Soil Microbiology,

Ecology, and

Biochemistry

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AMSTERDAM • BOSTON • HEIDELBERG • LONDONNEW YORK • OXFORD • PARIS • SAN DIEGO

SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO

Academic Press is an imprint of Elsevier

Soil Microbiology,

Ecology, and

Biochemistry

T H I R D E D I T I O N

EditorEldor A. Paul

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Academic Press is an imprint of Elsevier30 Corporate Drive, Suite 400, Burlington, MA 01803, USALinacre House, Jordan Hill, Oxford OX2 8DP, UK

Third edition 2007

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Library of Congress Cataloging-in-Publication Data

Soil microbiology, ecology, and biochemistry / editor, Eldor A. Paul. — 3rd ed.p. cm.

Rev. ed. of: Soil microbiology and biochemistry / E.A. Paul, F.E. Clark. 1989.Includes bibliographical references and index.ISBN 13: 978-0-12-546807-7 (hardcover : alk. paper)ISBN 10: 0-12-546807-5 (hardcover : alk. paper) 1. Soil microbiology. 2. Soil biochemistry.

I. Paul, Eldor Alvin. II. Paul, Eldor Alvin. Soil microbiology and biochemistry.QR111.P335 2007579�.1757—dc22

2006036420

Typeset by Charon Tec Ltd (A Macmillan Company), Chennai, Indiawww.charontec.comPrinted in the United States of America

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Contributors xviiPreface xix

PART I

Background

1Soil Microbiology, Ecology and Biochemistry

in PerspectiveE. A. Paul

General History and Scope 3Soil Microbiology 5Soil Ecology 10Soil Biochemistry 13In Perspective 19References and Suggested Reading 21

Contents

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2The Soil Habitat

R. P. Voroney

Introduction 25Soil Genesis and Formation of the Soil Habitat 26

Soil Profile 29Physical Aspects of Soil 29

Soil Texture 30Soil Structure 32

Soil Habitat Scale and Observation 33Scale of Soil Habitat 33Pore Space 35Soil Solution Chemistry 39Soil pH 43Soil Temperature 43Soil Water Content 45Environmental Factors, Temperature and Moisture Interactions 48

References and Suggested Reading 49

PART II

SOIL BIOTA

3Physiological and Biochemical Methods for

Studying Soil Biota and Their FunctionE. Kandeler

Introduction 53Scale of Investigations and Collection of Samples 54Storage and Pretreatment of Samples 56Microbial Biomass 57

Chloroform Fumigation Incubation and Extraction Methods 57Substrate-Induced Respiration 58Isotopic Composition of Microbial Biomass 58

Signature Molecules as a Measure of Microbial Biomass and MicrobialCommunity Structure 59

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ATP as a Measure of Active Microbial Biomass 59Microbial Membrane Components and Fatty Acids 60Respiratory Quinones as a Measure of Structural Diversity 62Ergosterol as a Measure of Fungal Biomass 63Lipopolysaccharides, Glycoproteins, and Cell Walls 64Growth Rates from Signature Molecules 65

Physiological Analyses 65Culture-Based Studies 65Isolation and Characterization of Specific Organisms 66Soil Organic Matter Decomposition and Respiration 67Nitrogen Mineralization 72

Activities and Locations of Enzymes 72Spectrophotometric Methods 73Fluorescence Methods 75Techniques for Imaging the Location of Enzymes 77

Functional Diversity 77References and Suggested Reading 80

4Molecular Methods for Studying

Soil EcologyJ. E. Thies

Introduction 85Types and Structures of Nucleic Acids 86Use of Nucleic Acid Analyses for Soil Ecology Studies 88Direct Molecular Analysis of Soil Biota 90

Nucleic Acid Hybridization 90Confocal Microscopy 91

Biosensors and Marker Gene Technologies 92Extraction of Nucleic Acids (DNA/RNA) 93Choosing between DNA and RNA for Soil Ecology Studies 96Analysis of Nucleic Acid Extracts 96

