Freshwater MicrobiologyBiodiversity and Dynamic Interactions of

Microorganisms in the Aquatic Environment

David C. SigeeUniversity of Manchester, UK

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Freshwater Microbiology

Freshwater MicrobiologyBiodiversity and Dynamic Interactions of

Microorganisms in the Aquatic Environment

David C. SigeeUniversity of Manchester, UK

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Library of Congress Cataloging-in-Publication Data

Sigee, D. C.Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the freshwater

environment / David C. Sigee.p. ; cm.

Includes bibliographical references and index.ISBN 0-471-48528-4 (cloth : alk. paper) – ISBN 0-471-48529-2 (pbk. : alk. paper) 1. Freshwater

microbiology.[DNLM: 1. Fresh Water – microbiology. QW 80 S574f 2004] I. Title.

QR105.5.S545 20045790.176–dc22 2004021738

British Library Cataloguing in Publication Data

A catalogue record for this book is available from the British Library

ISBN 0 471 48528 4 hardbackISBN 0 471 48529 2 paperback

Typeset in 10/12 pt Times by Thomson Press, New Delhi, IndiaPrinted and bound in Great Britain by Antony Rowe, Ltd, Chippenham, WiltshireThis book is printed on acid-free paper responsibly manufactured from sustainable forestryin which at least two trees are planted for each one used for paper production.

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Contents

Preface xvii

Copyright acknowledgements xix

1 Microbial diversity and freshwater ecosystems 1

1.1 General introduction 11.1.1 The aquatic existence 1

1.1.2 The global water supply – limnology and oceanography 1

1.1.3 Freshwater systems: some terms and definitions 3

1.1.4 The biology of freshwater microorganisms 4

A. BIOLOGICAL DIVERSITY IN THE FRESHWATER ENVIRONMENT 4

1.2 Biodiversity of microorganisms 41.2.1 Domains of life 4

1.2.2 Size range 6

1.2.3 Autotrophs and heterotrophs 7

1.2.4 Planktonic and benthic microorganisms 10

1.2.5 Metabolically active and inactive states 11

1.2.6 Evolutionary strategies: r-selected and K-selected organisms 12

1.3 Biodiversity in ecosystems, communities, and species populations 151.3.1 Main ecosystems 15

1.3.2 Diversity within subsidiary communities 16

1.3.3 Biodiversity within single-species populations 16

B. ECOSYSTEMS 17

1.4 The biofilm community: a small-scale freshwater ecosystem 181.4.1 Interactions between microorganisms 19

1.4.2 Biomass formation and transfer 20

1.4.3 Maintenance of the internal environment 20

1.4.4 Interactions with the external environment 21

1.5 The pelagic ecosystem: a large-scale unit within the lake environment 211.5.1 Interactions between organisms 21

1.5.2 Trophic connections and biomass transfer 23

1.5.3 Maintenance of the internal environment 28

1.5.4 Interactions with the external environment 28

1.6 Homeostasis and ecosystem stability 291.6.1 Stress factors 30

1.6.2 General theoretical predictions: the community response 30

1.6.3 Observed stress responses: from molecules to communities 31

1.6.4 Assessment of ecosystem stability 31

1.6.5 Ecosystem stability and community structure 32

1.6.6 Biological response signatures 34

C. FOOD WEBS IN LENTIC AND LOTIC SYSTEMS 34

1.7 Pelagic food webs 34CASE STUDY 1.1 MICROBIAL FOOD WEB ASSOCIATED WITH AN ALGAL BLOOM 34

CASE STUDY 1.2 GENERAL FOOD WEB IN THE WATER COLUMN OF LAKE BAIKAL (RUSSIA) 36

1.8 Communities and food webs of running waters 401.8.1 Allochthonous carbon: dissolved and particulate matter in river systems 40

1.8.2 Pelagic and benthic communities 42

1.8.3 The microbial food web 43

2 Freshwater environments: the influence of physico-chemicalconditions on microbial communities 47

A. INTRODUCTION 47

2.1 The aquatic medium: water, dissolved and particulate components 472.1.1 Particulate matter 47

2.1.2 Aquatic matrix 48

2.2 Freshwater environments 52

B. LAKES 53

2.3 Lake morphology and hydrology 532.3.1 Lake morphology 53

2.3.2 Lake hydrology and the surrounding terrestrial environment 57

2.4 Lakes as isolated environments 602.4.1 Isolated development 60

2.4.2 Lake Baikal: an ancient lake with a diverse and unique fauna and flora 60

2.5 Climatic influences on lakes 622.5.1 Temperate lakes – seasonal variations and lake stratification 63

2.5.2 Biological significance of stratification 65

2.5.3 Tropical lakes 66

2.5.4 Polar and sub-polar lakes 67

C. WETLANDS 68

2.6 General characteristics 682.6.1 Wetland diversity and global scale 68

2.6.2 Unifying features of wetlands 68

2.6.3 The role of wetlands in energy and material flow 69

2.7 Wetland habitats and communities 69

2.8 Case studies on wetland areas 70CASE STUDY 2.1 TŘEBOŇ BASIN BIOSPHERE RESERVE 71

D. STREAMS AND RIVERS 72

2.9 Comparison of lotic and lentic systems 72

2.10 River flow and the benthic community 732.10.1 Flow characteristics of lotic systems 73

2.10.2 Influence of water flow on benthic microorganisms 75

2.11 River hydrology 78

E. ESTUARIES 79

2.12 River inflow: water mixing, estuarine productivity, and eutrophication of coastal areas 80

vi CONTENTS

2.12.1 Mixing of fresh and saltwaters 80

2.12.2 High productivity of estuarine systems 81

2.12.3 Eutrophication of surrounding coastal areas 82

2.13 Habitats and communities 822.13.1 Pelagic zone 82

2.13.2 Sediments and mudflats 82

F. ADVERSE AND EXTREME CONDITIONS IN FRESHWATER ENVIRONMENTS 84

2.14 Adverse conditions as part of the environmental continuum 852.14.1 Variations in oxygen concentration 85

2.14.2 Nutrient availability 85

2.14.3 Solar radiation 86

2.15 Extreme environmental conditions 862.15.1 Temperature 86

2.15.2 pH 89

2.15.3 Conditions of low water availability: saline environments 91

2.15.4 Conditions of low water availability: ice and snow environments 92

2.15.5 Variations in hydrostatic pressure 93

2.15.6 Organic and inorganic pollution 93

2.16 A potentially extreme microenvironment: the air–water surface 952.16.1 Chemical composition of the surface microlayer 95

