Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses (Advances in Molecular and Cellular Microbiology, Series Number 15)

Bacteriophages, or phages, are viruses that infect bacteria and are believed to be the most abundant and genetically diverse organisms on Earth. As such, their ecology is vast both in quantitative and qualitative terms. Their abundance makes an understanding of phage ecology increasingly relevant to bacterial ecosystem ecology, bacterial genomics and bacterial pathology. Abedon provides the first text on phage ecology for almost 20 years. Written by leading experts, synthesizing the three key approaches to studying phage ecology, namely studying them in natural environments (in situ), experimentally in the lab, or theoretically using mathematical or computer models. With strong emphasis on microbial population biology and distilling cutting-edge research into basic principles, this book will complement other currently available volumes. It will therefore serve as an essential resource for graduate students and researchers, particularly those with an interest in phage ecology and evolutionary biology. Half-title......Page 3 Title......Page 7 Copyright......Page 8 Contents......Page 9 About the cover......Page 11 Contributors......Page 13 Foreword......Page 16 Preface......Page 19 1.1 INTRODUCTION......Page 21 1.2.1.1 Phages as viruses of bacteria......Page 22 1.2.1.2 Phages as unicellular-organism parasites......Page 23 1.2.2 Phages in terms of their diversity......Page 24 1.2.2.3 Phage types......Page 25 1.2.2.4 Types of phage infection......Page 27 1.2.2.4.1 Another word on pseudolysogeny......Page 30 1.2.2.5 Virulence versus temperance......Page 31 1.2.3.1 Phages as ecosystem modifiers......Page 32 1.2.3.2 Phages increase bacterial diversity......Page 33 1.2.3.3 Phage ubiquity and prevalence......Page 34 1.3 WHAT IS PHAGE ECOLOGY?......Page 35 1.4 WHAT IS PHAGE EVOLUTIONARY BIOLOGY?......Page 36 1.4.4 Phage evolutionary ecology......Page 37 REFERENCES......Page 38 Part I Phage ecology......Page 49 2.1 INTRODUCTION......Page 51 2.2 MATHEMATICAL ECOLOGY......Page 52 2.2.1 Lotka–Volterra modeling......Page 53 2.2.2 Modeling predator–prey dynamics using phages......Page 55 2.2.3 More complex phage-based models......Page 56 2.3.1 Microbial modules......Page 57 2.3.3.1 Trade-offs are stabilizing......Page 59 2.3.4 Communities with partially resistant bacteria......Page 61 2.3.5 Communities with phage host-range variants......Page 62 2.4.1 Optimal foraging theory......Page 63 2.4.2 Optimal “phoraging” theory......Page 64 2.4.3 Complications on phage optimal foraging......Page 68 2.5.1 Harmony through asynchrony......Page 69 2.5.2 Metacommunities of bacteria and phages......Page 70 2.6.1 Phage productivity versus competitive ability......Page 72 2.6.3 Evolution of restraint given spatial structure......Page 73 2.6.4 Evolution of restraint with vertical transmission......Page 74 2.7 FUTURE DIRECTIONS......Page 75 2.8 APPENDIX......Page 77 REFERENCES......Page 78 3.1.1 Productive phage infection......Page 84 3.1.2 Life-history optimization......Page 85 3.2.1 Selection during low-multiplicity growth (I)......Page 86 3.2.1.1 Strategies for effective exploitative competition......Page 87 3.2.1.2 Impact of bacterial density on latent-period evolution......Page 88 3.2.2 Selection acting at multiplicities approaching one (II)......Page 89 3.2.3 Selection acting at multiplicities of greater than one (III)......Page 90 3.2.5 Selection acting post population-wide lysis (V)......Page 91 3.3.1 Expedient versus economical phage population growth......Page 92 3.3.1.2 Shorter latent periods versus larger burst sizes......Page 93 3.3.1.4 Periodic dissemination as a selective force......Page 96 3.3.1.5 Founder effects and maintenance of clonality......Page 97 3.3.2 Phage virulence......Page 98 3.3.3 Selection for economy during dissemination......Page 100 3.4 SCENARIOS FOR PHAGE POPULATION GROWTH......Page 101 3.4.1 Initiating phage population growth......Page 102 3.4.2 Sustaining phage population growth......Page 103 3.4.4 