DNA:DNA Reassociation Kinetics 96Microarrays 98Restriction Fragment Length Polymorphism (RFLP) Analysis 100Cloning 101DNA Sequencing 102Stable Isotope Probing 102

Partial Community Analyses—PCR-Based Assays 104Electrophoresis of Nucleic Acids 107

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PCR Fingerprinting 107Similarity Analyses 112

Level of Resolution 112Other Factors That May Affect Molecular Analyses 113

Sample Handling 113Soil Chemical Factors 113Sampling Scale 114

Summary 114References 115

5The Prokaryotes

K. Killham and J. I. Prosser

Introduction 119Phylogeny 120

Cultivated Organisms 120Uncultivated Organisms 121Phylogeny and Function 125

General Features of Prokaryotes 126Cell Structure 127

Unicellular Growth Forms 127Filamentous and Mycelial Growth 129Cell Walls 129Internal Structure 131Motility 132

Metabolism and Physiology 132Carbon and Energy Sources 132Oxygen Requirements 133Substrate Utilization 134Autochthony and Zymogeny 136Oligotrophy, Copiotrophy, and the R–K Continuum 137Facultativeness 138

Biodegradation Capacity 138Cellulose 138Pollutants 139

Differentiation, Secondary Metabolism, and Antibiotic Production 141Conclusions 142References and General Reading 143

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6Fungi and Eukaryotic Algae

R. G. Thorn and M. D. J. Lynch

Introduction 145Classification, Characteristics, and Ecological Roles in Soil 151

Fungus-like Protists 151Fungi (Chytridiomycota, Glomeromycota, Zygomycota, Ascomycota, and

Basidiomycota) 153Eukaryotic Algae 156

References and Suggested Reading 158

7Fauna: The Engine for Microbial Activity and

TransportD. C. Coleman and D. H. Wall

Introduction 163The Microfauna 166

Methods for Extracting and Counting Protozoa 168Impacts of Protozoa on Ecosystem Function 168Distribution of Protozoa in Soil Profiles 169

Rotifera 169Nematoda 170

Nematode Feeding Habits 170Zones of Nematode Activity in Soil 173Nematode Extraction Techniques 174

Microarthropods 174Enchytraeids 175Macrofauna 178

Macroarthropods 178Importance of the Macroarthropods 179Oligochaeta (Earthworms) 179Formicidae (Ants) 183Termitidae (Termites) 183

Summary 185References 186

Contents ix

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PART III

CONCEPTS AND INTERACTIONS

8The Ecology of Soil Organisms

S. J. Morris and C. B. Blackwood

Introduction 195Mechanisms That Drive Community Structure 197

Physiological Limits 198Intraspecific Competition 199Dispersal in Space and Time 203Predicting Population Growth 204Interspecific Competition 204Direct Effects of Exploitation 207Indirect Effects of Exploitation 209Mutualisms 211Abiotic Factors 211Changes in Community Structure through Time and Space 212Historical and Geographic Contingency 214Hierarchical Community Assembly Rules 215

Ecosystem Dynamics 218Energy Flow 219Carbon, Nutrient, and Water Cycles 221Emergent Properties 224

Conclusion 225References and Suggested Reading 226

9The Physiology and Biochemistry of

Soil OrganismsW. B. McGill

Introduction 231Metabolic Classifications of Soil Organisms 233

Electrons and ATP 234Substrate-Level Phosphorylation 234

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Electron Transport Phosphorylation 235Overview of Mechanisms to Generate ATP and Reducing Equivalents 238

Examples of Soil Microbial Transformations 241Nitrogen Fixation 241Aerobic Chemolithotrophic Examples 242Oxidation of Reduced C 245

How Can the Microbial Contributions Be Viewed in a Simplified and Unified Concept? 251A Model of Interconnected Cycles of Electrons 252The Anoxygenic Cycle 253The Oxygenic Cycle 253