2.16.2 Physical processes and transformations in the surface biofilm 96

2.16.3 Microbial community at the air–water interface 98

2.17 Microbial communities of snow and ice: life in the frozen state 992.17.1 Snow and ice as an extreme environment 99

2.17.2 Requirement for water in the liquid state 99

2.17.3 Snow ecosystems 99

2.17.4 The physical properties of snow 100

2.17.5 Snow and ice microorganisms 102

3 Algae: the major microbial biomass in freshwater systems 105

A. TAXONOMIC AND MOLECULAR CHARACTERIZATION 107

3.1 Major taxonomic divisions of freshwater algae 1073.1.1 Microscopical appearance, motility and ecological features 107

3.1.2 Biochemical and cytological characteristics 110

3.1.3 General summary of the different groups 112

3.2 Algal species: taxonomy and intraspecific variation 1143.2.1 Taxonomy of algal species 114

3.2.2 Chemical diversity within species – enzyme analysis, molecular groups,

and elemental composition 115

3.3 Molecular analysis 1163.3.1 Molecular characterization and identification of algae 116

3.3.2 Investigation of gene function in freshwater algae 119

B. SIZE, SHAPE, AND SURFACE MUCILAGE 123

3.4 Phytoplankton size and shape 1233.4.1 Cell counts and biovolume 123

3.4.2 From picoplankton to macroplankton 123

3.4.3 Biological significance of size and shape 124

3.4.4 Variation in size and shape within phytoplankton populations 128

3.5 Mucilaginous and non-mucilaginous algae 1303.5.1 Chemical composition of mucilage 131

CONTENTS vii

3.5.2 Role of mucilage in phytoplankton activities 131

3.5.3 Environmental impact and biogeochemical cycles 133

C. ACTIVITIES WITHIN THE FRESHWATER ENVIRONMENT 133

3.6 Benthic algae: interactions with planktonic algae and ecological significance 1333.6.1 Planktonic and benthic algae 133

3.6.2 Lake periphyton 136

3.6.3 Benthic algae in flowing waters 138

3.6.4 Ecological role of benthic algae 138

3.7 Temporal activities of freshwater algae 1393.7.1 Short-term changes: molecular and cellular processes 140

3.7.2 Medium-term changes: algal succession 142

3.7.3 Long-term changes: variations over a number of years 146

3.8 Phytoplankton distribution within the water column 148CASE STUDY 3.1 VERTICAL ZONATION OF PHYTOPLANKTON IN A STRATIFIED LAKE 148

3.8.1 Active migration of algae 149

3.8.2 Passive movement of algae within the water column 156

3.9 Freshwater algae and nutrient status of the environment 1573.9.1 Phytoplankton species composition and lake nutrient status 157

3.9.2 Nutrient status of river environments – effect on benthic algal biofilms 160

D. STRATEGIES FOR SURVIVAL 161

3.10 Strategies for survival: the planktonic environment 1613.10.1 Meroplanktonic algae 162

3.10.2 Strategies for unstable and stable environments: r-selected and K-selected algae 164

3.11 Heterotrophic nutrition in freshwater algae 1653.11.1 Organotrophy 167

3.11.2 Phagotrophy 168

3.12 Survival in snow and ice: adaptations of cryophilic algae 1713.12.1 Major groups of cryophilic algae 171

3.12.2 Life cycles of snow algae 173

3.12.3 Physiological adaptations of snow algae 174

E. BIODIVERSITY IN THE ALGAL COMMUNITY 177

3.13 Variety of freshwater algae: indices of species diversity 1773.13.1 The paradox of phytoplankton diversity 177

3.13.2 Biodiversity indices 178

3.13.3 Numerical comparison of phytoplankton populations 179

3.13.4 Biodiversity and ecosystem function 180

4 Competition for light 181

4.1 The light environment 1824.1.1 Physical properties of light: terms and units of measurement 182

4.1.2 Light thresholds for biological activities 183

4.1.3 Light under water: refraction, absorption, and scattering 184

4.1.4 Light energy conversion: from lake surface to algal biomass 186

4.2 Photosynthetic processes in the freshwater environment 1884.2.1 Light and dark reactions 188

4.2.2 Photosynthetic microorganisms 189

4.2.3 Measurement of photosynthesis 189

4.2.4 Photosynthetic response to varying light intensity 190

4.3 Light as a growth resource 1924.3.1 Strategies for light uptake and utilization 192

4.3.2 Light–photosynthetic response in different algae 193

viii CONTENTS

4.3.3 Conservation of energy 194

4.3.4 Diversity in small molecular weight solutes and osmoregulation 195

4.4 Algal growth and productivity 1964.4.1 Primary production: concepts and terms 196

4.4.2 Primary production and algal biomass 197

4.4.3 Field measurements of primary productivity 197

4.5 Photosynthetic bacteria 1994.5.1 Major groups 200

4.5.2 Photosynthetic pigments 200

4.5.3 Bacterial primary productivity 201

4.6 Photoadaptation: responses of aquatic algae to limited supplies of light energy 2024.6.1 Different aspects of light limitation 203

4.6.2 Variable light intensity: light-responsive gene expression 204

4.6.3 Photosynthetic responses to low light intensity 205

4.6.4 Spectral composition of light: changes in pigment composition 209

4.7 Carbon uptake and excretion by algal cells 2104.7.1 Changes in environmental CO2 and pH 210

4.7.2 Excretion of dissolved organic carbon by phytoplankton cells 211

4.8 Competition for light and carbon dioxide between algae and higher plants 2154.8.1 The balance between algae and macrophytes in different aquatic environments 215

CASE STUDY 4.1 COMPETITION BETWEEN ALGAE AND MACROPHYTES IN SHALLOW

LAKES OF THE TŘEBOŇ WETLANDS 216

4.8.2 Physiological and environmental adaptations in the competition between

algae and macrophytes 218

4.9 Damaging effects of high levels of solar radiation: photoinhibition 2214.9.1 Specific mechanisms of photoinhibition 221

