Abstract
Bacteria and phages have co-existed for several billions of years. The direct observation of their relationship, and the evidence that phages cause bacterial lysis and death, has led researchers to believe that phages and bacteria are natural enemies and that phages can be applied as antimicrobial agents. However, phages are also known to provide various benefits for their bacterial hosts, and on many occasions the phage-host interaction resembles a symbiotic relationship. In this chapter, we evaluate findings in different bacterial genera and their associated phages to assess if phages should be considered as bacterial parasites or symbiotic organisms.
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References
Adams MH (1959) Bacteriophages. In, Bacteriophages, p 592
Ahmad AA, Stulberg MJ, Huang Q (2017) Prophage Rs551 and its repressor gene orf14 reduce virulence and increase competitive fitness of its Ralstonia solanacearum carrier strain UW551. Front Microbiol 8:2480. https://doi.org/10.3389/fmicb.2017.02480
Allué-Guardia A, MartÃnez-Castillo A, Muniesa M (2014) Persistence of infectious Shiga toxin-encoding bacteriophages after disinfection treatments. Appl Environ Microbiol 80:2142–2149. https://doi.org/10.1128/AEM.04006-13
Balcazar JL (2014) Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog 10:e1004219. https://doi.org/10.1371/journal.ppat.1004219
Barrangou R, Fremaux C, Deveau H et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712. https://doi.org/10.1126/science.1138140
Bednarz M, Halliday JA, Herman C, Golding I (2014) Revisiting bistability in the lysis/lysogeny circuit of bacteriophage lambda. PLoS One 9:e100876. https://doi.org/10.1371/journal.pone.0100876
Bertozzi Silva J, Storms Z, Sauvageau D (2016) Host receptors for bacteriophage adsorption. FEMS Microbiol Lett 363:fnw002. https://doi.org/10.1093/femsle/fnw002
Betley MJ, Mekalanos JJ (1985) Staphylococcal enterotoxin a is encoded by phage. Science (80- ) 229:185–187. https://doi.org/10.1126/science.3160112
Beumer A, Robinson JB (2005) A broad-host-range, generalized transducing phage (SN-T) acquires 16S rRNA genes from different genera of bacteria. Appl Environ Microbiol 71:8301–8304. https://doi.org/10.1128/AEM.71.12.8301-8304.2005
Bielaszewska M, Prager R, Zhang W et al (2006) Chromosomal dynamism in progeny of outbreak-related sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM. Appl Environ Microbiol 72:1900–1909. https://doi.org/10.1128/AEM.72.3.1900-1909.2006
Bondy-Denomy J, Davidson AR (2014) When a virus is not a parasite: the beneficial effects of prophages on bacterial fitness. J Microbiol 52:235–242. https://doi.org/10.1007/s12275-014-4083-3
Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR (2012) Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493:429–432. https://doi.org/10.1038/nature11723
Bondy-Denomy J, Qian J, Westra ER et al (2016) Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10:2854–2866. https://doi.org/10.1038/ismej.2016.79
Borges AL, Zhang JY, Rollins MF et al (2018) Bacteriophage cooperation suppresses CRISPR-Cas3 and Cas9 immunity. Cell 174:917–925.e10. https://doi.org/10.1016/j.cell.2018.06.013
Brown-Jaque M, Calero-Cáceres W, Espinal P et al (2018) Antibiotic resistance genes in phage particles isolated from human feces and induced from clinical bacterial isolates. Int J Antimicrob Agents 51:434–442
Brzuszkiewicz E, Thürmer A, Schuldes J et al (2011) Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: Entero-aggregative-haemorrhagic Escherichia coli (EAHEC). Arch Microbiol 193:883–891. https://doi.org/10.1007/s00203-011-0725-6