References 256

10The Ecology of Plant–Microbial Mutualisms

J. Powell and J. Klironomos

Introduction 257Roots as an Interface for Plant–Microbial Mutualisms 258Mycorrhizal Symbioses 259Symbioses Involving N-Fixing Organisms 267Interactions among Mutualists 270Interactions with Pathogens 272Implications for Plant Populations and Communities 275Challenges in the Study of Interactions 276Conclusions 277References and Suggested Reading 279

11Spatial Distribution of Soil Organisms

S. D. Frey

Introduction 283Geographical Differences in Soil Biota 285Association of Soil Organisms with Plants 287Spatial Heterogeneity of Soil Organisms 290

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Vertical Distribution within the Soil Profile 292Microscale Heterogeneity in Microbial Populations 296References and Suggested Reading 299

PART IV

BIOCHEMISTRY AND BIOGEOCHEMISTRY

12Carbon Cycling and Formation of Soil

Organic MatterW. Horwath

Introduction 303Long-Term Carbon Cycle 304The Short-Term C Cycle 307Ecosystem C Cycling 309Composition and Turnover of C Inputs to Soil 312

Plant and Microbial Lipids 315Starch 315Hemicelluloses, Pectins, and Cellulose 317Lignin 320Other Plant Cell Wall Carbohydrates and Proteins 324Plant Secondary Compounds 325Roots and Root Exudates 325Cell Walls of Microorganisms 327

Soil Organic Matter 329Soil Organic Matter Formation 329Classical Fractions of Soil Organic Matter 332Physical Analysis of Soil Organic Matter Fractions 333Structure of Soil Organic Matter 335

Quantity and Distribution of Organic Matter in Soils 335Role of Methane in the C Cycle 336Future Considerations 337References and Suggested Reading 337

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13Nitrogen TransformationsG. P. Robertson and P. M. Groffman

Introduction 341Nitrogen Mineralization and Immobilization 343Nitrification 347

The Biochemistry of Autotrophic Nitrification 347The Diversity of Autotrophic Nitrifiers 349Heterotrophic Nitrification 352Environmental Controls of Nitrification 353

Inhibition of Nitrification 355Denitrification 355

Denitrifier Diversity 356Environmental Controls of Denitrification 358

Other Nitrogen Transformations in Soil 359Nitrogen Movement in the Landscape 360References and Suggested Reading 362

14Biological N Inputs

P. J. Bottomley and D. D. Myrold

Global N Inputs 365Biological Nitrogen Fixation 367Free-Living N2-Fixing Bacteria 372Associative N2-Fixing Bacteria 373Phototrophic Bacteria 374Symbiotic N2-Fixing Associations between Legumes and Rhizobia 375

Formation of the Symbiosis 375Rhizobial Nodulation Genes 378Plant Nodulation Genes 380Development of BNF and Nitrogen Assimilatory Processes in Nodules 381Symbiotic Associations between Actinorhizal Plants and Frankia 383

Biotechnology of BNF 385Acknowledgments 386References and Suggested Reading 386

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15Soil Biogeochemical Cycling of Inorganic

Nutrients and MetalsA. F. Plante

Introduction 389Phosphorus 391

The Soil Phosphorus Cycle 391Nature and Forms of Phosphorus in Soil 393Biological Importance of Phosphorus 397Microbial Transformations of Phosphorus 398

Sulfur 400The Soil Sulfur Cycle 400Nature and Forms of Sulfur in Soil 402Biological Importance of Sulfur 406Microbial Transformations of Sulfur 406

Micronutrients and Trace Metals 413Micronutrient and Trace Metal Cycling in Soil 413Nature and Forms in Soil 414Biological Importance 415Microbial Transformations 417

Environmental Significance of P, S, and Metal Biogeochemistry 423Eutrophication 423Acid Sulfate Soils 423Acid Mine Drainage 424Heavy Metal Mining Using Microbes 426Microbial Corrosion of Buried Iron and Concrete Pipes 427