4.9.2 General effects of photoinhibition 224

4.9.3 Strategies for the avoidance of photoinhibition 225

4.9.4 Photoinhibition and cell size 227

4.9.5 Lack of photoinhibition in benthic communities 228

4.9.6 Photoinhibition in extreme high-light environments 228

4.10 Periodic effects of light on seasonal and diurnal activities of freshwater biota 2304.10.1 Seasonal periodicity 230

4.10.2 Diurnal changes 231

4.10.3 Circadian rhythms in blue-green algae 232

4.10.4 Circadian rhythms in dinoflagellates 234

5 Inorganic nutrients: uptake and cycling in freshwater systems 235

5.1 Chemical composition of natural waters 2355.1.1 Soluble inorganic matter in lakes and rivers 235

5.1.2 Aerial deposition of nutrients 237

5.1.3 Nutrient inflow from terrestrial sources 237

5.1.4 Chemical requirements and composition of freshwater biota 238

CASE STUDY 5.1 ELEMENTAL COMPOSITION OF CERATIUM HIRUNDINELLA 240

5.1.5 Nutrient availability and cycling in aquatic systems 243

5.2 Nutrient uptake and growth kinetics 2465.2.1 Empirical models for algal nutrient kinetics 246

5.2.2 Competition and growth in the aquatic environment 248

5.2.3 Nutrient availability and water movement 250

5.2.4 Acute nutrient deprivation as an environmental stress factor 251

A. NITROGEN 251

5.3 Biological availability of nitrogen in freshwater environments 2515.3.1 Soluble nitrogenous compounds 251

CONTENTS ix

5.4 The nitrogen cycle 2545.4.1 Nitrate entry and uptake (soluble inorganic to insoluble organic nitrogen) 254

5.4.2 Complex organic nitrogen (biomass) transformations

(successive states of insoluble organic nitrogen) 255

5.4.3 Remineralization (insoluble organic to soluble inorganic nitrogen) 255

5.4.4 Nitrification/denitrification (oxidation/reduction of soluble inorganic compounds) 255

5.5 Uptake of nitrate and ammonium ions by algae 2575.5.1 Biochemical processes 257

5.5.2 Species variations in nitrate uptake 258

5.5.3 Environmental regulation of nitrate assimilation 258

5.5.4 Nitrogen uptake, CO2 assimilation, and photosynthesis 259

5.6 Nitrogen fixation 2605.6.1 Ecological significance of nitrogen fixation 260

5.6.2 The nitrogenase enzyme and strategies of fixation 260

5.6.3 Heterocysts: nitrogen fixation by colonial blue-green algae 261

5.6.4 Diurnal control of nitrogen fixation: unicellular blue-green algae 262

5.6.5 Anaerobic environment: nitrogen-fixing bacteria 263

B. PHOSPHORUS 265

5.7 Occurrence and biological availability of phosphorus 2655.7.1 Phosphorus availability and limitation 265

5.7.2 The phosphorus cycle 266

5.8 Adaptations of freshwater microorganisms to low phosphorus concentrations 2695.8.1 Kinetics of phosphorus uptake 269

5.8.2 Luxury consumption of phosphate 269

5.8.3 Secretion of alkaline phosphatase 271

C. SILICON: A WIDELY-AVAILABLE ELEMENT OF LIMITED

METABOLIC IMPORTANCE 272

5.9 The silicon cycle 272

5.10 Silicon and diatoms 2745.10.1 Si uptake and phytoplankton succession 274

5.10.2 Si uptake and cell-wall formation 275

D. TRACE ELEMENTS 279

5.11 Biological role of trace elements 2805.11.1 Environmental uptake of trace elements 280

5.11.2 Stimulation of growth in aquatic environments 281

5.11.3 Importance of trace metals in the culture of aquatic algae 281

5.11.4 Biochemical roles of trace elements 282

5.12 Cycling of iron and other trace metals in the aquatic environment 2835.12.1 The iron cycle 283

5.12.2 The manganese cycle 286

6 Bacteria: the main heterotrophic microorganisms in freshwater systems 287

A. GENERAL DIVERSITY WITHIN THE ENVIRONMENT 287

6.1. General diversity, habitat preferences, and ecological significance of freshwater bacteria 2876.1.1 General diversity 287