Calero-Cáceres W, Muniesa M (2016) Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater. Water Res 95:11–18. https://doi.org/10.1016/j.watres.2016.03.006
Casjens S (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49:277–300
Chan BK, Sistrom M, Wertz JE et al (2016) Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci Rep 6:26717. https://doi.org/10.1038/srep26717
Chen J, Ram G, Penadés JR et al (2015) Pathogenicity Island-directed transfer of unlinked chromosomal virulence genes. Mol Cell 57:138–149. https://doi.org/10.1016/j.molcel.2014.11.011
Chen J, Quiles-Puchalt N, Chiang YN et al (2018) Genome hypermobility by lateral transduction. Science (80- ) 362:207–212. https://doi.org/10.1126/science.aat5867
Chung I-Y, Jang H-J, Bae H-W, Cho Y-H (2014) A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. Proc Natl Acad Sci 111:11503–11508. https://doi.org/10.1073/pnas.1403537111
Colomer-Lluch M, Imamovic L, Jofre J, Muniesa M (2011a) Bacteriophages carrying antibiotic resistance genes in fecal waste from cattle, pigs, and poultry. Antimicrob Agents Chemother 55:4908–4911. https://doi.org/10.1128/AAC.00535-11
Colomer-Lluch M, Jofre J, Muniesa M (2011b) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6:e17549
Crispim JS, Dias RS, Vidigal PMP et al (2018) Screening and characterization of prophages in Desulfovibrio genomes. Sci Rep 8:9273. https://doi.org/10.1038/s41598-018-27423-z
Delmar JA, Su C-C, Yu EW (2014) Bacterial Multidrug Efflux Transporters. Annu Rev Biophys 43:93–117. https://doi.org/10.1146/annurev-biophys-051013-022855
Diene SM, Corvaglia AR, François P et al (2017) Prophages and adaptation of Staphylococcus aureus ST398 to the human clinic. BMC Genomics 18:133. https://doi.org/10.1186/s12864-017-3516-x
Doménech-Sánchez A, MartÃnez-MartÃnez L, Hernández-Allés S et al (2003) Role of Klebsiella pneumoniae OmpK35 porin in antimicrobial resistance. Antimicrob Agents Chemother 47:3332–3335
Doolittle WF (2002) Lateral DNA transfer: mechanisms and consequences. CSHL Press
Du D, van Veen HW, Luisi BF (2015) Assembly and operation of bacterial tripartite multidrug efflux pumps. Trends Microbiol 23:311–319. https://doi.org/10.1016/j.tim.2015.01.010
Dupuis M-È, Villion M, Magadán AH, Moineau S (2013) CRISPR-Cas and restriction–modification systems are compatible and increase phage resistance. Nat Commun 4:2087. https://doi.org/10.1038/ncomms3087
Durán AE, Muniesa M, Méndez X et al (2002) Removal and inactivation of indicator bacteriophages in fresh waters. J Appl Microbiol 92:338–347
Eklund MW, Poysky FT (1974) Interconversion of type C and D strains of Clostridium botulinum by specific bacteriophages. Appl Microbiol 27:251–258
Eklund MW, Poysky FT, Reed SM (1972) Bacteriophage and the toxigenicity of clostridium botulinum type D. Nat New Biol 235:16–17. https://doi.org/10.1038/newbio235016a0
Erez Z, Steinberger-Levy I, Shamir M et al (2017) Communication between viruses guides lysis–lysogeny decisions. Nature 541:488–493. https://doi.org/10.1038/nature21049
Evans TJ, Crow MA, Williamson NR et al (2010) Characterization of a broad-host-range flagellum-dependent phage that mediates high-efficiency generalized transduction in, and between, Serratia and Pantoea. Microbiology 156:240–247. https://doi.org/10.1099/mic.0.032797-0
Feiner R, Argov T, Rabinovich L et al (2015) A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 13:641–650. https://doi.org/10.1038/nrmicro3527
Fogg PCM, Saunders JR, McCarthy AJ, Allison HE (2012) Cumulative effect of prophage burden on Shiga toxin production in Escherichia coli. Microbiology 158:488–497. https://doi.org/10.1099/mic.0.054981-0