Conclusion: Microorganisms as Unifiers of Elemental Cycles in Soil 430References and Suggested Reading 430

16The Dynamics of Soil Organic Matter and

Nutrient CyclingA. F. Plante and W. J. Parton

Introduction 433Reaction Kinetics 434

Zero-Order Reactions 434First-Order Reactions 435

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Enzymatic Kinetics 436Microbial Growth 437

Modeling the Dynamics of Decomposition and Nutrient Transformations 439Simple Models 441Multicompartmental Models 443Alternative SOM Models 453Models of Non-C Nutrient Elements 454Ecosystem Models: Interactions of Nutrient Cycling and SOM

Dynamics 457Establishing Pool Sizes and Kinetic Constants 459Model Selection and Evaluation 461References and Suggested Reading 464

PART V

Soil Organisms: Man and Nature

17Management of Organisms and Their Processes

in SoilsJ. L. Smith and H. P. Collins

Introduction 471Changing Soil Organism Populations and Processes 473

Tillage and Erosion 474Rangeland and Forest Health 477

Alternative Agricultural Management 480Organic Agriculture 480Biodynamic Agriculture 482Composting 483Crop Rotations and Green Manures 486

The Potential for Managing Microorganisms and Their Processes 487Management of Native and Introduced Microorganisms 487Managing Microbial Populations as Agents of Biological Control 488Control of Insects 490Weed Control 492Use of Synthetic and Natural Compounds to Modify Soil Communities

or Functions 493Manipulating Soil Populations for Bioremediation of Xenobiotics 495

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Concluding Comments on Microbial Ecology 499References and Suggested Reading 500

18Soil Microbiology, Ecology, and Biochemistry

for the 21st CenturyJ. Schimel

Introduction 503Soil Community Ecology—Controls over Population and Community

Dynamics 506Microbial Life at the Microbial Scale—the Microbial Landscape 507A Whole Profile Perspective 509Scaling to the Ecosystem 510Application 511Conclusions 512References 512

Index 515

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Christopher B. Blackwood Department of Biological Sciences, Kent StateUniversity, Kent, OH 44242

Peter J. Bottomley Department of Crop and Soil Science, Oregon State University,Corvallis, PR 97331-3804

David C. Coleman Institute of Ecology, University of Georgia, Athens, GA 30602-2360

Harold P. Collins USDA-ARS, Vegetable and Forage Research Unit, Prosser,WA 99350

Serita Frey Department of Natural Resources, University of New Hampshire,Durham, NH 03824

Peter M. Groffman Institute of Ecosystem Studies, Millbrook, NY 12545-0129

William H. Horwath Department of Land, Air, and Water Resources, Universityof California-Davis, Davis, CA 95616-8627

Ellen Kandeler Institute of Soil Science and Land Evaluation, Soil BiologySection, University of Hohenheim, D-70599 Stuttgart, Germany

Ken Killham School of Biological Sciences, University of Aberdeen, AberdeenAB24 3UU, Scotland

John Klironomos Department of Integrative Biology, College of BiologicalSciences, University of Guelph, Guelph, ON, N1G 2W1 Canada

Michael Lynch Department of Biology, University of Waterloo, Waterloo, OntarioN2L 3G1 Canada

W. Bill McGill University of Northern British Columbia, College of Science andManagement, Prince George, BC, Canada V2N 4Z9

Contributors

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Sherri J. Morris Biology Department, Bradley University, Peoria, IL 61625

David Myrold Department of Crop and Soil Science, Oregon State University,Corvallis, PR 97331-3804

Eldor A. Paul Natural Resource Ecology Laboratory and Soil and Crop Sciences,Colorado State University, Fort Collins, CO 80523-1499

William Parton Natural Resource Ecology Laboratory, Colorado State University,Fort Collins, CO 80523-1499

