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Phage Infection and Lysis

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Bacteriophages

Abstract

Viruses are differentiated from other mobile genetic elements by the encapsidation of their genomes during some stage of their life cycles. It is during their infection of bacteria that bacteriophage genomes are both generated and encapsidated. Overall, the process of virus infection involves virion acquisition of host cells, the infection itself, and then subsequent release of progeny virions from these cells: adsorption, infection, and release respectively. Successful phage infections also can be either productive or latent. Latent infections for phages generally are described as lysogenic and entail either insertion of a phage’s genome into its host’s chromosome, as a prophage, or instead prophage existence as a plasmid. Productive infections can be differentiated by their associated mechanisms of virion release. Depending on the phage, this can be lytic, but alternatively can involve chronic virion extrusion or budding. The lytic mechanism, which is an intracellularly effected, phage-induced lysis of phage-infected bacteria, appears to be far more common among bacteriophages than chronic release. Elsewhere in this volume, lysogenic infections and lysis-mediating phage endolysins are considered in depth. Here we focus on phage-productive infections and the various mechanisms of phage-induced bacterial lysis. Our emphasis also is on so-called phage growth parameters, including infection durations (latent period) and the number of virions produced per phage-infected bacterium (burst size). Growth parameters can affect the phage ability to negatively impact bacteria, i.e., as ideally is seen in the course of the phage therapy of bacterial infections.

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References

  • Abedon ST (1989) Selection for bacteriophage latent period length by bacterial density: a theoretical examination. Microb Ecol 18:79–88

    Article  CAS  PubMed  Google Scholar 

  • Abedon ST (1990) Selection for lysis inhibition in bacteriophage. J Theor Biol 146:501–511

    Article  CAS  PubMed  Google Scholar 

  • Abedon ST (1994) Lysis and the interaction between free phages and infected cells. In: Karam JD, Kutter E, Carlson K, Guttman B (eds) The molecular biology of bacteriophage T4. ASM Press, Washington, DC, pp 397–405

    Google Scholar 

  • Abedon ST (2008) Ecology of viruses infecting bacteria. In: Mahy BWJ, Van Regenmortel MHV (eds) Encyclopedia of virology, 3rd edn. Elsevier, Oxford, pp 71–77

    Chapter  Google Scholar 

  • Abedon ST (2009a) Bacteriophage intraspecific cooperation and defection. In: Adams HT (ed) Contemporary trends in bacteriophage research. Nova Science Publishers, Hauppauge, pp 191–215

    Google Scholar 

  • Abedon ST (2009b) Deconstructing chemostats towards greater phage-modeling precision. In: Adams HT (ed) Contemporary trends in bacteriophage research. Nova Science Publishers, Hauppauge, pp 249–283

    Google Scholar 

  • Abedon ST (2009c) Disambiguating bacteriophage pseudolysogeny: an historical analysis of lysogeny, pseudolysogeny, and the phage carrier state. In: Adams HT (ed) Contemporary trends in bacteriophage research. Nova Science Publishers, Hauppauge, pp 285–307

    Google Scholar 

  • Abedon ST (2011) Lysis from without. Bacteriophage 1:46–49

    Article  PubMed  PubMed Central  Google Scholar 

  • Abedon ST (2017a) Commentary: communication between viruses guides lysis-Lysogeny decisions. Front Microbiol 8:983

    Article  PubMed  PubMed Central  Google Scholar 

  • Abedon ST (2017b) Phage “delay” towards enhancing bacterial escape from biofilms: a more comprehensive way of viewing resistance to bacteriophages. AIMS Microbiol 3:186–226

    Article  PubMed  PubMed Central  Google Scholar 

  • Abedon ST (2019) Look who’s talking: T-even phage lysis inhibition, the granddaddy of virus-virus intercellular communication research. Viruses 11:951. https://pubmed.ncbi.nlm.nih.gov/31623057/

  • Abedon ST (2020) Phage-phage, phage-bacteria, and phage-environment communication. In: Witzany G (ed) Biocommunication of phages. Springer, Cham

    Google Scholar 

  • Abedon ST, Culler RR (2007a) Bacteriophage evolution given spatial constraint. J Theor Biol 248:111–119

    Article  PubMed  Google Scholar 

  • Abedon ST, Culler RR (2007b) Optimizing bacteriophage plaque fecundity. J Theor Biol 249:582–592

    Article  CAS  PubMed  Google Scholar 

  • Abedon ST, Duffy S, Turner PE (2009) Bacteriophage ecology. In: Schaecter M (ed) Encyclopedia of microbiology. Elsevier, Oxford, pp 42–57