6.1.2 Habitat preferences 288

6.1.3 Environmental significance of freshwater bacteria 290

6.2 Taxonomic, biochemical, and molecular characterization of freshwater bacteria 2916.2.1 Species identification 291

x CONTENTS

6.2.2 Genetic markers: detection of particular strains in the aquatic environment 292

6.2.3 Biochemical characterization of bacterial communities 293

CASE STUDY 6.1 CHANGES IN BACTERIAL COMMUNITY FUNCTION AND COMPOSITION AS

A RESPONSE TO VARIATIONS IN THE SUPPLY OF DISSOLVED ORGANIC MATERIAL (DOM) 293

B. GENETIC INTERACTIONS 294

6.3 Genetic diversity 2946.3.1 Chromosomal and accessory DNA 294

6.3.2 The ecological importance of gene transfer in freshwater systems 295

6.3.3 Total genetic diversity: the ‘community genome’ 296

6.4 Mechanisms for gene transfer in freshwater systems 2976.4.1 Transformation: uptake of exogenous DNA 297

6.4.2 Transduction: gene transfer between bacteria via bacteriophages 300

6.4.3 Conjugation: transfer of plasmid DNA by direct cell contact 300

6.5 Evidence for gene transfer in the aquatic environment 3006.5.1 Retrospective analysis 300

CASE STUDY 6.2 PLASMID-BORNE RESISTANCE IN AQUATIC BACTERIA 301

6.5.2 Laboratory (in vitro) studies on plasmid transfer 301

CASE STUDY 6.3 PLASMID TRANSFER IN PSEUDOMONAS AERUGINOSA 302

6.5.3 Field (in situ) studies on bacterial gene transfer 303

C. METABOLIC ACTIVITIES 304

6.6 Metabolic diversity of freshwater bacteria 3046.6.1 Key metabolic parameters 304

6.6.2 CO2 fixation 304

6.6.3 Breakdown of organic matter in aerobic and anaerobic environments 305

6.6.4 Bacterial adaptations to low-nutrient environments 310

6.7 Photosynthetic bacteria 3126.7.1 General characteristics 312

6.7.2 Motility 312

6.7.3 Ecology 314

6.8 Bacteria and inorganic cycles 3146.8.1 Bacterial metabolism and the sulphur cycle 315

D. BACTERIAL POPULATIONS AND PRODUCTIVITY 316

6.9 Bacterial populations 3166.9.1 Techniques for counting bacterial populations 316

6.9.2 Biological significance of total and viable counts 317

6.10 Bacterial productivity 3186.10.1 Measurement of productivity 318

6.10.2 Regulation of bacterial populations and biomass 319

6.10.3 Primary and secondary productivity: correlation between bacterial and algal populations 320

6.10.4 Primary and secondary productivity: the role of dissolved organic carbon 321

6.10.5 Bacterial productivity and aquatic food webs 323

E. BACTERIAL COMMUNITIES IN THE LOTIC ENVIRONMENT 324

6.11 Bacterial Biofilms 3246.11.1 The development of biofilms 324

6.11.2 Dynamic interactions in the establishment of biofilms: the role of bacterial co-aggregation 326

CASE STUDY 6.4 SPECIFIC RECOGNITION AND ADHESION AMONGST AQUATIC BIOFILM BACTERIA 326

F. BACTERIAL INTERACTIONS WITH PHYTOPLANKTON 328

6.12 Interactions between phytoplankton and planktonic bacteria 3286.12.1 Competition for inorganic nutrients 328

6.12.2 Antagonistic interactions between bacteria and algae 329

CONTENTS xi

6.13 Epiphytic associations of bacteria with phytoplankton 3326.13.1 Bacteria within the phycosphere 333

6.13.2 Observation and enumeration of epiphytic bacteria 334

6.13.3 Specific associations between bacteria and blue-green algae 336

7 Viruses: major parasites in the freshwater environment 339

7.1 Viruses as freshwater biota 3397.1.1 General role in the freshwater environment 339

7.1.2 Major groups and taxonomy of freshwater viruses 340

7.2 The virus life cycle: intracellular and free viral states 3407.2.1 Significance of the lysogenic state 341

7.3 Detection and quantitation of freshwater viruses 3427.3.1 Free particulate viruses 342

7.3.2 Infected host cells 345

7.4 The growth and control of viral populations 3457.4.1 Virus productivity 345

7.4.2 Regulation of viral abundance 346

7.5 Control of host populations by aquatic viruses: impact on the microbial food web 3497.5.1 Metabolic effects of viruses: reduction of algal primary productivity 349

7.5.2 Destruction of algal and bacterial populations 350

7.5.3 Viruses and the microbial loop 350

7.6 Cyanophages: viruses of blue-green algae 3517.6.1 Classification and taxonomic characteristics 351

7.6.2 Infection of host cells 352

7.7 Phycoviruses: parasites of eukaryote algae 3547.7.1 General characteristics 354

7.7.2 Host cell infection 356

CASE STUDY 7.1 THE INFECTIVE LIFE CYCLE OF CHLOROVIRUS 356

7.7.3 Ecological impact of phycoviruses 359

7.8 Virus infection of freshwater bacteria 3607.8.1 General role of bacteriophages in the biology of freshwater bacteria 360

7.8.2 Bacteriophages in pelagic and benthic systems 360

7.8.3 Occurrence of free bacteriophages in aquatic systems 361

7.8.4 Incidence of bacterial infection 361

7.8.5 Temperate/virulent phage equilibrium and bacterial survival 363

7.8.6 Bacteriophage control of planktonic bacterial populations 365

CASE STUDY 7.2 VIRAL LYSIS OF BACTERIA IN A EUTROPHIC LAKE 365

7.8.7 Transduction: bacteriophage-mediated gene transfer between freshwater bacteria 367

CASE STUDY 7.3 TRANSDUCTION OF PLASMID AND CHROMOSOMAL DNA IN

PSEUDOMONAS AERUGINOSA 368

8 Fungi and fungal-like organisms: aquatic biota with a mycelial growth form 371

A. ACTINOMYCETES, OOMYCETES, AND TRUE FUNGI 371

8.1 Fungi and fungal-like organisms: the mycelial growth habit 371

8.2 Actinomycetes 3728.2.1 Taxonomic characteristics 372

8.2.2 Habitat 373

8.2.3 Nutrition 374

8.2.4 Competition with other microorganisms 374

8.3 Oomycetes 3748.3.1 Oomycetes and true fungi 375

xii CONTENTS

8.3.2 Taxonomic diversity 376

8.4 True fungi 3778.4.1 Old and new terminology 377

8.4.2 Taxonomic diversity within the true fungi 378

B. FUNGI AS SAPROPHYTES AND PARASITES 381

8.5 Saprophytic activity of fungi 3818.5.1 Colonization, growth, and fungal succession 382

8.5.2 Breakdown of leaf litter 383

8.5.3 Saprophytic fungi – chytrids and deuteromycetes 386

8.6 Parasitic activities of aquatic fungi 3888.6.1 Parasitic and predatory deuteromycetes: fungi that attack small animals 388

8.6.2 Parasitic chytrids: highly specialized parasites of freshwater organisms 389

8.7 Fungal epidemics in the control of phytoplankton populations 3928.7.1 Ecological significance 392

CASE STUDY 8.1 CHYTRID INFECTION OF THE ASTERIONELLA DURING AN

AUTUMN DIATOM BLOOM 392

8.7.2 Net effect of infected and non-infected host cells 394

8.7.3 Factors affecting the development of fungal infection 395

9 Grazing activities in the freshwater environment: the role ofprotozoa and invertebrates 401

A. PROTOZOA 401

9.1 Introduction 4019.1.1 Relative importance of protozoans, rotifers, and crustaceans in pelagic communities 401

9.1.2 Ecological role of protozoa 402

9.2 Protozoa, algae, and indeterminate groups 402

9.3 Taxonomic diversity of protozoa in the freshwater environment 4039.3.1 Ciliates 403

9.3.2 Flagellate protozoa 407

9.3.3 Amoeboid protozoa 409

9.4 Ecological impact of protozoa: the pelagic environment 4129.4.1 Positioning within the water column 412

9.4.2 Trophic interactions in the water column 413

9.5 Heterotrophic nanoflagellates: an integral component of planktonic communities 4139.5.1 Enumeration of nanoflagellate populations in aquatic samples 414

9.5.2 Taxonomic composition of HNF communities 415

9.5.3 Abundance and control of flagellate populations 415

9.5.4 Nanoflagellate grazing rates and control of bacterial populations 416

9.5.5 Co-distribution of bacteria and protozoa within the water column 418

9.6 Ecological impact of protozoa: the benthic environment 4199.6.1 Benthic microenvironments 419

9.6.2 Seasonal changes 421

9.6.3 Organic pollution 421

9.6.4 Sewage-treatment plants: activated sludge 422

B. GRAZING OF MICROBIAL POPULATIONS BY ZOOPLANKTON 423

9.7 General features of zooplankton: rotifers, cladocerans and copepods 4239.7.1 Morphology and size 423

9.7.2 Reproduction and generation times 426

9.7.3 Predation of zooplankton 426

9.8 Grazing activity and prey selection 4279.8.1 Seasonal succession in zooplankton feeding 427

CONTENTS xiii

9.8.2 Method of feeding 429

9.8.3 Selection of food by zooplankton 429

9.9 Grazing rates of zooplankton 4329.9.1 Measurement 432

9.9.2 Factors affecting grazing rates 433

9.9.3 Diurnal variations in grazing activity 434

9.10 Effects of algal toxins on zooplankton 435

9.11 Biomass relationships between phytoplankton and zooplankton populations 4379.11.1 Control of zooplankton populations 437