Solving the exponential growth dilemma......Page 104 3.4.7 Positive-feedback selection and other problems......Page 105 3.4.9 Conclusion......Page 106 3.5 APPENDIX: PHAGE MULTIPLICITY OF ADSORPTION......Page 107 REFERENCES......Page 109 4.1 INTRODUCTION......Page 114 4.2 HOW PLAQUES FORM......Page 115 4.2.2 Stage 2: first adsorption/infection......Page 116 4.2.3.1 Alternating infection and diffusion, plus lawn growth......Page 117 4.2.3.3 Three sub-stages of plaque-size increase......Page 118 4.2.3.4.1 Predicting plaque front velocities......Page 119 4.2.4 Stage 4: termination of phage population growth......Page 120 4.2.5.1 Continued virion spreading......Page 121 4.3 PLAQUE SIZE AND MORPHOLOGY......Page 122 4.3.2.1 Plaque-morphology mutations......Page 123 4.3.2.2 Within-plaque inhomogeneity......Page 126 4.5 APPENDIX: ROLE OF TIME DEPENDENCE......Page 129 ACKNOWLEDGMENTS......Page 130 REFERENCES......Page 131 5.1 INTRODUCTION......Page 134 5.1.1.1 Lysogeny......Page 135 5.1.1.2 Pseudolysogeny......Page 136 5.2.1 Impact of nutrients on phage replication......Page 137 5.2.3 Impact of inorganic factors on phage lytic growth......Page 138 5.2.5 The paradox of viral numbers......Page 139 5.3.1 The lytic–lysogenic decision......Page 140 5.3.3 Lysogeny in aquatic environments......Page 141 5.3.4 Lysogen induction in aquatic environments......Page 142 5.3.5 Lysogeny in terrestrial environments......Page 143 5.3.7 Ecological relevance of lysogeny......Page 144 5.4.1 Defining pseudolysogeny......Page 145 5.4.2.1 Pseudolysogeny with Pseudomonas hosts......Page 147 5.4.2.2 Additional examples of pseudolysogeny......Page 149 5.5 PHAGE-INDUCED HOST ALTERATION......Page 151 5.5.2 “Lytic” conversion......Page 152 5.6 CONCLUSIONS......Page 153 REFERENCES......Page 154 Part II Phage evolutionary biology......Page 165 6.1 INTRODUCTION......Page 167 6.2 WHAT IS EVOLUTIONARY BIOLOGY?......Page 168 6.3.1 Mutation......Page 169 6.3.2 Recombination......Page 171 6.4.1 Natural selection......Page 172 6.4.1.1 Measuring fitness......Page 173 6.4.1.2 Consequences of selection......Page 174 6.4.1.3 Neutrality and selection against deleterious alleles......Page 175 6.4.1.4 Levels of selection......Page 176 6.4.2 Genetic drift......Page 177 6.4.2.1 Muller’s ratchet......Page 179 6.5.1 Trade-offs......Page 180 6.5.2 Epistasis......Page 182 6.5.2.1 Compensatory mutations......Page 184 6.5.3 Evolvability and robustness......Page 185 6.6.2 Phage “speciation”......Page 186 6.6.3 Host shifting......Page 187 6.6.5 Recombination and barriers to gene flow......Page 188 6.8 CONCLUDING REMARKS......Page 189 REFERENCES......Page 190 7.1 INTRODUCTION......Page 197 7.1.2 Phage diversity......Page 198 7.1.3 Biases in phage sampling......Page 199 7.2 GENOME COMPARISONS OF dsDNA TAILED PHAGES......Page 200 7.2.1.1 Non-homologous recombination......Page 201 7.2.1.2 Homologous recombination......Page 203 7.2.1.3 Coevolving gene groups......Page 204 7.2.3 Additions to the genome and genome rearrangements......Page 205 7.3 POPULATION STRUCTURE AND METAGENOMIC STUDIES......Page 207 7.4 OTHER PHAGES AND DEEP PHYLOGENY......Page 209 7.5 CONCLUSION......Page 211 REFERENCES......Page 212 8.1.1 Evolutionary ecology of phage–phage interaction......Page 215 8.1.2 Multiple adsorption and infection terminology......Page 216 8.2 PROXIMATE EFFECTS OF COINFECTION......Page 217 8.2.1 Sex......Page 218 8.2.3 Complementation......Page 219 8.2.4 Intracellular competition......Page 220 8.3.1 Phage φ6 and coinfection......Page 221 8.3.3 Ultimate consequences of coinfection (sexuality)......Page 222 8.3.3.2 Selection for intracellular replication strategies......Page 223 8.3.3.3 Coinfection and game theory......Page 224 8.3.3.4 Phages, sex, and adaptation......Page 225 8.3.3.5 Phages, sex, and purifying selection......Page 226 8.4.1 Long-term hyperparasitism (P4-like phages)......Page 227 8.4.2 Phage biogeography......Page 228 8.5.1 Coinfection weakens selection for robust genomes......Page 229 8.5.2 Sex and the selfish gene......Page 230 8.6 CLOSING REMARKS......Page 232 REFERENCES......Page 