SOIL MICROBIOLOGY,

ECOLOGY, AND

BIOCHEMISTRY

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

EDITOR
ELDOR A. P A U L

Universitats- und Landes-

bibliothek 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

 CONTENTS

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 I I

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
CONTENTS 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

S O I L 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
CONTENTS IX

6
FUNGI AND EUKARYOTIC ALGAE
R. G. THORN AND M. D. J . LYNCH

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: T H E 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
 CONTENTS

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
CONTENTS 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
 CONTENTS

ibution within the Soil Profile 292

leterogeneity in Microbial Populations 296
nd Suggested Reading 299

PART I V

HEMISTRY AND BIOGEOCHEMISTRY

12
CYCLING AND FORMATION OF S O I L
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
CONTENTS XIII

13
NITROGEN TRANSFORMATIONS
G. P. ROBERTSON AND P. M. GROFFMAN

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 N2-Fixing Bacteria 372
Associative N2-Fixing Bacteria 373
Phototrophic Bacteria 374
Symbiotic N2-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 CONTENTS

15
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
CONTENTS 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