Fortier L-C, Sekulovic O (2013) Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354–365. https://doi.org/10.4161/viru.24498
GarcÃa-Aljaro C, Ballesté E, Muniesa M (2017) Beyond the canonical strategies of horizontal gene transfer in prokaryotes. Curr Opin Microbiol 38:95–105. https://doi.org/10.1016/j.mib.2017.04.011
Gómez-Gómez C, Blanco-Picazo P, Brown-Jaque M et al (2019) Infectious phage particles packaging antibiotic resistance genes found in meat products and chicken feces. Sci Rep 9:13281. https://doi.org/10.1038/s41598-019-49898-0
Grad YH, Godfrey P, Cerquiera GC et al (2013) Comparative genomics of recent Shiga toxin-producing Escherichia coli O104:H4: short-term evolution of an emerging pathogen. MBio 4:e00452–e00412. https://doi.org/10.1128/mBio.00452-12
Graveland H, Duim B, van Duijkeren E et al (2011) Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol 301:630–634. https://doi.org/10.1016/j.ijmm.2011.09.004
Groth AC, Calos MP (2004) Phage integrases: biology and applications. J Mol Biol 335:667–678
Hayashi T, Baba T, Matsumoto H, Terawaki Y (1990) Phage-conversion of cytotoxin production in Pseudomonas aeruginosa. Mol Microbiol 4:1703–1709. https://doi.org/10.1111/j.1365-2958.1990.tb00547.x
Herold S, Siebert J, Huber A, Schmidt H (2005) Global expression of Prophage genes in Escherichia coli O157:H7 strain EDL933 in response to Norfloxacin. Antimicrob Agents Chemother 49:931–944. https://doi.org/10.1128/AAC.49.3.931-944.2005
Holt GS, Lodge JK, McCarthy AJ et al (2017) Shigatoxin encoding bacteriophage φ24B modulates bacterial metabolism to raise antimicrobial tolerance. Sci Rep 7:40424. https://doi.org/10.1038/srep40424
Hossain MJ, Rahman KS, Terhune JS, Liles MR (2012) An outer membrane porin protein modulates phage susceptibility in Edwardsiella ictaluri. Microbiology 158:474–487. https://doi.org/10.1099/mic.0.054866-0
Imamovic L, Ballesté E, MartÃnez-Castillo A et al (2016) Heterogeneity in phage induction enables the survival of the lysogenic population. Environ Microbiol 18:957–969. https://doi.org/10.1111/1462-2920.13151
Inoue K, Iida H (1970) Conversion of Toxigenicity in Clostridium botulinum type C. Jpn J Microbiol 14:87–89. https://doi.org/10.1111/j.1348-0421.1970.tb00495.x
Jensen EC, Schrader HS, Rieland B et al (1998) Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa. Appl Environ Microbiol 64:575–580
Johnson TA, Looft T, Severin AJ et al (2017) The in-feed antibiotic carbadox induces phage gene transcription in the swine gut microbiome. MBio 8. https://doi.org/10.1128/mBio.00709-17
Jończyk E, Kłak M, Międzybrodzki R, Górski A (2011) The influence of external factors on bacteriophages--review. Folia Microbiol (Praha) 56:191–200. https://doi.org/10.1007/s12223-011-0039-8
Kaneko J, Kimura T, Kawakami Y et al (1997) Panton-valentine leukocidin genes in a phage-like particle isolated from mitomycin C-treated Staphylococcus aureus V8 (ATCC 49775). Biosci Biotechnol Biochem 61:1960–1962
Karaolis DKR, Somara S, Maneval DR et al (1999) A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399:375–379. https://doi.org/10.1038/20715
Kimmitt PT, Harwood CR, Barer MR (2000) Toxin gene expression by Shiga toxin-producing Escherichia coli: the role of antibiotics and the bacterial SOS response. Emerg Infect Dis 6:458–465
Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327. https://doi.org/10.1038/nrmicro2315
Lang AS, Zhaxybayeva O, Beatty JT (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol 10:472–482. https://doi.org/10.1038/nrmicro2802
Larrañaga O, Brown-Jaque M, Quirós P et al (2018) Phage particles harboring antibiotic resistance genes in fresh-cut vegetables and agricultural soil. Environ Int 115:133–141. https://doi.org/10.1016/j.envint.2018.03.019