9.11.2 Biomass transfer 437

C. GRAZING OF BENTHIC MICROORGANISMS 438

9.12 Comparison of pelagic and benthic systems 438

9.13 Role of invertebrates in consuming river microorganisms 4409.13.1 Grazing of periphyton biomass 440

9.13.2 Effects of grazing on periphyton community structure 441

10 Eutrophication: the microbial response to high nutrient levels 443

A. ORIGINS OF EUTROPHICATION 444

10.1 Nutrient status of freshwater environments: from oligotrophic to eutrophic systems 44410.1.1 Eutrophic and oligotrophic lakes: definition of terms 444

10.1.2 Determinants of trophic status: location, morphology and hydrology 445

10.1.3 Artificial eutrophication: the impact of human activities 446

10.1.4 Eutrophication of rivers and streams 446

B. ECOLOGICAL EFFECTS OF EUTROPHICATION IN STANDING WATERS 448

10.2 General biological changes 44810.2.1 The progression from oligotrophic to eutrophic waters 448

10.2.2 Effects of eutrophication on the water column of stratified lakes 452

10.2.3 Major changes in ecological balance: the breakdown of homeostasis 452

10.3 Biological assessment of water quality 45310.3.1 Algal indicator groups 453

CASE STUDY 10.1 USING THE A/C (ARAPHID PENNATE/CENTRIC) DIATOM RATIO TO ASSESS

EUTROPHICATION IN LAKE TAHOE (USA) 454

10.3.2 Indices of species diversity 455

10.4 Problems with intentional eutrophication: destabilization of fishpond ecosystems 45510.4.1 Promotion of high productivity in fishponds 455

10.4.2 Destabilization and restoration of the ecosystem 456

C. THE GROWTH AND IMPACT OF ALGAL BLOOMS 457

10.5 Algal blooms and eutrophication 457

10.6 Formation of colonial blue-green algal blooms 45910.6.1 General requirements for bloom formation 459

10.6.2 Competition with other algae 459

CASE STUDY 10.2 USE OF ENCLOSURE EXPERIMENTS TO STUDY FACTORS AFFECTING

BLUE-GREEN DOMINANCE 461

10.7 Environmental effects of blue-green blooms 46110.7.1 General environmental changes 461

10.7.2 Specific effects on water quality 462

10.7.3 Production of toxins 462

xiv CONTENTS

D. CONTROL OF BLUE-GREEN ALGAE 464

10.8 Strategies for the control of blue-green algae 46410.8.1 Nutrient limitation (bottom-up control) 465

CASE STUDY 10.3 RESTORATION OF WATER QUALITY IN LAKE WASHINGTON, NORTH WEST USA 466

10.8.2 Direct eradication 466

10.8.3 Top-down control of blue-green algae: the use of biomanipulation 467

CASE STUDY 10.4 TOP-DOWN AND BOTTOM-UP CONTROL OF ALGAL POPULATIONS IN

THE BROADS WETLAND AREA (UK) 467

10.9 Biological control of blue-green algae 47110.9.1 Biological control agents 472

10.9.2 Protocol for the development of biological control agents 474

CASE STUDY 10.5 POTENTIAL PROTOZOON CONTROL AGENTS 475

10.9.3 Application of plant litter to control blue-green algae 475

10.10 Strategies for the control of blue-green algae in different water bodies 47710.10.1 Integrated management policy 477

CASE STUDY 10.6 ENVIRONMENTAL MONITORING AT HOLLINGWORTH LAKE,

GREATER MANCHESTER (UK) 479

10.10.2 Specific remedial measures in different freshwater systems 481

Glossary 483

References 495

Index 517

CONTENTS xv

Preface

Although freshwater microorganisms are not as

readily apparent as macroscopic fauna (inverte-

brates, fish) and flora (higher plants, large algae),

they are universally present within aquatic habitats

and their ecological impact is of fundamental

importance. This book examines the diversity and

dynamic activities of freshwater microbes including

micro-algae, bacteria, viruses, actinomycetes, fungi,

and protozoa.

On an environmental scale, the activities of

these organisms range from the microlevel (e.g.,

localized adsorption of nutrients, surface secretion

of exoenzymes) through community dynamics

(interactions within planktonic and benthic popula-

tions) to large-scale environmental effects. These

include major changes in inorganic nutrient con-

centrations, formation of anaerobic hypolimnia,

and stabilization of mudflats. Thus, although fresh-

water microorganisms are strongly influenced

by their physical and chemical environment,

they can in turn exert their own effects on their

surroundings.

In a temporal dimension, the biology of these

biota embraces activities which range from femto-

seconds (e.g., light receptor parameters) to sec-

onds (light responsive gene activity), diurnal

oscillations, seasonal changes (phytoplankton

succession), and transitions over decades and cen-

turies (e.g., long-term response to acidification and

nutrient changes).

The study of freshwater microorganisms involves

all major disciplines within biology, and I have

attempted to bring together aspects of taxonomy,

molecular biology, biochemistry, structural biology,

and classical ecology within this volume. A com-

plete study of freshwater microorganisms must also

clearly relate to other freshwater biota, and I have

emphasized links in relation to general food webs –

plus specific interactions such as zooplankton graz-

ing, algal/higher plant competition, and the role of

fish and macrophytes in the biomanipulation of

algal populations.

In addition to being an area of intrinsic biol-

ogical interest, freshwater microbiology has

increasing practical relevance in relation to human

activities, population increase, and our use of

environmental resources. In this respect microor-

ganisms play a key role in the deterioration of

freshwater environments that results from eutro-

phication, and management of aquatic systems

requires a good understanding of the principles of

freshwater microbiology. The biology of these

biota is also important in relation to other applied

aspects such as the breakdown of organic pollutants,

the spread of human pathogens, and the environ-

mental impact of genetically-engineered micro-

organisms.

Inevitably, a book of this type relies heavily on

previously published work, and I would like to

thank holders of copyright (see separate listing)

for granting permission to publish original diagrams

and figures. I am also grateful to colleagues (parti-

cularly Professor A.P.J. Trinci and Dr R.D. Butler)

for commenting on sections of the manuscript, and

for the helpful, detailed comments of anonymous

reviewers. Finally, my thanks are due to the

numerous research colleagues who I have worked

with over the years, including Jo Abraham,

Martin Andrews, Ed Bellinger, Karen Booth, Ron

Butler, Sue Clay, Andrew Dean, Ebtesam El-

Bestawy, Robert Glenn, Harry Epton, Larry Kearns,

Vlad Krivtsov, Eugenia Levado, Christina Tien, and

Keith White.