    Chapter  Google Scholar 

  • Abedon ST, Herschler TD, Stopar D (2001) Bacteriophage latent-period evolution as a response to resource availability. Appl Environ Microbiol 67:4233–4241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abedon ST, Hyman P, Thomas C (2003) Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl Environ Microbiol 69:7499–7506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson TF, Doermann AH (1952) The intracellular growth of bacteriophages. II. The growth of T3 studied by sonic disintegration and by T6-cyanide lysis of infected cell. J Gen Physiol 35:657–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benzer S, Hudson W, Weidel W, Delbrück M, Stent GS, Weigle JJ, Dulbecco R, Watson JD, Wollman EL (1950) A syllabus on procedures, facts, and interpretations in phage. In: Delbrück M (ed) Viruses 1950. California Institute of Technology, Pasadena, pp 100–147

    Google Scholar 

  • Bernhardt TG, Wang I-N, Struck DK, Young R (2002) Breaking free: “protein antibiotics” and phage lysis. Res Microbiol 153:493–501

    Article  CAS  PubMed  Google Scholar 

  • Berry J, Rajaure M, Pang T, Young R (2012) The spanin complex is essential for lambda lysis. J Bacteriol 194:5667–5674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blasdel BG, Abedon ST (2012) Superinfection immunity. In: Mayloy S, Hughes K (eds) Brenner’s encyclopedia of genetics. Elsevier/Academic, Amsterdam

    Google Scholar 

  • Bohannan BJM, Lenski RE (1997) Effect of resource enrichment on a chemostat community of bacteria and bacteriophage. Ecology 78:2303–2315

    Article  Google Scholar 

  • Bonachela JA, Levin SA (2014) Evolutionary comparison between viral lysis rate and latent period. J Theor Biol 345:32–42

    Article  PubMed  Google Scholar 

  • Breitbart M, Rohwer F, Abedon ST (2005) Phage ecology and bacterial pathogenesis. In: Waldor MK, Friedman DI, Adhya SL (eds) Phages: their role in bacterial pathogenesis and biotechnology. ASM Press, Washington, DC, pp 66–91

    Google Scholar 

  • Bryan D, El-Shibiny A, Hobbs Z, Porter J, Kutter EM (2016) Bacteriophage T4 infection of stationary phase E. coli: life after log from a phage perspective. Front Microbiol 7:1391

    Article  PubMed  PubMed Central  Google Scholar 

  • Bull JJ (2006) Optimality models of phage life history and parallels in disease evolution. J Theor Biol 241:928–938

    Article  CAS  PubMed  Google Scholar 

  • Bull JJ, Pfennig DW, Wang I-W (2004) Genetic details, optimization, and phage life histories. Trends Ecol Evol 19:76–82

    Article  CAS  PubMed  Google Scholar 

  • Cahill J, Young R (2019) Phage lysis: multiple genes for multiple barriers. Adv Virus Res 103:33–70

    Article  CAS  PubMed  Google Scholar 

  • Chamakura K, Young R (2018) Phage single-gene lysis: finding the weak spot in the bacterial cell wall. J Biol Chem 294:3350–3358

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang C-Y, Nam K, Young R (1995) S gene expression and the timing of lysis by bacteriophage lambda. J Bacteriol 177:3283–3294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaturongakul S, Ounjai P (2014) Phage-host interplay: examples from tailed phages and gram-negative bacterial pathogens. Front Microbiol 5:442

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Young R (2016) The last r locus unveiled: T4 RIII is a cytoplasmic antiholin. J Bacteriol 198:2448–2457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delbrück M (1940) The growth of bacteriophage and lysis of the host. J Gen Physiol 23:643–660

    Article  PubMed  PubMed Central  Google Scholar 

  • Delbrück M (1946) Bacterial viruses or bacteriophages. Biol Rev 21:30–40

    Article  PubMed  Google Scholar 

  • Dennehy JJ, Abedon ST, Turner PE (2007) Host density impacts relative fitness of bacteriophage Φ6 genotypes in structured habitats. Evolution 61:2516–2527

    Article  PubMed  Google Scholar 

  • Dennehy JJ, Wang IN (2011) Factors influencing lysis time stochasticity in bacteriophage lambda. BMC Microbiol 11:174

    Article  PubMed  PubMed Central  Google Scholar 

  • Doermann AH (1951) Intracellular phage growth as studied by premature lysis. Fed Proc 10:591–594

    CAS  PubMed  Google Scholar 

  • Doermann AH (1952) The intracellular growth of bacteriophages I. liberation of intracellular bacteriophage T4 by premature lysis with another phage or with cyanide. J Gen Physiol 35:645–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forterre P (2012) The virocell concept and environmental microbiology. ISME J 7:233–236

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gallet R, Kannoly S, Wang IN (2011) Effects of bacteriophage traits on plaque formation. BMC Microbiol 11:181