Lee HS, Sobsey MD (2011) Survival of prototype strains of somatic coliphage families in environmental waters and when exposed to UV low-pressure monochromatic radiation or heat. Water Res 45:3723–3734. https://doi.org/10.1016/j.watres.2011.04.024
Lindsay JA, Ruzin A, Ross HF et al (1998) The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29:527–543. https://doi.org/10.1046/j.1365-2958.1998.00947.x
Ma D, Cook DN, Hearst JE, Nikaido H (1994) Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol 2:489–493. https://doi.org/10.1016/0966-842X(94)90654-8
Mann NH, Cook A, Millard A et al (2003) Bacterial photosynthesis genes in a virus. Nature 424:741. https://doi.org/10.1038/424741a
Marti E, Variatza E, Balcázar JL (2014) Bacteriophages as a reservoir of extended-spectrum β-lactamase and fluoroquinolone resistance genes in the environment. Clin Microbiol Infect 20:O456–O459. https://doi.org/10.1111/1469-0691.12446
Martinez JL, Sánchez MB, MartÃnez-Solano L et al (2009) Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol Rev 33:430–449. https://doi.org/10.1111/j.1574-6976.2008.00157.x
Menge C, Wieler LH, Schlapp T, Baljer G (1999) Shiga toxin 1 from Escherichia coli blocks activation and proliferation of bovine lymphocyte subpopulations in vitro. Infect Immun 67:2209–2217
Menge C, Stamm I, Van Diemen PM et al (2004) Phenotypic and functional characterization of intraepithelial lymphocytes in a bovine ligated intestinal loop model of enterohaemorrhagic Escherichia coli infection. J Med Microbiol 53:573–579. https://doi.org/10.1099/jmm.0.45530-0
Miller C, Thomsen LE, Gaggero C et al (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305:1629–1631. https://doi.org/10.1126/science.1101630
Moat AG, Foster JW, Spector MP (2003) Bacteriophage genetics. In: Microbial physiology. Fourth Edi. John Wiley & Sons, Inc., Hoboken, NJ, USA, pp 239–276
Mocé-llivina L, Muniesa M, Pimenta-vale H et al (2003) Survival of Bacterial Indicator Species and Bacteriophages after Thermal Treatment of Sludge and Sewage. Appl Environ Microbiol 69:1452–1456. https://doi.org/10.1128/AEM.69.3.1452
Mojica FJM, Rodriguez-Valera F (2016) The discovery of CRISPR in archaea and bacteria. FEBS J 283:3162–3169. https://doi.org/10.1111/febs.13766
Moon BY, Park JY, Hwang SY et al (2015) Phage-mediated horizontal transfer of a Staphylococcus aureus virulence-associated genomic island. Sci Rep 5:9784. https://doi.org/10.1038/srep09784
Morabito S (2014) Pathogenic Escherichia coli: molecular and cellular microbiology. Horizon Press, Linton
Moussay E, Stamm I, Taubert A et al (2006) Escherichia coli Shiga toxin 1 enhances il-4 transcripts in bovine ileal intraepithelial lymphocytes. Vet Immunol Immunopathol 113:367–382. https://doi.org/10.1016/j.vetimm.2006.06.007
Müller MG, Ing JY, Cheng MK-W et al (2013) Identification of a phage-encoded Ig-binding protein from invasive Neisseria meningitidis. J Immunol 191:3287–3296. https://doi.org/10.4049/jimmunol.1301153
Muniesa M, Lucena F, Jofre J (1999) Comparative survival of free Shiga toxin 2-encoding Phages and. Society 65:5615–5618
Muniesa M, De Simon M, Prats G et al (2003) Shiga toxin 2-converting bacteriophages associated with clonal variability in Escherichia coli O157:H7 strains of human origin isolated from a single outbreak. Infect Immun 71. https://doi.org/10.1128/IAI.71.8.4554-4562.2003
Muniesa M, Hammerl JA, Hertwig S et al (2012) Shiga toxin-producing Escherichia coli O104:H4: a new challenge for microbiology. Appl Environ Microbiol 78:4065–4073. https://doi.org/10.1128/AEM.00217-12
