Microbial Ecology of the Oceans

About the Editors Josep M. Gasol is a Research Professor at the Institut de Ciències del Mar, CSIC, in Barcelona, Spain. David L. Kirchman is a Professor in the School of Marine Science and Policy at the University of Delaware, USA.

PREFACE xiii

CONTRIBUTORS xv

1 INTRODUCTION: THE EVOLUTION OF MICROBIAL ECOLOGY OF THE OCEAN 1
Josep M. Gasol and David L. Kirchman

1.1 Introduction 1

1.2 A Brief History of Marine Microbial Ecology 3

1.2.1 Biological Oceanography and “Black Box” Microbial Ecology 6

1.2.2 Opening the Black Box for Variability in Activity and Growth Rates 9

1.2.3 The Molecular Description of Microbial Diversity: rRNA]Based Approaches 11

1.2.4 The Molecular Description of Microbial Diversity: Whole Organisms and Genomes 14

1.2.5 N2 Fixation Studies as a Model for Marine Microbial Ecology 18

1.3 An Assessment of Current Marine Microbial Ecology 20

1.4 The Future of Marine Microbial Ecology 24

1.4.1 Toward Single]Cell Microbial Oceanography 24

1.4.2 Toward Understanding Cell]Cell Interactions 26

1.4.3 Toward Comprehensive Exploration of All Marine Habitats 27

1.4.4 Toward Changing Our View of the Fluxes of C and the Role of the Various Microbes 28

1.4.5 Toward Describing the Unknown Component of Microbial Diversity in the Oceans 29

1.5 Summary 30

1.6 References 31

2 MARINE MICROBIAL DIVERSITY AS SEEN BY HIGH]THROUGHPUT SEQUENCING 47
Carlos Pedrós]Alió, Silvia G. Acinas, Ramiro Logares and Ramon Massana

2.1 Diversity 47

2.1.1 Mechanisms Promoting Appearance of Novel Taxa 48

2.1.2 Mechanisms Promoting Coexistence 50

2.2 The Methods 53

2.2.1 First Applications of Sequencing Technology to the Marine Environment 55

2.2.2 HTS for Diversity Studies 56

2.2.3 rDNA Tags Extracted from Metagenomes 58

2.2.4 Single]Cell Genomics 58

2.2.5 Challenges of Processing Sequence Data 59

2.3 The Use of Sequences as Proxies for Taxa 59

2.3.1 Building Taxonomic Units from Sequences 59

2.3.2 Tools for Data Analysis 64

2.3.3 Comparison of Tag Sequences and the Biological Species Concept 65

2.3.4 Contribution of HTS and Genomes to a Novel Definition of Microbial Species 66

2.4 Diversity after HTS 68

2.4.1 One Sample (Alpha Diversity) 68

2.4.2 Comparison of Several Samples (Beta and Gamma Diversity) 71

2.4.3 The Unknown Marine Microbial Diversity 84

2.5 Conclusion 86

2.6 Summary 87

2.7 Acknowledgments 87

2.8 References 87

3 ECOLOGICAL SIGNIFICANCE OF MICROBIAL TROPHIC MIXING IN THE OLIGOTROPHIC OCEAN: THE ATLANTIC OCEAN CASE STUDIES 99
Mikhail V. Zubkov and Manuela Hartmann

3.1 Oligotrophic Oceanic Gyres: The Most Extensive, Microbe]Dominated Biome on Earth 99

3.2 Microbial Composition of the Subtropical Gyres 101

3.3 Prokaryotic Photoheterotrophy in Gyres: The Ability to Use Light Energy and to Take up Organic Molecules Simultaneously 103

3.4 Eukaryotic Mixotrophy in Gyres: The Ability to Use Light Energy and Simultaneously Prey on Bacterioplankton 106

3.5 How Do Photoheterotrophy and Mixotrophy Affect the Coexistence of Bacteria and Eukaryotes in Gyres? 109

3.6 Knowledge Gaps 112

3.7 Summary 114

3.8 Acknowledgments 114

3.9 References 114

4 METATRANSCRIPTOMICS AND METAPROTEOMICS: ELUCIDATING MARINE MICROBIAL ECOSYSTEM FUNCTIONS 123
Robert M. Morris

4.1 Introduction to Marine “Omics” and Big Data 123

4.2 Overview of the Metatranscriptomics Approach 126

4.3 Overview of the Metaproteomics Approach 129

4.4 Key Considerations in Detecting Community Ecosystem Functions 131

4.5 Importance of Cultivation]Based Studies, Replication, and Quantification 134

4.6 Marine Microbial Community Transcriptomics and Proteomics 134

4.6.1 Primary and Secondary Transporters Signal Shifts in Marine Microbial Communities 136

4.6.2 Significant Photoheterotrophic Contribution to Marine Microbial Communities 137

4.6.3 Microbial Metabolism of Single]Carbon Compounds 139

4.6.4 Uncovering Suspected and Surprising Temporal Rhythms 139

4.7 Summary 141

4.8 Acknowledgments 141

4.9 References 142

5 ADVANCES IN MICROBIAL ECOLOGY FROM MODEL MARINE BACTERIA: BEYOND THE ESCHERICHIA COLI PARADIGM 149
Sandra Martínez]García and Jarone Pinhassi