David Sigee

Manchester, 2004.

xv PREFACEiii

Copyright acknowledgements

I am very grateful to the following individuals

for allowing me to use previously unpublished

material – Drs Nina Bondarenko, Andrew Dean,

Harry Epton, Robert Glenn, Eugenia Levado, Ms

Elishka Rigney, Mr Richard Sigee, Mrs Rosemary

Sigee, Dr Christina Tien, Professor James Van Etten

and Dr Keith White.

I also thank the following copyright holders for

giving me permission to use previously published

material – The American Society for Micro-

biology, Biopress Ltd., Blackwell Publishing

Ltd., Cambridge University Press, Elsevier

Science, European Journal of Phycology, Inter-

research Science, John Wiley & Sons, Parthenon

Publishing, Kluwer Academic Publishers, The

Linnean Society of London, NRC Research

Press, Scanning Microscopy Inc. and Springer-

Verlag.

1Microbial diversity and freshwaterecosystems

1.1 General introduction

This book explores the diversity, interactions and

activities of microbes (microorganisms) within

freshwater environments. These form an important

part of the biosphere, which also includes oceans,

terrestrial environments and the earth’s atmosphere.

1.1.1 The aquatic existence

It is now generally accepted that life originated

between 3.5 and 4 billion years ago in the aquatic

environment, initially as self-replicating molecules

(Alberts et al., 1962). The subsequent evolution of

prokaryotes, followed by eukaryotes, led to the

existence of microorganisms which are highly

adapted to aquatic systems. The biological import-

ance of the physical properties of water is discussed

in Section 2.1.2.

Life in the aquatic environment (freshwater and

marine) has numerous potential advantages over

terrestrial existence. These include physical support

(buoyancy), accessibility of three-dimensional

space, passive movement by water currents, disper-

sal of motile gametes in a liquid medium, minimal

loss of water (freshwater systems), lower extremes

of temperature and solar radiation, and ready avail-

ability of soluble organic and inorganic nutrients.

Potential disadvantages of aquatic environments

include osmotic differences between the organism

and the surrounding aquatic medium (leading to

endosmosis or exosmosis) and a high degree of

physical disturbance in many aquatic systems. In

undisturbed aquatic systems such as lakes, photosyn-

thetic organisms have to maintain their position at

the top of the water column for light availability. In

many water bodies (e.g., lake water column), physi-

cal and chemical parameters show a continuum –

with few distinct microhabitats. In these situations,

species compete in relation to different growth and

reproductive strategies rather than specific adapta-

tions to localized environmental conditions.

1.1.2 The global water supply – limnologyand oceanography

Water covers seven tenths of the Earth’s surface and

occupies an estimated total volume of 1.38�109 km3 (Table 1.1). Most of this water occurs

between continents, where it is present as oceans

(96.1 per cent of global water) plus a major part of

the atmospheric water. The remaining 3.9 per cent

of water (Table 1.1 shaded boxes), present within

continental boundaries (including polar ice-caps),

occurs mainly as polar ice and ground water. The

latter is present as freely exchangeable (i.e., not

Freshwater Microbiology: Biodiversity and Dynamic Interactions of Microorganisms in the Aquatic Environment David C. Sigee# 2005 John Wiley & Sons, Ltd ISBNs: 0-471-48529-2 (pbk) 0-471-48528-4 (hbk)

chemically-bound) water in subterranean regions

such as aquifers at varying depths within the Earth’s

crust. Non-polar surface freshwaters, including soil

water, lakes, rivers and streams occupy approxi-

mately 0.0013 per cent of the global water, or

0.37 per cent of water occurring within continental

boundaries. The volume of saline lakewater approxi-

mately equals that of freshwater lakes. The largest

uncertainty is the estimation of ground water

volume. Annual inputs by precipitation are esti-

mated at 5:2� 108 km3, with a resulting flow fromcontinental (freshwater) systems to oceans of about

38 600 km3.

The distinction between oceans and continental

water bodies leads to the two main disciplines of

aquatic biology – oceanography and limnology.

� Oceanography is the study of aquatic systemsbetween continents. It mainly involves saltwater,

with major impact on global parameters such as

temperature change, the carbon cycle and water

circulation.

� Limnology is the study of aquatic systems con-tained within continental boundaries, including

freshwater and saltwater sites.

The study of freshwater biology is thus part of

limnology. Although freshwater systems do not

have the global impact of oceans, they are of

major importance to biology. They are important

ecological features within continental boundaries,

have distinctive groups of organisms, and show

close links with terrestrial ecosystems.

The two main sites (over 99 per cent by volume)

of continental water – the polar ice-caps and

exchangeable ground water – are extreme environ-

ments which have received relatively little micro-

biological attention until recent years. Although

most limnological studies have been carried out

on lakes, rivers, and wetlands the importance of

other water bodies – particularly the vast frozen

environments of the polar regions (see below) –

should not be overlooked. Microbiological aspects

of snow and ice environments are discussed in

Sections 2.17 and 3.12, and the metabolic activities

of bacteria in ground water in Section 2.14.2.

Although there are many differences between

limnological (inland) and oceanic (intercontinental)

systems, there are also some close similarities. The

biology of planktonic organisms in lakes, for exam-

ple, shows many similarities to that of oceans – and

much of our understanding of freshwater biota (e.g.,

Table 1.1 Global distribution of water (adapted from Horne and Goldman, 1994)

Site Volume (km3) % of water within continents

Oceans 1 322 000 000

Polar ice caps and glaciers 29 200 000 54.57

Exchangeable ground water 24 000 000 44.85

Freshwater lakes 125 000 0.23

Saline lakes and inland seas 104 000 0.19

Soil and subsoil water 65 000 0.12

Atmospheric vapour 14 000 0.026

Rivers and streams 1 200 0.022

Annual inputs

Surface runoff to ocean 37 000

Ground water to sea 1 600

Precipitation

Rainfall on ocean 412 000 000

Rainfall on land and lakes 108 000 000

2 MICROBIAL DIVERSITYAND FRESHWATER ECOSYSTEMS

the biology of aquatic viruses (Chapter 7) comes

from studies on marine systems.

