Modeling tailed bacteriophage adsorption: Insight into mechanisms.

The process of a bacteriophage attaching to its host cell is a combination of physical diffusion, biochemical surface interactions, and reaction-induced conformational changes in receptor proteins. Local variations in the physico-chemical properties of the medium, the phage׳s mode of action, and the physiology of the host cell also all influence adsorption kinetics. These characteristics can affect a specific phage׳s binding capabilities and the susceptibility of the host cell to phage attack. Despite the complexity of this process, describing adsorption kinetics of a population of bacteriophages binding to a culture of cells has been accomplished with relatively simple equations governed by the laws of mass-action. Many permutations and modifications to the basic set of reactions have been suggested through the years. While no single solution emerges as a universal answer, this review provides the fundamentals of current phage adsorption modeling and will guide researchers in the selection of valid, appropriate models.

[1]  T. Lenormand,et al.  PHENOTYPIC STOCHASTICITY PROTECTS LYTIC BACTERIOPHAGE POPULATIONS FROM EXTINCTION DURING THE BACTERIAL STATIONARY PHASE , 2012, Evolution; international journal of organic evolution.

[2]  John W. Beaber,et al.  Genetic Evidence for the Involvement of the S-Layer Protein Gene sap and the Sporulation Genes spo0A, spo0B, and spo0F in Phage AP50c Infection of Bacillus anthracis , 2013, Journal of bacteriology.

[3]  A. Buckling,et al.  Introducing yesterday's phage therapy in today's medicine , 2012 .

[4]  E. Änggård,et al.  A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic‐resistant Pseudomonas aeruginosa; a preliminary report of efficacy , 2009, Clinical otolaryngology : official journal of ENT-UK ; official journal of Netherlands Society for Oto-Rhino-Laryngology & Cervico-Facial Surgery.

[5]  E. Chapman-McQuiston,et al.  Stochastic receptor expression allows sensitive bacteria to evade phage attack. Part I: experiments. , 2008, Biophysical journal.

[6]  E. Schnabel,et al.  Isolation and Characterization of FiveErwinia amylovora Bacteriophages and Assessment of Phage Resistance in Strains of Erwinia amylovora , 2001, Applied and Environmental Microbiology.

[7]  M. van Heel,et al.  Structure, Adsorption to Host, and Infection Mechanism of Virulent Lactococcal Phage p2 , 2013, Journal of Virology.

[8]  A. L. Koch The growth of viral plaques during the enlargement phase. , 1964, Journal of theoretical biology.

[9]  F. M. Stewart,et al.  Resource-Limited Growth, Competition, and Predation: A Model and Experimental Studies with Bacteria and Bacteriophage , 1977, The American Naturalist.

[10]  G. Węgrzyn,et al.  Bacteriophage T4 can produce progeny virions in extremely slowly growing Escherichia coli host: comparison of a mathematical model with the experimental data. , 2014, FEMS microbiology letters.

[11]  Tobin J Dickerson,et al.  Bacteriophage-mediated protein delivery into the central nervous system and its application in immunopharmacotherapy , 2005, Expert opinion on biological therapy.

[12]  S. Chatterjee,et al.  Interaction of Bacteriophage λ with Its E. coli Receptor, LamB , 2012, Viruses.

[13]  M. Schwartz,et al.  The adsorption of coliphage lambda to its host: effect of variations in the surface density of receptor and in phage-receptor affinity. , 1976, Journal of molecular biology.

[14]  G. Volckaert,et al.  Quality-Controlled Small-Scale Production of a Well-Defined Bacteriophage Cocktail for Use in Human Clinical Trials , 2009, PloS one.

[15]  Michel Meunier,et al.  Surface plasmon resonance detection of E. coli and methicillin-resistant S. aureus using bacteriophages. , 2012, Biosensors & bioelectronics.

[16]  Jack A Heinemann,et al.  Models of phage growth and their applicability to phage therapy. , 2004, Journal of theoretical biology.

[17]  J. R. Christensen The kinetics of reversible and irreversible attachment of bacteriophage T-1. , 1965, Virology.

[18]  M. Loessner,et al.  Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells , 1996, Applied and environmental microbiology.

[19]  Evelien M. Adriaenssens,et al.  T4-Related Bacteriophage LIMEstone Isolates for the Control of Soft Rot on Potato Caused by ‘Dickeya solani’ , 2012, PloS one.

[20]  A. Zaritsky,et al.  The initial adsorption of T4 bacteriophages to Escherichia coli cells at equivalent concentrations: Experiments and mathematical modeling , 2010 .

[21]  F. Twort AN INVESTIGATION ON THE NATURE OF ULTRA-MICROSCOPIC VIRUSES. , 1915 .

[22]  I. Molineux,et al.  Diagnostic Bioluminescent Phage for Detection of Yersinia pestis , 2009, Journal of Clinical Microbiology.

