MICROBIAL ECOLOGY FUNDAMENTALS AND APPLICATIONS. An imprint of Addison Wesley Longman, Inc.

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1 2 MICROBIAL ECOLOGY FUNDAMENTALS AND APPLICATIONS f o u r t h e d i t i o n RONALD M. ATLAS UNIVERSITY OF LOUISVILLE RICHARD BARTHA RUTGERS UNIVERSITY An imprint of Addison Wesley Longman, Inc. Menlo Park, California Reading, Massachusetts New York Harlow, England Don Mills, Ontario Sydney Mexico City Madrid Amsterdam

2 CONTENTS PARTI ECOLOGY AND EVOLUTION 1 CHAPTER 1 Microbial Ecology: Historical Development 2 The Scope of Microbial Ecology 2 Historical Overview 3 The Beginnings of Microbiology 5 The Pure Culture Period 7 Microbial Ecology in the Twentieth Century 8 Martinus Beijerinck: Personality and Science 10 Relation of Microbial Ecology to General Ecology and the Environmental Sciences 13 Sources of Information for the Microbial Ecologist 16 Chapter Summary 23 Study Questions 24 References and Suggested Readings 24 CHAPTER 2 Microbial Evolution and Biodiversity 27 The Origins of Life 27 Chemical Evolution 29 Cellular Evolution 3 \-' J Did Life Evolve Extraterrestrially? 32 Ribosomal RNA Analyses for Tracing Microbial Evolution 36 Evolution of Organelles 39 Genetic Basis for Evolution 41 Evolution of Physiological Diversity 43 Microbial Biodiversity 45 Bacterial Biodiversity 45 Archaeal Biodiversity 46 Eucaryal Biodiversity. 49 Chapter Summary 52 Study Questions 53 References and Suggested Readings 54 PART II POPULATION INTERACTIONS 59 CHAPTER 3 Interactions Among Microbial Populations 60 Interactions Within a Single Microbial Population 60

3 vi Contents Positive Interactions 61 v, Negative Interactions 63 Interactions Between Diverse Microbial Populations 65 Populations Within Biofilms 66 Neutralism 67 Commensalism 68 Synergism (Protocooperation) 71 Mutualism 76 Competition 80 Amensalism (Antagonism) 83 Parasitism 85 Predation 88 Chapter Summary 91 Study Questions 93 References and Suggested Readings 93 CHAPTER 4 Interactions Between Microorganisms and Plants 99 Interactions with Plant Roots 99 The Rhizosphere 99 Mycorrhizae 103 Nitrogen Fixation in Nodules 108 Nitrogen-Fixing Associations Between Rhizobia and Legumes 108 Nonleguminbus Nitrogen-Fixing Mutualistic Relationships 115 Interactions with Aerial Plant Structures 116 Microbial Diseases of Plants Plant Pathogens 119 Emerging and Reemerging Diseases of Plants 122 Viral Diseases of Plants 124 Bacterial Diseases of Plants 125 Fungal Diseases of Plants 128 Chapter Summary 131 Study Questions 133 References and Suggested Readings 133 CHAPTER 5 Microbial Interactions with Animals 141 Microbial Contributions to Animal Nutrition 141 Predation on Microorganisms by Animals 141 Cultivation of Microorganisms by Animals for Food and Food Processing 143 Commensal and Mutualistic Intestinal Symbionts 147 Digestion Within the Rumen 149 Mutualistic Associations of Invertebrates with Photosynthetic Microorganisms 153 Mutualistic Associations of Invertebrates with Chemolithotrophic and Methanotrophic Microorganisms 155 Fungal Predation on Animals 157 Nematode- and Rotifer-Trapping Fungi 157 Fungal-Scale Insect Associations 159 Other Symbiotic Relationships 160 Symbiotic Light Production 160 Novel Procarydtic Endosymbionts 161 Ecological Aspects of Animal Diseases 162 Ecology of Emerging Infectious Diseases 166 Chapter Summary 167 Study Questions 167 References and Suggested Readings 168 PART III MICROBIAL COMMUNITIES AND ECOSYSTEMS 173 CHAPTER 6 Development of Microbial Communities 174 Microbial Community Dynamics 174 Population Selection Within Communities: r and K Strategies 175 Succession Within Microbial Communities 177