1.1.3 Freshwater systems: some termsand definitions

Freshwater microorganisms

Microorganisms may be defined as those organisms

that are not readily visible to the naked eye, requir-

ing a microscope for detailed observation. These

biota have a size range (maximum linear dimension)

up to 200 mm, and vary from viruses, throughbacteria and archea, to micro-algae, fungi and pro-

tozoa. Higher plants, macro-algae, invertebrates and

vertebrates do not fall in this category and are not

considered in detail, except where they relate to

microbial activities. These include photosynthetic

competition between higher plants and micro-algae

(Section 4.8) and the role of zooplankton as grazers

of algae and bacteria (Section 9.8).

Freshwater environments: water in theliquid and frozen state

Freshwater environments are considered to include

all those sites where freshwater occurs as the main

external medium, either in the liquid or frozen state.

Although frozen aquatic environments have long

been thought of as microbiological deserts, recent

studies have shown this not to be the case. The

Antarctic sub-continent, for example, is now known

to be rich in microorganisms (Vincent, 1988), with

protozoa, fungi, bacteria, and microalgae often

locally abundant and interacting to form highly-

structured communities. New microorganisms,

including freeze-tolerant phototrophs and hetero-

trophs, have been discovered and include a number

of endemic organisms. New biotic environments

have also been discovered within this apparently

hostile environment – which includes extensive

snow-fields, tidal lakes, ice-shelf pools, rock crystal

pools, hypersaline soils, fellfield microhabitats, and

glacial melt-water streams. Many of these polar en-

vironments are saline, and the aquatic microbiology

of these regions is considered here mainly in terms

of freshwater snow-fields in relation to extreme

aquatic environments (Section 2.17) and the cryo-

philic adaptations of micro-algae (Section 3.12).

This book deals with aquatic systems where water

is present in the liquid state for at least part of the

year. In most situations (temperate lakes, rivers, and

wetlands) water is frozen for only a limited time,

but in polar regions the reverse is true. Some regions

of the ice-caps are permanently frozen, but other

areas have occasional or periodic melting. In many

snow-fields, the short-term presence of water in the

liquid state during the annual melt results in a burst

of metabolic activity and is important for the lim-

ited growth and dispersal of snow microorganisms

and for the completion of microbial life cycles

(Section 3.12).

Freshwater and saline environments

Within inland waters, aquatic sites show a gradation

from water with a low ionic content (freshwater) to

environments with a high ionic content (saline) –

typically dominated by sodium and chlorine ions.

Saline waters include estuaries (Sections 2.12 and

2.13), saline lakes (Section 2.15.3) and extensive

regions of the polar ice-caps (Vincent, 1988). The

high ionic concentrations of these sites can also be

recorded in terms of high electrical conductivity

(specific conductance) and high osmotic potential.

The physiological demands of saline and fresh-

water conditions are so different that aquatic orga-

nisms are normally adapted to one set of conditions

but not the other, so they occur in either saline or

freshwater conditions. The importance of salinity in

determining the species composition of the aquatic

microbial community was demonstrated in a recent

survey of Australian saline lakes (Gell and Gasse,

1990), where distinct assemblages of diatoms were

present in low salinity (oligosaline) and high sali-

nity (hypersaline) waters. Some diatom species,

however, were present over the whole range of

saline conditions, indicating the ability of some

microorganisms to be completely independent of

salt concentration and ionic ratios. Long-term adapt-

ability to different saline conditions is also indicated

GENERAL INTRODUCTION 3

by the ability of some organisms to migrate from

saltwater to freshwater sites, and establish them-

selves in their new conditions. This appears to be

the case for various littoral red algae of freshwater

lakes (Section 3.1.3), which were originally derived

from marine environments (Lin and Blum, 1977).

Differences between freshwater/saltwater environ-

ments and their microbial communities, are parti-

cularly significant in global terms (Chapter 2),

where the dominance of saline conditions is clear

in terms of area coverage, total biomass, and overall

contribution to carbon cycling.

Lentic and lotic freshwater systems

Freshwater environments show wide variations in

terms of their physical and chemical characteristics,

and the influence these parameters have on the micro-

bial communities they contain. These aspects are

considered in Chapter 2, but one important distinc-

tion needs to be made at this stage – between lentic

and lotic systems. Freshwater environments can be

grouped into standing waters (lentic systems –

including ponds, lakes, marshes and other enclosed

water bodies) and flowing waters (lotic systems –

rivers, estuaries and canals). The distinction

between lentic and lotic systems is not absolute,

and almost all water bodies have some element of

through-flow. Key differences between lentic and

lotic systems in terms of carbon availability and

food webs are considered in Section 1.8.

1.1.4 The biology of freshwater microorganisms

In this book the biology of freshwater microorga-

nisms is considered from five major aspects:

� Microbial diversity and interactions within eco-systems (Chapter 1); these interactions include

temporal changes in succession and feeding

(trophic) interactions.

� Variations between different environmental sys-tems, including lakes, rivers, and wetlands (Chap-

ter 2). Each system has its own mixture of

microbial communities, and its own set of physi-

cal and biological characteristics.

� Characteristics and activities of the five majorgroups of microbial organisms – algae (Chapter 3),

bacteria (Chapter 6), viruses (Chapter 7), fungi

(Chapter 8), and protozoa (Chapter 9).

� The requirement of freshwater microorganismsfor two major environmental resources – light

(Chapter 4) and inorganic nutrients (Chapter 5).

These are considered immediately after the sec-

tion on algae, since these organisms are the major

consumers of both commodities.

� Themicrobial response to eutrophication. Environ-mental problems associated with nutrient increase

are of increasing importance and reflect both a

microbial response to environmental change and

a microbial effect on environmental conditions.

A. BIOLOGICAL DIVERSITY IN THE FRESHWATER ENVIRONMENT

1.2 Biodiversity of microorganisms

1.2.1 Domains of life

With the exception of viruses (which constitute a

distinct group of non-freeliving organisms) the most

fundamental element of taxonomic diversity within

the freshwater environment lies in the separation of

biota into three major domains – the Bacteria,

Archaea, and Eukarya. Organisms within these

domains can be distinguished in terms of a number

of key fine-structural, biochemical, and physiologi-

cal characteristics (Table 1.2).

Cell organization is a key feature, with the

absence of a nuclear membrane defining the

Bacteria (Figure 3.2) and Archaea as prokaryotes.

These prokaryote domains also lack complex

systems of membrane-enclosed organelles, have

4 MICROBIAL DIVERSITYAND FRESHWATER ECOSYSTEMS

70s ribosomes and have genetic systems which

include plasmids and function by operons.