Alain Plante Department of Earth and Environmental Science, University ofPennsylvania, Philadelphia, PA 19104-6316

Jeff Powell Department of Integrative Biology, College of Biological Sciences,University of Guelph, Guelph, ON, N1G 2W1 Canada

Jim I. Prosser School of Biological Sciences, University of Aberdeen, Aberdeen4,Scotland AB24 3UU United Kingdom

G. Philip Robertson Department of Crop and Soil Sciences and W. K. KelloggBiological Station, Michigan State University, Hickory Corners, MI 49060

Joshua P. Schimel Department of Ecology, Evolution, and Marine Biology,University of California-Santa Barbara, Santa Barbara, CA 93106-9610

Jeffrey L. Smith USDA-ARS, Washington State University, Pullman, WA99164-6421

Janice E. Thies Department of Crop and Soil Science, Cornell University,Ithaca, NY

R. Greg Thorn Department of Biology, University of Western Ontario, London,ON, N6A 5B7 Canada

Paul Voroney Land Resource Science, University of Guelph, Guelph, ON, CanadaN1G 2W1

Diana H. Wall Natural Resource Ecology Laboratory and Department of Biology,Colorado State University, Fort Collins, CO 80523-1499

xviii Contributors

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Soil microbiology traditionally has been the study of microorganisms and theirprocesses in soil. The interaction of organisms with each other and their environ-ments involves soil ecology. Soil biochemistry includes microbial processes, soilenzymes, and the formation and turnover of soil organic matter. Soil, in thenonengineering definition, is usually defined as the surface of the earth affected byplant roots, even though life, especially that of microorganisms, occurs at greatdepths in geological deposits, caves, and sediments. Although the organismsinvolved are often different, their ecological and abiotic controls and the productsof their metabolism have great similarities in all locations. Thus, there is now arecognized similarity and interaction with soil and biogeochemical studies inmarine and fresh water systems, sediments, and the atmosphere. What we knowfrom these processes on earth will also guide future extraterrestrial investigationsand, as a result, the number of people interested in this field has greatly increased.The textbook “Soil Microbiology and Biochemistry” by Paul and Clark (1989,1996) is available in Chinese and Korean translations. It has been incorporatedinto the teaching of engineering, biogeochemistry, ecology, and general biology ina variety of university departments, including those of private, undergraduate, andteaching universities, and is widely used in many research applications.

The biological processes that occur in soil are intertwined with and inseparablefrom activities of the soil fauna, which feed on plants, soil microorganisms, andlitter. Their larger forms act as environmental engineers through their soil-mixingfunctions. They also contain microbial endophytes that carry out much of theirdecomposition function. The name of this edited volume has been changed toreflect its broader applicability and has been expanded to include both more basicand applied approaches. Soil microbiology, ecology, and biochemistry are being

Preface

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used in a broad range of applications from agronomy, plant pathology, general ecol-ogy, microbial ecology, engineering, organic agriculture, forestry, range manage-ment, and global change. We have thus included chapters on invertebrate–microbialinteractions, basic physiology, and ecological interpretations. Information on themanagement of microorganisms and their reactions has been expanded while wehave strived to retain readability, conciseness, and a reasonable cost.

The definition of microbiology is usually associated with organisms not seenwithout the use of a microscope, although this does not apply to many fungallichen and algal growth forms. The communal structure of the Armillaria associ-ated with tree roots in a number of areas is hectares in size, although it is still afungus by definition. The soil fauna also range in size and diversity. This bookreflects the great advances in molecular techniques, the broader use of tracers, andthe maturation of modeling in interpretation of data and development of new con-cepts. We finally know enough about our field to be able to impact management ofsuch modern problems as biodiversity, biological invasions, global change,ecosystem services, sustainable agriculture, and urban ecosystems. This textbookhas been designed to provide access to necessary knowledge for those working inthese diverse fields. The authors of the individual chapters hope that the readerswill find this a readable, accessible introduction to both the concepts involved andthe background literature.

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