisms 66 Soil Organic Matter Decomposition and Respiration 67 Nitrogen Mineralization 72 Activities and Locations of Enzymes 72 Spectrophotometric Methods 73 Fluorescence Methods 75 Techniques for Imaging the Location of Enzymes 11 Functional Diversity 77 References and Suggested Reading 80 MOLECULAR METHODS FOR STUDYING SOIL ECOLOGY J. E. THIES Introduction 85 Types and Structures of Nucleic Acids 86 Use of Nucleic Acid Analyses for Soil Ecology Studies 88 Direct Molecular Analysis of Soil Biota 90 Nucleic Acid Hybridization 90 Confocal Microscopy 91 Biosensors and Marker Gene Technologies 92 Extraction of Nucleic Acids (DNA/RNA) 93 Choosing between DNA and RNA for Soil Ecology Studies 96 Analysis of Nucleic Acid Extracts 96 DNA:DNA Reassociation Kinetics 96 Microarrays 98 Restriction Fragment Length Polymorphism (RFLP) Analysis 100 Cloning 101 DNA Sequencing 102 Stable Isotope Probing 102 Partial Community Analyses PCR-Based Assays 104 Electrophoresis of Nucleic Acids 107

VI11 CONTENTS PCR Fingerprinting 107 Similarity Analyses 112 Level of Resolution 112 Other Factors That May Affect Molecular Analyses 113 Sample Handling 113 Soil Chemical Factors 113 Sampling Scale 114 Summary 114 References 115 THE PROKARYOTES K. KlLLHAM AND J. I. PROSSER Introduction 119 Phylogeny 120 Cultivated Organisms 120 Uncultivated Organisms 121 Phylogeny and Function 125 General Features of Prokaryotes 126 Cell Structure 127 Unicellular Growth Forms 127 Filamentous and Mycelial Growth 129 Cell Walls 129 Internal Structure 131 Motility 132 Metabolism and Physiology 132 Carbon and Energy Sources 132 Oxygen Requirements 133 Substrate Utilization 134 Autochthony and Zymogeny 136 Oligotrophy, Copiotrophy, and the R-K Continuum 137 Facultativeness 138 Biodegradation Capacity 138 Cellulose 138 Pollutants 139 Differentiation, Secondary Metabolism, and Antibiotic Production 141 Conclusions 142 References and General Reading 143

6 FUNGI AND EUKARYOTIC ALGAE R. G. THORN AND M. D. J. LYNCH IX Introduction 145 Classification, Characteristics, and Ecological Roles in Soil 151 Fungus-like Protists 151 Fungi (Chytridiomycota, Glomeromycota, Zygomycota, Ascomycota, and Basidiomycota) 153 Eukaryotic Algae 156 References and Suggested Reading 158 FAUNA: THE ENGINE FOR MICROBIAL ACTIVITY AND TRANSPORT D. C. COLEMAN AND D. H. WALL Introduction 163 The Microfauna 166 Methods for Extracting and Counting Protozoa 168 Impacts of Protozoa on Ecosystem Function 168 Distribution of Protozoa in Soil Profiles 169 Rotifera 169 Nematoda 170 Nematode Feeding Habits 170 Zones of Nematode Activity in Soil 173 Nematode Extraction Techniques 174 Microarthropods 174 Enchytraeids 175 Macrofauna 178 Macroarthropods 178 Importance of the Macroarthropods 179 Oligochaeta (Earthworms) 179 Formicidae (Ants) 183 Termitidae (Termites) 183 Summary 185 References 186

PART III CONCEPTS AND INTERACTIONS 8 THE ECOLOGY OF SOIL ORGANISMS S. J. MORRIS AND C. B. BLACKWOOD Introduction 195 Mechanisms That Drive Community Structure 197 Physiological Limits 198 Intraspecific Competition 199 Dispersal in Space and Time 203 Predicting Population Growth 204 Interspecific Competition 204 Direct Effects of Exploitation 207 Indirect Effects of Exploitation 209 Mutualisms 211 Abiotic Factors 211 Changes in Community Structure through Time and Space 212 Historical and Geographic Contingency 214 Hierarchical Community Assembly Rules 215 Ecosystem Dynamics 218 Energy Flow 219 Carbon, Nutrient, and Water Cycles 221 Emergent Properties 224 Conclusion 225 References and Suggested Reading 226 9 THE PHYSIOLOGY AND BIOCHEMISTRY OF SOIL ORGANISMS W. B. McGlLL Introduction 231 Metabolic Classifications of Soil Organisms 233 Electrons and ATP 234 Substrate-Level Phosphorylation 234

XI Electron Transport Phosphorylation 235 Overview of Mechanisms to Generate ATP and Reducing Equivalents 238 Examples of Soil Microbial Transformations 241 Nitrogen Fixation 241 Aerobic Chemolithotrophic Examples 242 Oxidation of Reduced C 245 How Can the Microbial Contributions Be Viewed in a Simplified and Unified Concept? 251 A Model of Interconnected Cycles of Electrons 252 The Anoxygenie Cycle 253 The Oxygenie Cycle 253 References 256 1O THE ECOLOGY OF PLANT-MICROBIAL MUTUALISMS J. POWELL AND J. KLIRONOMOS Introduction 257 Roots as an Interface for Plant-Microbial Mutualisms 258 Mycorrhizal Symbioses 259 Symbioses Involving N-Fixing Organisms 267 Interactions among Mutualists 270 Interactions with Pathogens 272 Implications for Plant Populations and Communities 275 Challenges in the Study of Interactions 276 Conclusions 277 References and Suggested Reading 279 1 1 SPATIAL DISTRIBUTION OF SOIL ORGANISMS S. D. FREY Introduction 283 Geographical Differences in Soil Biota 285 Association of Soil Organisms with Plants 287 Spatial Heterogeneity of Soil Organisms 290