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghusinga KR, Dennehy JJ, Singh A (2017) First-passage time approach to controlling noise in the timing of intracellular events. Proc Natl Acad Sci U S A 114:693–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gründling A, Bläsi U, Young R (2000) Biochemical and genetic evidence for three transmembrane domains in the class I holin, λ S. J Biol Chem 275:769–776

    Article  PubMed  Google Scholar 

  • Gründling A, Manson MD, Young R (2001) Holins kill without warning. Proc Natl Acad Sci U S A 98:9348–9352

    Article  PubMed  PubMed Central  Google Scholar 

  • Hadas H, Einav M, Fishov I, Zaritsky A (1997) Bacteriophage T4 development depends on the physiology of its host Escherichia coli. Microbiology 143:179–185

    Article  CAS  PubMed  Google Scholar 

  • Hagens S, Habel A, von Ahsen U, von Gabain A, Bläsi U (2004) Therapy of experimental Pseudomonas infections with a nonreplicating genetically modified phage. Antimicrob Agents Chemother 48:3817–3822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hinton DM (2010) Transcriptional control in the prereplicative phase of T4 development. Virol J 7:289

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hobbs Z, Abedon ST (2016) Diversity of phage infection types and associated terminology: the problem with 'Lytic or lysogenic'. FEMS Microbiol Lett 363:fnw047

    Article  PubMed  CAS  Google Scholar 

  • Hyman P (2019) Phages for phage therapy: isolation, characterization, and host range breadth. Pharmaceuticals (Basel) 12:35. https://pubmed.ncbi.nlm.nih.gov/30862020/

  • Hyman P, Abedon ST (2009) Practical methods for determining phage growth parameters. Methods Mol Biol 501:175–202

    Article  CAS  PubMed  Google Scholar 

  • Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248

    Article  CAS  PubMed  Google Scholar 

  • Kannoly S, Gao T, Dey S, Wang IN, Singh A, Dennehy JJ (2020) Optimum threshold minimizes noise in timing of intracellular events. iScience 23:101186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kao SH, McClain WH (1980) Roles of T4 gene 5 and gene s products in cell lysis. J Virol 34:104–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kongari R, Rajaure M, Cahill J, Rasche E, Mijalis E, Berry J, Young R (2018) Phage spanins: diversity, topological dynamics and gene convergence. BMC Bioinf 19:326

    Article  CAS  Google Scholar 

  • Kropinski AM (2018) Practical advice on the one-step growth curve. Methods Mol Biol 1681:41–47

    Article  CAS  PubMed  Google Scholar 

  • Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327

    Article  CAS  PubMed  Google Scholar 

  • Los M, Wegrzyn G (2012) Pseudolysogeny. Adv Virus Res 82:339–349

    Article  CAS  PubMed  Google Scholar 

  • Lwoff A (1953) Lysogeny. Bacteriol Rev 17:269–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maniloff J, Dybvig K (2006) Mycoplasma phages. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford, pp 636–652

    Google Scholar 

  • Maniloff J, Haberer K, Gourlay RN, Das J, Cole R (1982) Mycoplasma viruses. Intervirology 18:177–188

    Article  CAS  PubMed  Google Scholar 

  • Miller RV, Day M (2008) Contribution of lysogeny, pseudolysogeny, and starvation to phage ecology. In: Abedon ST (ed) Bacteriophage ecology. Cambridge University Press, Cambridge, UK, pp 114–143

    Chapter  Google Scholar 

  • Molineux IJ (2006) The T7 group. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford

    Google Scholar 

  • Moradpour Z, Sepehrizadeh Z, Rahbarizadeh F, Ghasemian A, Yazdi MT, Shahverdi AR (2009) Genetically engineered phage harbouring the lethal catabolite gene activator protein gene with an inducer-independent promoter for biocontrol of Escherichia coli. FEMS Microbiol Lett 296:67–71

    Article  CAS  PubMed  Google Scholar 

  • Mosig G, Eiserling F (2006) T4 and related phages: structure and development. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford

    Google Scholar 

  • Narajczyk M, Baranska S, Wegrzyn A, Wegrzyn G (2007) Switch from theta to sigma replication of bacteriophage lambda DNA: factors involved in the process and a model for its regulation. Mol Gen Genomics 278:65–74

    Article  CAS  Google Scholar 

  • Ngo-Duc TT, Alibay Z, Plank JM, Cheeney JE, Haberer ED (2020) Gold-decorated M13 I-forms and S-forms for targeted photothermal lysis of bacteria. ACS Appl Mater Interfaces 12:126–134

    Article  CAS  PubMed  Google Scholar 

  • Peng H, Borg RE, Dow LP, Pruitt BL, Chen IA (2020) Controlled phage therapy by photothermal ablation of specific bacterial species using gold nanorods targeted by chimeric phages. Proc Natl Acad Sci U S A 117:1951–1961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raj A, van Oudenaarden A (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216–226