Muniesa M, Allué-Guardia A, MartÃnez-Castillo A (2013) Bacteriophage-driven emergence of novel pathogens. Futur Virol 8:323–325. https://doi.org/10.2217/fvl.13.13
Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656
Oppenheim AB, Kobiler O, Stavans J et al (2005) Switches in bacteriophage lambda development. Annu Rev Genet 39:409–429. https://doi.org/10.1146/annurev.genet.39.073003.113656
Parsons EI, Frobisher M (1951) Effect of bacteriophage on virulence of Corynebacterium diphtheriae. Exp Biol Med 78:746–747. https://doi.org/10.3181/00379727-78-19204
Paul JH (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2:579–589. https://doi.org/10.1038/ismej.2008.35
Penades JR, Chen J, Quiles-Puchalt N et al (2015) Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23:171–178. https://doi.org/10.1016/j.mib.2014.11.019
Perez-Rodriguez R, Haitjema C, Huang Q et al (2011) Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli. Mol Microbiol 79:584–599. https://doi.org/10.1111/j.1365-2958.2010.07482.x
Poole K (2002) Outer membranes and efflux: the path to multidrug resistance in gram-negative bacteria. Curr Pharm Biotechnol 3:77–98
Quirós P, Colomer-Lluch M, MartÃnez-Castillo A et al (2014) Antibiotic resistance genes in the bacteriophage DNA fraction of human fecal samples. Antimicrob Agents Chemother 58:606–609. https://doi.org/10.1128/AAC.01684-13
Rajala-Mustonen RL, Heinonen-Tanski H (1994) Sensitivity of host strains and host range of coliphages isolated from finnish and nicaraguan wastewater. Water Res 28:1811–1815. https://doi.org/10.1016/0043-1354(94)90254-2
Ricci V, Piddock LJV (2010) Exploiting the role of TolC in pathogenicity: identification of a bacteriophage for eradication of Salmonella Serovars from poultry. Appl Environ Microbiol 76:1704–1706. https://doi.org/10.1128/AEM.02681-09
Riede I, Eschbach ML (1986) Evidence that TraT interacts with OmpA of Escherichia Coli. FEBS Lett 205(2):241–5. https://doi.org/10.1016/0014-5793(86)80905-x
Ruzin A, Lindsay J, Novick RP (2001) Molecular genetics of SaPI1 - a mobile pathogenicity island in Ataphylococcus aureus. Mol Microbiol 41:365–377. https://doi.org/10.1046/j.1365-2958.2001.02488.x
Samson JE, Magadán AH, Sabri M, Moineau S (2013) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11:675–687. https://doi.org/10.1038/nrmicro3096
Seed KD, Lazinski DW, Calderwood SB, Camilli A (2013) A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489–491. https://doi.org/10.1038/nature11927
Selva L, Viana D, Regev-Yochay G et al (2009) Killing niche competitors by remote-control bacteriophage induction. PNAS 106:1234–1238
Serra-Moreno R, Jofre J, Muniesa M (2008) The CI repressors of Shiga toxin-converting prophages are involved in coinfection of Escherichia coli strains, which causes a down regulation in the production of Shiga toxin 2. J Bacteriol 190:4722–4735. https://doi.org/10.1128/JB.00069-08
Shaikh N, Tarr PI (2003) Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J Bacteriol 185:3596–3605
Shariat N, Timme RE, Pettengill JB et al (2015) Characterization and evolution of Salmonella CRISPR-Cas systems. Microbiology 161:374–386. https://doi.org/10.1099/mic.0.000005
Shestakov SV, Karbysheva EA (2015) The role of viruses in the evolution of cyanobacteria. Biol Bull Rev 5:527–537. https://doi.org/10.1134/s2079086415060079
Soutourina OA, Monot M, Boudry P et al (2013) Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLoS Genet 9:e1003493. https://doi.org/10.1371/journal.pgen.1003493
Souza KA, Ginoza HS, Haight RD (1972) Isolation of a polyvalent bacteriophage for Escherichia coli, Klebsiella pneumoniae and Aerobacter Aerogenes. J Virol 9:851–856