ibution within the Soil Profile 292 leterogeneity in Microbial Populations 296 nd Suggested Reading 299 PART IV HEMISTRY AND BIOGEOCHEMISTRY 12 CYCLING AND FORMATION OF SOIL ORGANIC MATTER W. HORWATH i 303 Carbon Cycle 304 rerm C Cycle 307 C Cycling 309 >n and Turnover of C Inputs to Soil 312 and Microbial Lipids 315 h 315 celluloses, Pectins, and Cellulose 317 n 320 r Plant Cell Wall Carbohydrates and Proteins 324 t Secondary Compounds 325 s and Root Exudates 325 Walls of Microorganisms 327 ic Matter 329 Organic Matter Formation 329 sical Fractions of Soil Organic Matter 332 ical Analysis of Soil Organic Matter Fractions 333 "ture of Soil Organic Matter 335 nd Distribution of Organic Matter in Soils 335 ethane in the C Cycle 336 nsiderations 337 s and Suggested Reading 337

13 NITROGEN TRANSFORMATIONS G. P. ROBERTSON AND P. M. GROFFMAN XIII Introduction 341 Nitrogen Mineralization and Immobilization 343 Nitrification 347 The Biochemistry of Autotrophic Nitrification 347 The Diversity of Autotrophic Nitrifiers 349 Heterotrophic Nitrification 352 Environmental Controls of Nitrification 353 Inhibition of Nitrification 355 Denitrification 355 Denitrifier Diversity 356 Environmental Controls of Denitrification 358 Other Nitrogen Transformations in Soil 359 Nitrogen Movement in the Landscape 360 References and Suggested Reading 362 14 BIOLOGICAL N INPUTS P. J. BOTTOMLEY AND D. D. MYROLD Global N Inputs 365 Biological Nitrogen Fixation 367 Free-Living N 2 -Fixing Bacteria 372 Associative N 2 -Fixing Bacteria 373 Phototrophic Bacteria 374 Symbiotic N 2 -Fixing Associations between Legumes and Rhizobia 375 Formation of the Symbiosis 375 Rhizobial Nodulation Genes 378 Plant Nodulation Genes 380 Development ofbnf and Nitrogen Assimilatory Processes in Nodules 381 Symbiotic Associations between Actinorhizal Plants and Frankia 383 Biotechnology of BNF 385 Acknowledgments 386 References and Suggested Reading 386

XIV 15 CONTENTS SOIL BIOGEOCHEMICAL CYCLING OF INORGANIC NUTRIENTS AND METALS A. F. PLANTE Introduction 389 Phosphorus 391 The Soil Phosphorus Cycle 391 Nature and Forms of Phosphorus in Soil 393 Biological Importance of Phosphorus 397 Microbial Transformations of Phosphorus 398 Sulfur 400 The Soil Sulfur Cycle 400 Nature and Forms of Sulfur in Soil 402 Biological Importance of Sulfur 406 Microbial Transformations of Sulfur 406 Micronutrients and Trace Metals 413 Micronutrient and Trace Metal Cycling in Soil 413 Nature and Forms in Soil 414 Biological Importance 415 Microbial Transformations 417 Environmental Significance of P, S, and Metal Biogeochemistry 423 Eutrophication 423 Acid Sulfate Soils 423 Acid Mine Drainage 424 Heavy Metal Mining Using Microbes 426 Microbial Corrosion of Buried Iron and Concrete Pipes All Conclusion: Microorganisms as Unifiers of Elemental Cycles in Soil 430 References and Suggested Reading 430 16 THE DYNAMICS OF SOIL ORGANIC MATTER AND NUTRIENT CYCLING A. F. PLANTE AND W. J. PARTON Introduction 433 Reaction Kinetics 434 Zero-Order Reactions 434 First-Order Reactions 435

XV Enzymatic Kinetics 436 Microbial Growth 437 Modeling the Dynamics of Decomposition and Nutrient Transformations 439 Simple Models 441 Multicompartmental Models 443 Alternative SOM Models 453 Models ofnon-c Nutrient Elements 454 Ecosystem Models: Interactions of Nutrient Cycling and SOM Dynamics 457 Establishing Pool Sizes and Kinetic Constants 459 Model Selection and Evaluation 461 References and Suggested Reading 464 PART V SOIL ORGANISMS: MAN AND NATURE 17 MANAGEMENT OF ORGANISMS AND THEIR PROCESSES IN SOILS J. L. SMITH AND H. P. COLLINS Introduction 471 Changing Soil Organism Populations and Processes 473 Tillage and Erosion 474 Rangeland and Forest Health All Alternative Agricultural Management 480 Organic Agriculture 480 Biodynamic Agriculture 482 Composting 483 Crop Rotations and Green Manures 486 The Potential for Managing Microorganisms and Their Processes 487 Management of Native and Introduced Microorganisms 487 Managing Microbial Populations as Agents of Biological Control 488 Control of Insects 490 Weed Control 492 Use of Synthetic and Natural Compounds to Modify Soil Communities or Functions 493 Manipulating Soil Populations for Bio remediation of Xenobiotics 495

XVI CONTENTS Concluding Comments on Microbial Ecology 499 References and Suggested Reading 500 18 SOIL MICROBIOLOGY, ECOLOGY, AND BIOCHEMISTRY FOR THE 21ST CENTURY J. SCHIMEL Introduction 503 Soil Community Ecology Controls over Population and Community Dynamics 506 Microbial Life at the Microbial Scale the Microbial Landscape 507 A Whole Profile Perspective 509 Scaling to the Ecosystem 510 Application 511 Conclusions 512 References 512 INDEX 515