[23]  G. Stent,et al.  On the two step nature of bacteriophage absorption. , 1952, Biochimica et biophysica acta.

[24]  I. Huys,et al.  Optimizing the European Regulatory Framework for Sustainable Bacteriophage Therapy in Human Medicine , 2012, Archivum Immunologiae et Therapiae Experimentalis.

[25]  I. Connerton,et al.  Bacteriophage Therapy To Reduce Campylobacter jejuni Colonization of Broiler Chickens , 2005, Applied and Environmental Microbiology.

[26]  A. Obradović,et al.  Bacteriophages for plant disease control. , 2007, Annual review of phytopathology.

[27]  Eugénio C. Ferreira,et al.  Population Dynamics of a Salmonella Lytic Phage and Its Host: Implications of the Host Bacterial Growth Rate in Modelling , 2014, PloS one.

[28]  J. Dushoff,et al.  Alternative stable states in host–phage dynamics , 2008, Theoretical Ecology.

[29]  M. Schlesinger Über die Bindung des Bakteriophagen an homologe Bakterien , 1932, Zeitschrift für Hygiene und Infektionskrankheiten.

[30]  M. Loessner,et al.  Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2. , 2012, International journal of food microbiology.

[31]  A. Kropinski,et al.  Romulus and Remus, Two Phage Isolates Representing a Distinct Clade within the Twortlikevirus Genus, Display Suitable Properties for Phage Therapy Applications , 2013, Journal of Virology.

[32]  Takashi Yamada,et al.  Biocontrol of Ralstonia solanacearum by Treatment with Lytic Bacteriophages , 2011, Applied and Environmental Microbiology.

[33]  S. Andleeb,et al.  Characterization of a virulent bacteriophage LK1 specific for Citrobacter freundii isolated from sewage water , 2014, Journal of basic microbiology.

[34]  Mark Ptashne,et al.  A Genetic Switch, Phage Lambda Revisited , 2004 .

[35]  Bo Hu,et al.  The Bacteriophage T7 Virion Undergoes Extensive Structural Remodeling During Infection , 2013, Science.

[36]  G. Wolf,et al.  A mathematical model for the reversible two-step interaction between the T5 phage and its receptor in vitro , 1980 .

[37]  M. Schlesinger Über die Bindung des Bakteriophagen an homologe Bakterien , 1932, Zeitschrift für Hygiene und Infektionskrankheiten.

[38]  T. Nakai,et al.  Bacteriophage control of Pseudomonas plecoglossicida infection in ayu Plecoglossus altivelis. , 2003, Diseases of aquatic organisms.

[39]  B. Levin,et al.  Phage Therapy Revisited: The Population Biology of a Bacterial Infection and Its Treatment with Bacteriophage and Antibiotics , 1996, The American Naturalist.

[40]  H. Berg,et al.  Physics of chemoreception. , 1977, Biophysical journal.

[41]  Christian Cambillau,et al.  Structures and host-adhesion mechanisms of lactococcal siphophages , 2014, Front. Microbiol..

[42]  V A Petrenko,et al.  The effect of salt and phage concentrations on the binding sensitivity of magnetoelastic biosensors for Bacillus anthracis detection , 2008, Biotechnology and bioengineering.

[43]  C. Rees,et al.  Bacteriophage applications: where are we now? , 2010, Letters in applied microbiology.

[44]  H. Steensma An evaluation of the rate constants for the adsorption of the defective phage PBS Z to Bacillus subtilis , 1982, Antonie van Leeuwenhoek.

[45]  Daniel Campos,et al.  Approximate solution to the speed of spreading viruses. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[46]  E. Chapman-McQuiston,et al.  On kinetics of phage adsorption. , 2007, Biophysical journal.

[47]  E. Dey,et al.  Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. , 2010, Polish journal of microbiology.

[48]  A. Garen Thermodynamic and kinetic studies on the attachment of Tl bacteriophage to bacteria , 1954 .

[49]  T. Puck The first steps of virus invasion. , 1953, Cold Spring Harbor symposia on quantitative biology.

[50]  V. Jansen,et al.  Understanding bacteriophage therapy as a density-dependent kinetic process. , 2001, Journal of theoretical biology.

[51]  L. You,et al.  Amplification and spread of viruses in a growing plaque. , 1999, Journal of theoretical biology.

[52]  Dominic Sauvageau,et al.  Evidence That the Heterogeneity of a T4 Population Is the Result of Heritable Traits , 2014, PloS one.

[53]  W. Tan,et al.  Evaluation of a lytic bacteriophage, Φ st1, for biocontrol of Salmonella enterica serovar Typhimurium in chickens. , 2014, International journal of food microbiology.

[54]  C. São-José,et al.  Phage SPP1 Reversible Adsorption to Bacillus subtilis Cell Wall Teichoic Acids Accelerates Virus Recognition of Membrane Receptor YueB , 2008, Journal of bacteriology.