233 9.1.1 Why phages? Easy manipulation, rapid evolution, sequencing......Page 237 9.1.3 Patterns of adaptation and fitness change......Page 238 9.2.1 Matching design with theory......Page 239 9.2.3 Biases against certain mechanisms......Page 241 9.2.4 Competing beneficial mutations and recombination......Page 242 9.2.4.3 Interference from epistasis......Page 243 9.3.1.1 Adaptive walks......Page 244 9.3.1.2 Landscape topology......Page 245 9.3.2 Increasing rates of adaptation: N·μ·s......Page 246 9.4.1 Fitness limits......Page 247 9.4.1.2 Comparison between different genome types......Page 248 9.4.1.3 Possible additional approaches......Page 249 9.4.2 Routes toward higher fitness: redundancy, divergence......Page 250 9.4.3.1 First steps......Page 251 9.4.3.2 Steps across the entire walk: sizes and order......Page 253 9.4.3.3 The largest step is often big......Page 254 9.4.3.4 Rates of substitution......Page 255 9.5 RECOMBINATION......Page 257 9.6.1 Methods of propagation......Page 258 9.6.1.2 Liquid culture, two-tube chemostat......Page 259 9.6.1.4 Plates......Page 260 9.6.2.1 Selection for propagation......Page 261 9.7 CONCLUSION......Page 262 REFERENCES......Page 263 Part III Phage ecology in environments......Page 269 10.1 INTRODUCTION......Page 271 10.2 VIRAL ABUNDANCE......Page 272 10.3.1 Detection of viral production......Page 273 10.3.3 Lytic or lysogenic?......Page 275 10.3.4 Factors controlling viral activity......Page 276 10.3.5 Aquatic viral diversity......Page 277 10.4.1 Viruses and organic-carbon release......Page 278 10.5 ECOLOGICAL THEORY OF AQUATIC FOOD WEBS......Page 280 10.5.1.1 Hutchinson’s paradox......Page 281 10.5.1.2 A viral solution to Hutchinson’s paradox......Page 282 10.5.2.1 Number of simultaneously dominant host populations......Page 285 10.5.2.2 Number of simultaneously dominant virus groups......Page 287 10.5.2.3 Phage abundance......Page 288 10.5.3 More biogeochemical impacts......Page 289 10.5.4.1 Support for hypothesis H1......Page 290 10.5.4.4 Support (or lack thereof) for hypothesis H4......Page 291 REFERENCES......Page 292 11.1 INTRODUCTION......Page 301 11.1.1.1 Soil......Page 302 11.1.1.2 Biome-to-biome diversity......Page 303 11.2.1.1 Virion durability......Page 304 11.2.1.2 Lysogeny......Page 306 11.2.2 Spatial heterogeneity......Page 307 11.3 PHAGE EXISTENCE IN SOIL......Page 308 11.3.1 High soil phage densities......Page 309 11.3.2 Impact of terrestrial environments on phage......Page 310 11.4.1 Quantitative impact of phages on terrestrial bacteria......Page 311 11.4.2 Qualitative impact of phages on terrestrial bacteria......Page 312 11.5.1 Transduction......Page 314 11.5.2 Transduction in terrestrial ecosystems, etc.......Page 315 11.5.3 Transduction prevalence in the wild......Page 316 11.6 CONCLUSIONS AND UNANSWERED QUESTIONS......Page 317 REFERENCES......Page 318 12.1 INTRODUCTION......Page 322 12.2.1 Dairy phages......Page 323 12.2.2 Indigenous phages in other fermented foods......Page 324 12.2.3 Phages as indicators of fecal contamination......Page 325 12.2.4 Phages as animal-virus surrogates......Page 327 12.3 DETECTION OF FOODBORNE PATHOGENS......Page 328 12.3.1.1 Qualitative detection of foodborne bacteria......Page 329 12.3.1.2 Quantification of foodborne bacteria......Page 330 12.3.2 Labeled bacteriophage assays......Page 331 12.3.3 Bacteriophage amplification......Page 332 12.4 PHAGE-MEDIATED BIOCONTROL OF BACTERIA......Page 333 12.4.1.1 Control of Escherichia coli O157:H7......Page 334 12.4.1.2 Control of Salmonella spp.......Page 335 12.4.1.3 Control of Campylobacter jejuni......Page 336 12.4.1.4 Control of Listeria monocytogenes......Page 337 12.4.2 Bacteriophage biocontrol of food spoilage......Page 338 12.4.3 Phage stability within the food matrix......Page 339 12.5 THE FUTURE IS NOW......Page 340 12.6.1 Bacterial density and free-phage loss rates......Page 341 12.6.2 Phage density and bacterial loss rates......Page 343 REFERENCES......Page 344 13.1 INTRODUCTION......Page 352 13.2 POTENTIAL FOR PHAGE–ANIMAL INTERACTION......Page 353 13.3 THE FATE OF PHAGES