5.1 Introduction 149

5.2 Cultivation Approaches 153

5.3 Lessons Learned from Ecophysiological Response Experiments with Cultivated Bacteria 155

5.3.1 Nutrient Cycling (C, N, P, S, and Micronutrients) 155

5.3.2 Photoheterotrophy in Marine Bacteria 163

5.3.3 Microbial Interactions 166

5.3.4 Phage]Host Model Systems in Cyanobacteria and Heterotrophic Bacteria 168

5.3.5 Deep]Sea Bacteria 171

5.4 Concluding Remarks 172

5.5 Summary 174

5.6 Acknowledgments 175

5.7 References 175

6 AN INSEPARABLE LIAISON: MARINE MICROBES AND NONLIVING ORGANIC MATTER 189
Thorsten Dittmar and Carol Arnosti

6.1 An Inseparable Liaison: Marine Microbes and Nonliving Organic Matter 189

6.2 Marine Carbon Reservoirs 192

6.3 Biogeochemical Cycles and Their Microbial Engines 195

6.3.1 Surface Ocean Cycling 195

6.3.2 Particle Formation and Flux 197

6.3.3 Cycling in Sediments 198

6.4 Driving Forces for Turnover Kinetics 200

6.5 Spatial and Temporal Changes in Organic Matter and Microbial Communities 209

6.5.1 Terrestrial Inputs and Transformations 209

6.5.2 Variability in Primary Productivity and Microbial Communities 210

6.5.3 Broad]Scale Patterns of Microbial Community Composition and Activities 211

6.6 The Challenge for Future Research: Understanding the Functional Network of Marine Microbes and Organic Molecules 214

6.7 Summary 217

6.8 Acknowledgments 218

6.9 References 218

7 MICROBIAL ECOLOGY AND BIOGEOCHEMISTRY OF OXYGEN]DEFICIENT WATER COLUMNS 231
Klaus Jürgens and Gordon T. Taylor

7.1 Introduction 231

7.2 Current Trends 233

7.3 Characterizing Oxygen Deficiency: Terms and Definitions 234

7.4 Types of Oxygen]Deficient Aquatic Systems 237

7.5 Physico]Chemical Profiles as Indicators of Biogeochemical Zones 240

7.6 General Considerations of Microbial Metabolism in ODWCs 243

7.7 Biogeochemical Cycles in Oxygen]Deficient Systems and Major Prokaryotes Involved 249

7.7.1 Carbon Cycle 252

7.7.2 Nitrogen Cycle 254

7.7.3 Sulfur Cycle 261

7.7.4 Trace Metal Cycling (with a Focus on Manganese) 264

7.8 Microbial Food Webs in ODWCs 265

7.9 Summary 272

7.10 Acknowledgments 273

7.11 References 273

8 THE OCEAN’S MICROSCALE: A MICROBE’S VIEW OF THE SEA 289
Justin R. Seymour and Roman Stocker

8.1 Introduction 289

8.2 The Microscale Physics of the Pelagic Ocean 292

8.2.1 The Importance of Cell]to]Cell Distance 292

8.2.2 A World Dominated by Diffusion 295

8.2.3 The Effects of Turbulence at the Microscale 299

8.2.4 Other Effects of Flow on Marine Microbes 301

8.3 Particles, Patches, and Phycospheres 302

8.3.1 Particles as Resource Islands 302

8.3.2 A Continuum of Organic Matter? 303

8.3.3 Microbial Processes Create Patchiness 305

8.3.4 The Phycosphere 306

8.4 Motility and Chemotaxis 306

8.4.1 Motility in the Ocean 307

8.4.2 Chemotaxis to Microscale Hotspots 313

8.5 Microscale Microbial Interactions 319

8.5.1 Quorum Sensing in Microscale Hotspots 319

8.5.2 Antagonistic Interactions within Microscale Habitats 321

8.5.3 Symbiosis within the Phycosphere 322

8.6 Microbial Metabolic Adaptions to Microscale Heterogeneity in Seawater 325

8.7 Biogeochemical Implications of Microscale Interactions 327

8.7.1 Phytoplankton Production 327

8.7.2 Carbon Cycling 328

8.7.3 Nitrogen Cycling 329

8.7.4 Sulfur Cycling 330

8.8 Summary 331

8.9 Acknowledgments 332

8.10 References 332

9 ECOLOGICAL GENOMICS OF MARINE VIRUSES 345
Jennifer R. Brum and Matthew B. Sullivan

9.1 Introduction 345

9.2 Genomics of Isolated Marine Viruses 348

9.3 Investigating Viral Community Diversity in Nature 350

9.4 Marine Viral Community Diversity and Structure 351

9.4.1 Estimating the Size of the Global Virome 353

9.4.2 Estimating Viral Richness 354