4 Contents vii Succession Within Biofilm Communities 179 Genetic Exchange in Microbial Communities 186 Structure of Microbial Communities 188 Diversity and Stability of Microbial Communities 188 Risks of Introducing Genetically Modified Microorganisms 189 Species Diversity Indices 191 Genetic/Molecular Diversity Indices 193 Ecosystems 196 Experimental Ecosystem Models 196 Mathematical Models 199 Microbial Communities in Nature 204 Microbes Within Macro-communities 204 Structure and Function of Some Microbial Communities 204 Chapter Summary 207 Study Questions 209 References and Suggested Readings 209 CHAPTER 7 Quantitative Ecology: Numbers, Biomass, and Activities 218 Sample Collection 218 Soil Samples 219 Water Samples 220 Sediment Samples 222 Air Samples 222 Biological Samples 222 Sample Processing 223 Detection of Microbial Populations 225 Phenotypic Detection 225 Lipid Profile Analysis 226 Molecular Detection 228 Determination of Microbial Numbers 235 Direct Count Procedures 236 Viable Count Procedures 242 Detecting Nonculturable Bacteria 246 Determination of Microbial Biomass 249 Biochemical Assays 249 Physiological Approaches to Biomass Determination 253 Measurement of Microbial Metabolism 254 Heterotrophic Potential 254 Productivity and Decomposition 256 Specific Enzyme Assays 260 Chapter Summary 261 Study Questions 263 References and Suggested Readings 263 CHAPTER 8 Physiological Ecology of Microorganisms: Adaptations to Environmental Conditions 281 Abiotic Limitations to Microbial Growth 281 Liebig's Law of the Minimum 281 Shelford's Law of Tolerance 282 Starvation Strategies 284 Environmental Determinants 290 Temperature 291 Longevity in Adversity 292 Radiation 30 l x Pressure 305 Salinity 308 Water Activity 309 Movement 313 Hydrogen Ion Concentration 314 Redox Potential 316 Magnetic Force 317 Organic Compounds 318 Inorganic Compounds 320 Chapter Summary 324 Study Questions 325 References and Suggested Readings 325

5 viii Contents CHAPTER 9 Microorganisms in Their Natural Habitats: Air, Water, and Soil Microbiology 332 The Habitat and Its Microbial Inhabitants 332 Atmo-Ecosphere 333 Characteristics and Stratification of the Atmosphere 333 The Atmosphere as Habitat and Medium for Microbial Dispersal 334 Microorganisms in the Atmo-Ecosphere 338 Hydro-Ecosphere 340 Freshwater Habitats 341 Composition and Activity of Freshwater Microbial Communities 348 Marine Habitats 352 Characteristics and Stratefication of the Ocean 353 Composition and Activity of Marine Microbial Communities 357 Rocks 362 Soils 362 >' Litho-Ecosphere 362 Deep Subsurface Microbiology 364 Determining Soil Texture and Humic Acid Characteristics 368 Chapter Summary 374 Extreme Habitats 375 Study Questions 379 References and Suggested Readings 379 PART IV BIOGEOCHEMICAL CYCLING 385 CHAPTER 10 Biogeochemical Cycling: Carbon, Hydrogen, and Oxygen 386 Biogeochemical Cycling 386 Resevoirs and Transfer Rates 387 The Carbon Cycle 389 Carbon Transfer Through Food Webs 391 Combatting the Greenhouse Effect with Microorganisms 394 Carbon Cycling Within Habitats 397 Methanogenesis and Methylotrophy 398 Acetogenesis 399 Carbon Monoxide Cycling 399 Limitations to Microbial Carbon Cycling 400 Microbial Degradation of Polysaccharides 401 Microbial Degradation of Lignin 403 Biodegradation and Heterotrophic Production in Aquatic Environments 405 The Hydrogen Cycle 406 The Oxygen Cycle 408 Chapter Summary 409 Study Questions 410 References and Suggested Readings 410 CHAPTER 11 Biogeochemical Cycling: Nitrogen, Sulfur, Phosphorus, Iron, and Other Elements 414 The Nitrogen Cycle 414, Fixation of Molecular Nitrogen 416 Ammonification 421 Nitrification 421 Nitrate Reduction and Denitrification 423 The Sulfur Cycle 425 Management of the Nitrogen Cycle in Agriculture 426 Oxidative Sulfur Transformations 428 Reductive Sulfur Transformations 430 Winogradsky Column 432 Interactions of Sulfur and Iron Cycling 437 Smog and Acid Rain 439 The Phosphorus Cycle 437 The Iron Cycle 440