    Google Scholar 

  • Ross A, Ward S, Hyman P (2016) More is better: selecting for broad host range bacteriophages. Front Microbiol 7:1352

    Article  PubMed  PubMed Central  Google Scholar 

  • Russel M, Model P (2006) Filamentous bacteriophages. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford, pp 146–160

    Google Scholar 

  • Samson JE, Magadan AH, Sabri M, Moineau S (2013) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11:675–687

    Article  CAS  PubMed  Google Scholar 

  • Shao Y, Wang I-N (2008) Bacteriophage adsorption rate and optimal lysis time. Genetics 180:471–482

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh A, Dennehy JJ (2014) Stochastic holin expression can account for lysis time variation in the bacteriophage lambda. J R Soc Interface 11:20140140

    Article  PubMed  PubMed Central  Google Scholar 

  • Stern A, Sorek R (2011) The phage-host arms race: shaping the evolution of microbes. Bioessays 33:43–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran TA, Struck DK, Young R (2005) Periplasmic domains define holin-antiholin interactions in T4 lysis inhibition. J Bacteriol 187:6631–6640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang I-N (2006) Lysis timing and bacteriophage fitness. Genetics 172:17–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang I-N, Deaton J, Young R (2003) Sizing the holin lesion with an endolysin-β-galactosidase fusion. J Bacteriol 185:779–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang I-N, Dykhuizen DE, Slobodkin LB (1996) The evolution of phage lysis timing. Evol Ecol 10:545–558

    Article  Google Scholar 

  • Wang I-N, Smith DL, Young R (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799–825

    Article  CAS  PubMed  Google Scholar 

  • Wegrzyn G, Wegrzyn A (2005) Genetic switches during bacteriophage lambda development. Prog Nucleic Acid Res Mol Biol 79:1–48

    Article  CAS  PubMed  Google Scholar 

  • Weinbauer MG, Wilehelm SW, Suttle CA, Garza DR (1997) Photoreactivation compensates for UV damage and restores infectivity to natural marine virus communities. Appl Environ Microbiol 63:2200–2205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yacoby I, Benhar I (2008) Targeted filamentous bacteriophages as therapeutic agents. Expert Opin Drug Deliv 5:321–329

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Ma Y, Wang Y, Yang H, Shen W, Chen X (2014) Transcription regulation mechanisms of bacteriophages: recent advances and future prospects. Bioengineered 5:300–304

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin J (1991) A quantifiable phenotype of viral propagation. Biochem Biophys Res Com 174:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • Young R (1992) Bacteriophage lysis: mechanisms and regulation. Microbiol Rev 56:430–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young R (2005) Phage lysis. In: Waldor MK, Friedman DI, Adhya SL (eds) Phages: their role in pathogenesis and biotechnology. ASM Press, Washington, DC, pp 92–127

    Google Scholar 

  • Young R (2013) Phage lysis: do we have the hole story yet? Curr Opin Microbiol 16:790–797

    Article  CAS  PubMed  Google Scholar 

  • Young R (2014) Phage lysis: three steps, three choices, one outcome. J Microbiol 52:243–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young R, Wang I-N (2006) Phage lysis. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford, pp 104–125

    Google Scholar 

  • Young R, Wang I-N, Roof WD (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8:120–128

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

JJD acknowledges financial support from the National Institutes of Health NIGMS through grant number 1R01GM124446-01.

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Authors and Affiliations

  1. Biology Department, Queens College and The Graduate Center of the City University of New York, New York, NY, USA

    John J. Dennehy

  2. Department of Microbiology, The Ohio State University, Mansfield, OH, USA

    Stephen T. Abedon

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  1. John J. Dennehy
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  2. Stephen T. Abedon
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Correspondence to Stephen T. Abedon .

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Editors and Affiliations

  1. Evolution Biotechnologies, Milton Keynes, UK

    David R. Harper

  2. Dept. of Microbiology, The Ohio State University Dept. of Microbiology, Mansfield, OH, USA

    Stephen T. Abedon

  3. GeneWEAVE Biosciences, Roche Molecular Systems GeneWEAVE Biosciences, Los Gatos, AR, USA

    Benjamin H. Burrowes

  4. Evolution Biotechnologies, Milton Keynes, UK

    Malcolm L. McConville

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Dennehy, J.J., Abedon, S.T. (2020). Phage Infection and Lysis. In: Harper, D.R., Abedon, S.T., Burrowes, B.H., McConville, M.L. (eds) Bacteriophages. Springer, Cham. https://doi.org/10.1007/978-3-319-40598-8_53-1

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  • DOI: https://doi.org/10.1007/978-3-319-40598-8_53-1

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