Stamm I, Mohr M, Bridger PS et al (2008) Epithelial and mesenchymal cells in the bovine colonic mucosa differ in their responsiveness to Escherichia coli Shiga toxin 1. Infect Immun 76:5381–5391. https://doi.org/10.1128/IAI.00553-08
Sternberg N, Coulby JN (1990) Cleavage of the bacteriophage P1 packaging site (pac) is regulated by adenine methylation. PNAS 87:8070–8074. https://doi.org/10.1016/0378-1119(88)90287-9
Subirats J, Sà nchez-Melsió A, Borrego CM et al (2016) Metagenomic analysis reveals that bacteriophages are reservoirs of antibiotic resistance genes. Int J Antimicrob Agents 48:163–167. https://doi.org/10.1016/j.ijantimicag.2016.04.028
Sullivan MB, Lindell D, Lee JA et al (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4:1344–1357. https://doi.org/10.1371/journal.pbio.0040234
Sweere JM, Van Belleghem JD, Ishak H et al (2019) Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science (80- ) 363:eaat9691. https://doi.org/10.1126/science.aat9691
Thierauf A, Perez G, Maloy AS (2009) Generalized transduction. Methods Mol Biol 501:267–286. https://doi.org/10.1007/978-1-60327-164-6_23
Touchon M, Moura de Sousa JA, Rocha EP (2017) Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Curr Opin Microbiol 38:66–73
Tree JJ, Granneman S, McAteer SP et al (2014) Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli. Mol Cell 55:199–213. https://doi.org/10.1016/j.molcel.2014.05.006
Ubeda C, Maiques E, Knecht E et al (2005) Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56:836–844. https://doi.org/10.1111/j.1365-2958.2005.04584.x
Utter B, Deutsch DR, Schuch R et al (2014) Beyond the chromosome: the prevalence of unique extra-chromosomal bacteriophages with integrated virulence genes in pathogenic Staphylococcus aureus. PLoS One 9:e100502. https://doi.org/10.1371/journal.pone.0100502
Verkade E, Bergmans AMC, Budding AE et al (2012) Recent emergence of Staphylococcus aureus clonal complex 398 in human blood cultures. PLoS One 7:e41855. https://doi.org/10.1371/journal.pone.0041855
Wagner PL, Waldor MK (2002) Bacteriophage control of bacterial virulence. Infect Immun 70:3985–3993
Waldor MK, Friedman DI (2005) Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol 8:459–465. https://doi.org/10.1016/j.mib.2005.06.001
Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914
Watson BNJ, Staals RHJ, Fineran PC (2018) CRISPR-Cas-mediated phage resistance enhances horizontal gene transfer by transduction. MBio 9. https://doi.org/10.1128/mBio.02406-17
Xia G, Wolz C (2014) Phages of Staphylococcus aureus and their impact on host evolution. Infect Genet Evol 21:593–601. https://doi.org/10.1016/j.meegid.2013.04.022
Yamaguchi T, Hayashi T, Takami H et al (2000) Phage conversion of exfoliative toxin a production in Staphylococcus aureus. Mol Microbiol 38:694–705. https://doi.org/10.1046/j.1365-2958.2000.02169.x
Yu P, Mathieu J, Li M et al (2016) Isolation of polyvalent bacteriophages by sequential multiple-host approaches. Appl Environ Microbiol 82:808–815. https://doi.org/10.1128/AEM.02382-15
Acknowledgements
This work was supported by the Ministerio de Ciencia e Innovación (AGL2016-75536-P). P. B-P has a grant from the Spanish Ministry of Economy, Industry and Competitiveness (BES-2017-081296). L. R.-R is supported by the Beatriu de Pinós postdoctoral program of the Government of Catalonia.
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RodrÃguez-Rubio, L., Blanco-Picazo, P., Muniesa, M. (2020). Are Phages Parasites or Symbionts of Bacteria?. In: Witzany, G. (eds) Biocommunication of Phages. Springer, Cham. https://doi.org/10.1007/978-3-030-45885-0_7
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