6 Contents ix The Manganese Cycle 444 Calcium Cycling 446 Silicon Cycling 447 Metal Cycling 448 Interrelations Between the Cycling of Individual Elements 448 Chapter Summary 450 Study Questions 453 References and Suggested Readings 454 PART V BIOTECHNOLOGICAL ASPECTS OF MICROBIAL ECOLOGY 461 CHAPTER 12 Ecological Aspects of Biodeterioration Control and Soil, Waste, and Water Management 462 Control of Biodeterioration 462 Management of Agricultural Soils 465 Fouling Biofilms 466 Treatment of Solid Waste 469 Landfills 469 Composting 470 Treatment of Liquid Wastes 476 Biological Oxygen Demand 477 Fixed Film Sewage Treatment Systems 480 Suspended Cell Sewage Treatment Systems 483 Tertiary Treatments 497 Disinfection 498 Treatment and Safety of Water Supplies 499 Water Quality Testing 500 Chapter Summary 503 Safe Drinking Water 504 Study Questions 506 References and Suggested Readings 507 CHAPTER 13 Microbial Interactions with Xenobiotic and Inorganic Pollutants Persistence and Biomagnification of Xenobiotic Molecules 512 Recalcitrant Halocarbons 514 Recalcitrant Nitroaromatic Compounds Polychlorinated Biphenyls and Dioxins Synthetic Polymers 521 Alkyl Benzyl Sulfonates 523 Petroleum Hydrocarbons 523 Pesticides 531 Microbial Interactions with Some Inorganic Pollutants 535 Acid Mine Drainage Biochemistry and Genetics of2,4-d Biodegradation Microbial Conversions of Nitrate 541 Microbial Methylations 543 Microbial Accumulation of Heavy Metals and Radionuclides 546 Chapter Summary 547 Study Questions 548 References and Suggested Readings 549 CHAPTER 14 Biodegradability Testing and Monitoring the Bioremediation of Xenobiotic Pollutants Biodegradability and Ecological Side Effect Testing 556 Testing for Biodegradability and Biomagnification 556 Biosensor Detection of Pollutants 560 Testing for Effects on Microoganisms 561 Bioremediation 562 Bioremediation Efficacy Testing 563 Side Effects Testing 564 Approaches to Bioremediation 566

7 Contents Environmental Modification for Bioremediation 566 Microbial Seeding and Bioengineering Approaches to the Bioremediation of Pollutants 570 Bioremediation of Various Ecosystems 573 Bioremediation of Contaminated Soils and Aquifers 573 Bioremediation of Marine Oil Pollutants 581 Bioremediation of the Exxon Valdez Alaskan Oil Spill 582 Bioremediation of Air Pollutants 585 Chapter Summary 588 Study Questions 590 References and Suggested Readings 590 CHAPTER 15 Microorganisms in Mineral and Energy Recovery and Fuel and Biomass Production 599 Recovery of Metals 599 Microbial Assimilation of Metals 602 Bioleaching of Copper and Gold 603 Uranium Bioleaching 604 Phosphate Recovery 605 Recovery of Petroleum 605 Production of Fuels 607 Ethanol 608 Methane 610 Hydrocarbons Other Than Methane 612 Hydrogen 612 Biotechnological Production of Hydrogen to Reverse Global Warming 613 Production of Microbial Biomass 614 Single-Cell Protein Production 614 Mushroom Production 616 Chapter Summary 617 Study Questions 618 References and Suggested Readings 619 CHAPTER 16 Microbial Control of Pests and Disease-Causing Populations 624 Modification of Host Populations 625 Immunization 626 Modification of Reservoirs of Pathogens 627 Modification of Vector Populations 628 Microbial Amensalism and Parasitism to Control Microbial Pathogens 628 Antifungal Amensalism and Parasitism 630 Antibacterial Amensalism and Parasitism 632 Microbial Pathogens and Predators for Controlling Pest Populations of Plants and Animals 632 Microbial Control of Insect Pests 633 Microbial Control of Other Animal Pests 640 Biological Control of Rabbits 641 Microbial Control of Weeds and Cyanobacterial Blooms 643 Bacterial Control of Dutch Elm Disease 644 Genetic Engineering in Biological Control 644 Frost Protection 646 Bacillus thuringiensis Pesticides 648 Other Applications 649 Additional Practical Considerations 650 Chapter Summary 651 Study Questions 652 References and Suggested Readings 652 Glossary 659 Index 675

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