Prokaryote features also include a unicellular or

colonial (but not multicellular) organization, and a

small cell size (

1.2.2 Size range

Size is an important parameter for all freshwater

microorganisms, affecting their location within the

freshwater environment, their biological activities,

and their removal by predators. The importance

of size and shape in planktonic algae is considered

in some detail in Section 3.4, and includes aspects

such as predation by other organisms, sinking rates,

and potential growth rates.

In the case of free-floating (planktonic) orga-

nisms, the maximum linear dimension ranges from

200 mm, with separation of the biotainto five major size categories (Table 1.3), from

femtoplankton to macroplankton.

Femtoplankton (

Within this assemblage, unicellular algae, along

with picocyanobacteria, are particularly important

in the short-term development of algal blooms

which may occur during brief growing seasons or

at various points in a more prolonged seasonal

sequence.

Microplankton (20–200 �m)

Larger microplankton are retained by traditional

�70 mm mesh size phytoplankton nets, and arehighly prone to sinking in the absence of buoyancy

aids. These organisms are consumed by larger

crustacea, and are also the principal food of pelagic

and benthic omnivorous fish. Growth rates are mode-

rate to low.

Macroplankton (>200 �m)

These have similar biological features to the larger

microplankton, and are characterized by the colonial

blue-green algae and by the multicellular zooplank-

ton (rotifers and crustacea). The biology of meso-

trophic and eutrophic lakes in temperate climates

are typically dominated by these size categories

over the summer growth period, with separate

population peaks of colonial algae (diatoms, blue-

greens) and zooplankton (crustacea) at different

times of year. Although macroplanktonic organisms

are characteristically slow-growing, they typically

make the greatest contribution to biomass under

conditions of adequate nutrient supply. Differences

between picoplankton and macroplankton in terms

of growth rate, short-term colonization and long-

term domination of freshwater environments reflect

fundamental differences in evolutionary selection

strategy and the way these biota are adapted to

different environmental conditions. The distinction

between small size (r-strategist) and large size (K-

strategist) organisms is considered more fully below.

1.2.3 Autotrophs and heterotrophs

Freshwater microorganisms may be divided accord-

ing to their feeding activity (trophic status) into two

major groups:

� Autotrophs – synthesize their complex carboncompounds from external CO2. Most also obtain

their supplies of nutrient (e.g., nitrogen and

phosphorus) from simple inorganic compounds.

These phototrophic microorganisms include

microalgae and photosynthetic bacteria, and are

the main creators of biomass (primary producers)

in many freshwater ecosystems. This is not

always the case, however, since photosynthetic

microorganisms are outcompeted by larger algae

and macrophytes in some aquatic systems, parti-

cularly wetland communities (Section 4.8).

� Heterotrophs – use complex organic compoundsas a source of carbon. By far the majority of

freshwater microorganisms (most bacteria, proto-

zoa, fungi) are heterotrophic. Even within the

algae, various groups have evolved the capacity

for heterotrophic nutrition (Section 3.11) and

many organisms currently included in the proto-

zoon assemblage have probably evolved from

photosynthetic ancestors.

Heterotrophic nutrition involves a wide diversity

of activities (Table 1.4) with microorganisms ob-

taining their organic material in three main ways –

saprotrophy, predation, and in association with

living organisms. Saprotrophic organisms obtain

their nutrients from non-living material. This may

be assimilated in three main ways: direct uptake

as soluble compounds (chiefly bacteria), indirect

uptake by secretion of external enzymes (exo-

enzymes) followed by absorption of the hydrolytic

products (bacteria and fungi), and ingestion of

particulate matter by phagocytosis (protozoa). Pre-

dation is carried out by protozoa, and involves

capture, ingestion, and internal digestion of other

living organisms such as bacteria and algae. Proto-

zoa can capture their prey either by active motility

or, as sedentary organisms, by the use of filter feed-

ing processes. The third major aspect of hetero-

trophy involves associations with living organisms

and includes parasitism and symbiosis. Parasitism

almost invariably involves a strict dependence of the

parasite on the host organism as part of the parasitic

life cycle, though in some cases the benefits to

the parasite are not entirely clear. The common

BIODIVERSITY OF MICROORGANISMS 7

Table 1.4 Heterotrophic nutrition in freshwater microorganisms

Mode of nutrition Group of organisms

Characteristics and

ecological importance Book reference

Saprophytic

Uptake of

nonliving biomass

(a) Osmotrophy:

direct uptake of

soluble organic

compounds

Planktonic heterotrophic

bacteria

Assimilation of dissolved organic

carbon (DOC) secreted by

phytoplankton basis of microbial

loop in planktonic systems

Section 4.7.2

Section 6.10

Figures 6.13 and 6.16

Osmotrophic algae

and protozoa

Uptake of soluble organic compounds

in high nutrient environments

Algae: Section 3.11

Protozoa: Section 9.6.3

and 9.6.4

(b) External

digestion of

insoluble biomass

Bacteria, actinomycetes,

and fungi

Secretion of exo-enzymes, uptake of

digestion products; typical of

benthic environments of lakes

and streams where organic detritus

accumulates

Bacteria Divide and penetrate biomass

as invasive populations

Section 6.6.3

Actinomycetes and fungi Penetrate biomass via extension

of mycelial system

Actinomycetes:

Section 8.2.3

Fungi: Section 8.5

(c) Detritus

feeders; ingestion

of dead particulate

material

Protozoa Engulph dead particulate biomass by

phagocytosis; typical of benthic

environments

Section 9.6

Predation

(carnivory);

ingestion and

killing of live

organisms

Protozoa Catch and ingest living microorganisms

by phagocytosis; important in the

control of bacterioplankton

populations by heterotrophic

nanoflagellates (HNFs) and in

benthic environments

HNFs: Sections 6.10.2;

and 9.5

Benthic: Section 9.6

Heterotrophic algae Catch and ingest bacteria and other

algae; strategic response to

limitations in photosynthesis

Section 3.11

Association with

living organisms

(a) Parasitism

(unilateral nutritive

benefit)

Viruses Major parasites of all freshwater biota;

important in the control of

phytoplankton and bacterioplankton

populations

Chapter 7: Phycoviruses

Cyanophages

Bacteriophages

Fungi Important parasites of a wide range

of organisms, including:

(a) Phytoplankton; chytrid fungi

have major importance in limiting

planktonic algal populations

Sections 8.6 and 8.7

(b) Invertebrates Section 8.6.2

Bacteria Carried out by specialized bacteria

such as Bdellovibrio

Section 6.12.2

8 MICROBIAL DIVERSITYAND FRESHWATER ECOSYSTEMS