[55]  J. McCaskill,et al.  Replication of viruses in a growing plaque: a reaction-diffusion model. , 1992, Biophysical journal.

[56]  Dominic Sauvageau,et al.  Modeling bacteriophage attachment using adsorption efficiency , 2012 .

[57]  Dominic Sauvageau,et al.  Bacteriophages as antimicrobial agents against bacterial contaminants in yeast fermentation processes , 2014, Biotechnology for Biofuels.

[58]  A. Garen Thermodynamic and kinetic studies on the attachment of T1 bacteriophage to bacteria. , 1954, Biochimica et biophysica acta.

[59]  R. Hendrix,et al.  Bacteriophage lambda PaPa: not the mother of all lambda phages. , 1992, Science.

[60]  J. Sha,et al.  Mutated and Bacteriophage T4 Nanoparticle Arrayed F1-V Immunogens from Yersinia pestis as Next Generation Plague Vaccines , 2013, PLoS pathogens.

[61]  H. Steensma Adsorption of the defective phage PBS Z1 to Bacillus subtilis 168 Wt. , 1981, The Journal of general virology.

[62]  G. Jensen,et al.  Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus , 2011, Proceedings of the National Academy of Sciences.

[63]  T. Puck,et al.  THE MECHANISM OF VIRUS ATTACHMENT TO HOST CELLS , 1950, The Journal of experimental medicine.

[64]  B. Chin,et al.  Detection and identification of methicillin resistant and sensitive strains of Staphylococcus aureus using tandem measurements. , 2012, Journal of microbiological methods.

[65]  T. Puck,et al.  THE FIRST TWO STEPS OF THE INVASION OF HOST CELLS BY BACTERIAL VIRUSES. II , 1951, The Journal of experimental medicine.

[66]  S. Abedon,et al.  Bacteriophage evolution given spatial constraint. , 2007, Journal of theoretical biology.

[67]  A. Zaritsky,et al.  Bacteriophage T4 development depends on the physiology of its host Escherichia coli. , 1997, Microbiology.

[68]  D. Stopar Bacteriophage Ecology: Modeling bacteriophage population growth , 2008 .

[69]  A. P. Krueger THE SORPTION OF BACTERIOPHAGE BY LIVING AND DEAD SUSCEPTIBLE BACTERIA , 1931, The Journal of general physiology.

[70]  D. Cooper,et al.  Two-stage, self-cycling process for the production of bacteriophages , 2010, Microbial cell factories.

[71]  M. Deshusses,et al.  Reduction of invasive bacteria in ethanol fermentations using bacteriophages , 2015, Biotechnology and bioengineering.

[72]  Dominic Sauvageau,et al.  Bacteriophage adsorption efficiency and its effect on amplification , 2010, Bioprocess and biosystems engineering.

[73]  Richard L Leask,et al.  Impact of the cell life-cycle on bacteriophage T4 infection. , 2014, FEMS microbiology letters.

[74]  A. Chopra,et al.  In vitro and in vivo delivery of genes and proteins using the bacteriophage T4 DNA packaging machine , 2013, Proceedings of the National Academy of Sciences.

[75]  Michael S Strano,et al.  Virus-templated self-assembled single-walled carbon nanotubes for highly efficient electron collection in photovoltaic devices. , 2011, Nature nanotechnology.

[76]  Rodolphe Barrangou,et al.  The Population and Evolutionary Dynamics of Phage and Bacteria with CRISPR–Mediated Immunity , 2013, PLoS genetics.

[77]  J. Maniloff,et al.  Adsorption of the tailed mycoplasma virus L3 to cell membranes , 1982, Journal of virology.

[78]  M. Kuskowski,et al.  Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. , 2009, Journal of wound care.

[79]  A. Buckling,et al.  The Phage Therapy Paradigm: Prêt-à-Porter or Sur-mesure? , 2011, Pharmaceutical Research.

[80]  T. F. Anderson The reactions of bacterial viruses with their host cells , 1949, The Botanical Review.

[81]  Peixuan Guo,et al.  Construction of Bacteriophage Phi29 DNA Packaging Motor and its Applications in Nanotechnology and Therapy , 2009, Annals of Biomedical Engineering.

[82]  J. Bull,et al.  Phenotypic Resistance and the Dynamics of Bacterial Escape from Phage Control , 2014, PloS one.

[83]  E. Chapman-McQuiston,et al.  Stochastic receptor expression allows sensitive bacteria to evade phage attack. Part II: theoretical analyses. , 2008, Biophysical journal.

[84]  M. A. Lauffer,et al.  FUNCTIONS AND PROPERTIES RELATED TO THE TAIL FIBERS OF BACTERIOPHAGE T4. , 1965, Virology.

[85]  Ido Golding,et al.  Single-virus tracking reveals a spatial receptor-dependent search mechanism. , 2011, Biophysical journal.