ADMINISTERED TO ANIMALS......Page 355 13.3.2 Phage interactions with the innate immune system......Page 356 13.3.4 Phages in the nasopharnyx and central nervous system......Page 358 13.4 PHAGE APPLICATIONS IN ANIMALS......Page 359 13.4.1 Phage antibacterial therapies......Page 360 13.4.2 Phage-based vaccines......Page 361 13.4.3 Phage-based gene delivery systems......Page 362 13.4.4 Phage interactions with the vascular system......Page 363 13.5.1 Phage metabolic impact on mammalian cells......Page 364 13.6 CONCLUSION......Page 366 REFERENCES......Page 367 14.1 INTRODUCTION......Page 373 14.2.1 Linkage and linkage disequilibrium......Page 374 14.2.2 Prophage–bacterial co-replication......Page 375 14.2.3 VF gene–phage co-replication......Page 376 14.2.4 Lack of φVFs in obligately lytic phages......Page 379 14.3.1 Linkage and epistasis......Page 380 14.3.3 Enhancement of phage fitness......Page 381 14.4 CONTEXT OF VF EXPRESSION AND UTILITY......Page 382 14.4.1 VFs and the colon as a bacterial niche......Page 383 14.4.2 VFs and the colon as a phage niche......Page 384 14.5 SURVEY OF EXOTOXIN-ENCODING PHAGES......Page 385 14.5.2 Escherichia coli......Page 386 14.5.2.1 STEC and Shiga toxin......Page 387 14.5.2.2 Stx and Stx-encoding phage induction and release......Page 388 14.5.3 Vibrio cholerae......Page 389 14.5.4 Salmonella enterica......Page 391 14.5.6 Clostridium botulinum......Page 392 14.6.1 Phage transmission in animals......Page 393 14.6.2 Host-range breadth of VF-encoding phages......Page 394 14.6.3 Contribution of phage transmission to pathogenesis......Page 395 14.7 CONCLUSIONS......Page 396 REFERENCES......Page 397 Part IV Modeling phage ecology......Page 407 15.1 INTRODUCTION......Page 409 15.2.2 Adsorption......Page 410 15.2.2.1 Law of mass action......Page 412 15.2.3 Latent period and burst size......Page 413 15.3.1 Algorithms for simulating phage population growth......Page 414 15.3.2 Simulating phage population growth......Page 416 15.3.3 Algorithms used to simulate phage–bacterial co-culture......Page 418 15.4 CHEMOSTAT PHAGE–BACTERIAL CO-CULTURE......Page 420 15.4.2.1 Modeling chemostat bacterium losses and gains......Page 421 15.4.2.3 Modeling phage losses and gains......Page 423 15.4.2.5 Summary of a chemostat model......Page 425 15.4.2.7 Simulations of chemostat co-cultures......Page 426 15.5.1 Fixing steady-state densities without phages......Page 428 15.5.1.3 Simultaneous fixing of substrate and bacteria......Page 429 15.5.2 Continuous models with phage infection......Page 430 15.6 CONCLUDING REMARKS......Page 431 REFERENCES......Page 432 16.1 INTRODUCTION......Page 435 16.2 MODELS OF PLAQUE-DIAMETER INCREASE......Page 436 16.2.1 Koch’s model of plaque enlargement......Page 438 16.2.2.1 Qualitative description of Yin and McCaskill’s model......Page 439 16.2.2.2 Quantitative description of Yin and McCaskill’s model......Page 440 16.2.2.3 Calculating wavefront velocity as plaques spread......Page 442 16.3.1 Modeling a three-dimensional plaque......Page 443 16.3.2 Estimating final plaque radius......Page 445 16.3.3 Estimating plaque productivity......Page 446 16.4 CELLULAR AUTOMATA MODELS......Page 447 16.4.1 Simple CA model for plaque growth......Page 448 16.4.2 CA model with mutation......Page 450 16.4.3.1 Between-plaque competition experiments......Page 451 16.4.3.3 The competition CA model......Page 452 16.5 CONCLUSION......Page 455 REFERENCES......Page 456 17.1 INTRODUCTION......Page 459 17.1.2 Phage therapy......Page 460 17.1.3 Why do we model?......Page 461 17.2 MODELING PHAGE THERAPY......Page 462 17.2.1 Model overview......Page 463 17.2.2 Basic model......Page 464 17.2.3 The Payne and Jansen model......Page 468 17.2.4 Modeling resistance of bacteria to phage......Page 471 17.2.5 Non-mutational resistance......Page 473 17.3 MODELS IN THE REAL WORLD......Page 475 17.3.1 Predictive value of current models......Page 476 17.3.2 Spatial structure and heterogeneous populations......Page 477 17.3.3 Parameter estimation......Page 478 17.4 CONCLUSIONS......Page 481 REFERENCES......Page 482 Index......Page 485