9.4.3 Marine Viral Community Structure and Ecological Drivers 354

9.5 Depth]Related Patterns Emerging from Analysis of Marine Viral Metagenomic Data Sets 356

9.6 Emerging Temporal Patterns in Marine Viral Communities 359

9.7 Annotating the Unknown: The Need for Creative Solutions 361

9.8 Investigation of Virus]Host Interactions in the Wild 364

9.9 Future Challenges in Marine Viral Ecology 365

9.9.1 The Need to Capture Other Viral Types 365

9.9.2 Moving Beyond Upper]Ocean Waters 366

9.9.3 Making the Genes]to]Ecosystems Leap to Evaluate Processes 367

9.10 Summary 368

9.11 Acknowledgments 369

9.12 References 369

10 MICROBIAL PHYSIOLOGICAL ECOLOGY OF THE MARINE PHOSPHORUS CYCLE 377
Sonya T. Dyhrman

10.1 Introduction 377

10.2 Methodological Advances and Challenges 379

10.3 Phosphorus Biogeochemistry 382

10.3.1 The Phosphorus Cycle 382

10.3.2 Sources and Sinks 382

10.3.3 Phosphorus Stoichiometry 383

10.4 Phosphorus in the Cell 383

10.4.1 Phosphorus Biochemicals 383

10.4.2 Phosphorus Redox State 385

10.4.3 Phosphorus Bond Classes 386

10.5 Microbial Biogeochemistry of Phosphorus Bond Types 386

10.5.1 Polyphosphate 387

10.5.2 Phosphoester 389

10.5.3 Phosphonate 390

10.6 Inorganic Phosphorus Utilization 391

10.6.1 Phosphate Uptake 391

10.6.2 Polyphosphate Utilization 393

10.6.3 Phosphite Metabolism 394

10.7 Organic Phosphorus Utilization 395

10.7.1 Phosphoester Enzymes 395

10.7.2 Phosphonate Enzymes 400

10.8 Phosphorus Stress Responses 402

10.8.1 Phosphorus Stress Signaling 405

10.8.2 Phosphorus Sparing or Recycling 406

10.8.3 High]Affinity or Increased Phosphate Transport 410

10.8.4 Utilization of Alternative Phosphorus Forms 410

10.9 Case Studies in Phosphorus Physiology 411

10.9.1 Bacteria: Pelagibacter 411

10.9.2 Diazotroph: Trichodesmium 413

10.9.3 Archaea: Nitrosopumilus 414

10.9.4 Microeukaryote: Thalassiosira 415

10.10 Case Studies with Different Systems 416

10.10.1 Western North Atlantic 416

10.10.2 Mediterranean 417

10.10.3 Gulf of Mexico 418

10.11 Summary 419

10.12 Acknowledgments 420

10.13 References 420

11 PHYTOPLANKTON FUNCTIONAL TYPES: A TRAIT PERSPECTIVE 435
Andrew J. Irwin and Zoe V. Finkel

11.1 What Are Functional Types? 435

11.2 The Major Functional Traits 437

11.2.1 What Is a Trait? 437

11.2.2 Types of Traits 438

11.2.3 Size as a Master Trait 443

11.2.4 Trait Trade]Offs 445

11.2.5 Trait Differences across Phytoplankton Functional Types 445

11.3 Challenges Using Traits to Represent Functional Types 446

11.3.1 Challenges Estimating Average Trait Values for Phytoplankton Functional Types 446

11.3.2 Challenges Posed by Acclimation and Adaptation 449

11.4 Using Field Data to Identify Relevant Traits and Estimate Trait Values 450

11.4.1 Why Use Field Data? 450

11.4.2 How Can We Identify Traits and Niches of Phytoplankton Functional Types from Field Data? 452

11.4.3 Are Phytoplankton Niches Stable over Time? 453

11.5 Should We Model Functional Types or Individual Species? 455

11.6 A Way Forward 457

11.7 Summary 459

11.8 References 459

12 THEORETICAL INTERPRETATIONS OF SUBTROPICAL PLANKTON BIOGEOGRAPHY 467
Michael J. Follows, Stephanie Dutkiewicz, Ben A. Ward and Christopher N. Follett

12.1 Introduction: Phytoplankton Biogeography in the Subtropical Ocean 468

12.2 Resource Competition, Fitness, and Cell Size 476

12.3 Coexisting Size Classes: Predation Levels the Playing Field 481

12.4 Niche Differentiation and Resource Ratio Theory 483

12.4.1 Resource Ratio Theory for Nitrogen Fixation 485

12.4.2 Predicted Global Biogeography of Nitrogen Fixation 488

12.5 Discussion and Outlook 488

12.5.1 Outlook 489

12.6 Summary 490

12.7 Acknowledgments 490

12.8 References 491

INDEX 495