Skip to main content

The Role of Phage in the Adaptation of Bacteria to New Environmental Niches

Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)

Abstract

Bacteria and their viruses (bacteriophages or phages) have a complex relationship that is in constant flux. Studies in natural environments, and by manipulations of phages and bacteria in a laboratory setting, have demonstrated that phages can profoundly influence bacterial populations. Phages can alter the density of different bacteria by lytic infection, and the genetic makeup of bacteria can be altered by lysogeny or transduction. Phages are promiscuous mediators of genetic exchange and often carry genes capable of altering the phenotypes of their bacterial hosts. The genetic traits acquired from phages can influence adaptation of bacteria to an environment by providing enhanced or novel metabolic properties, resistance to other phages or protozoan predators, and acquisition of antibiotic resistance or new virulence traits. The improvement in sequencing technology that sparked the microbial metagenomic revolution has provided another tool for understanding the impact of phages on bacterial populations. Metagenomic analysis of virus populations (“viromics”) has provided insight into the surprising extent that phages modulate the bacterial genome. While the benefit to the phages for transferring novel properties to its host is often poorly understood, this relationship clearly provides a selective advantage because these properties are maintained in many environments and including otherwise adverse conditions for the bacterial host. In this chapter, we will discuss how phages influence the fitness of bacteria in particular environmental niches.

Keywords

  • Bacterial Host
  • Phage Predation
  • Niche Adaptation
  • Antibiotic Resistance Genes
  • Exotoxin Genes

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-319-69078-0_11
  • Chapter length: 40 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   219.00
Price excludes VAT (USA)
  • ISBN: 978-3-319-69078-0
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   279.99
Price excludes VAT (USA)
Hardcover Book
USD   279.99
Price excludes VAT (USA)
Fig. 11.1
Fig. 11.2
Fig. 11.3

References

  • Al-Attar S, Westra ER, van der Oost J, Brouns SJJ (2011) Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes. Biol Chem 392:277–289

    CAS  PubMed  CrossRef  Google Scholar 

  • Allue-Guardia A, Garcia-Aljaro C, Muniesa M (2011) Bacteriophage-encoding cytolethal distending toxin type v gene induced from nonclinical Escherichia coli isolates. Infect Immun 79:3262–3272

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Allue-Guardia A, Martinez-Castillo A, Muniesa M (2014) Persistence of infectious shiga toxin-encoding bacteriophages after disinfection treatments. Appl Environ Microbiol 80:2142–2149

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Altmann M, Wadl M, Altmann D, Benzler J, Eckmanns T, Krause G, Spode A, an der Heiden M (2011) Timeliness of surveillance during outbreak of shiga toxin-producing Escherichia coli infection, Germany, 2011. Emerg Infect Dis 17:1906–1909

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Anantharaman A, Duhaime MB, Breier JA, Wendt KA, Toner BM, Dick GJ (2014) Sulfur oxidation genes in diverse deep-sea viruses. Science 344(6185):757–760. https://doi.org/10.1126/science.1252229

    CAS  CrossRef  PubMed  Google Scholar 

  • Anderson RE, Sogin ML, Baross JA, Uversky VN (2014) Evolutionary strategies of viruses, bacteria and archaea in hydrothermal vent ecosystems revealed through metagenomics. PLoS One 9(10):e109696

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Arnold JW, Koudelka GB (2014) The Trojan Horse of the microbiological arms race: phage-encoded toxins as a defence against eukaryotic predators. Environ Microbiol 16(2):454–466

    CAS  PubMed  CrossRef  Google Scholar 

  • Aziz RK, Edwards RA, Taylor WW, Low DE, McGeer A, Kotb M (2005) Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J Bacteriol 187(10):3311–3318

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Bao YJ, Liang Z, Mayfield JA, Donahue DL, Carothers KE, Lee SW, Ploplis VA, Castellino FJ (2016) Genomic characterization of a pattern D Streptococcus pyogenes emm53 isolate reveals a genetic rationale for invasive skin tropicity. J Bacteriol 198:1712–1724

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Barondess J, Beckwith J (1990) A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature 346:871–874

    CAS  PubMed  CrossRef  Google Scholar 

  • Baugher JL, Durmaz E, Klaenhammer TR (2014) Spontaneously induced prophages in Lactobacillus gasseri contribute to horizontal gene transfer. Appl Environ Microbiol 80(11):3508–3517. https://doi.org/10.1128/aem.04092-13

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Benveniste R, Davies J (1973) Mechanisms of antibiotic resistance in bacteria. Annu Rev Biochem 42(1):471–506

    CAS  PubMed  CrossRef  Google Scholar 

  • Betley M, Mekalanos J (1985) Staphylococcal enterotoxin A is encoded by phage. Science 229(4709):185–187

    CAS  PubMed  CrossRef  Google Scholar 

  • Beutin L, Hammerl JA, Reetz J, Strauch E (2013) Shiga toxin-producing Escherichia coli strains from cattle as a source of the Stx2a bacteriophages present in enteroaggregative Escherichia coli O104:H4 strains. Int J Med Microbiol 303(8):595–602. https://doi.org/10.1016/j.ijmm.2013.08.001

    CAS  CrossRef  PubMed  Google Scholar 

  • Bonanno L, Petit MA, Loukiadis E, Michel V, Auvraya F (2016) Heterogeneity in induction level, infection ability, and morphology of shiga toxin-encoding phages (stx phages) from dairy and human shiga toxin-producing Escherichia coli O26:H11 Isolates. Appl Environ Microbiol 82:2177–2186

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Bondy-Denomy J, Davidson AR (2014) When a virus is not a parasite: the beneficial effects of prophages on bacterial fitness. J Microbiol 52(3):235–242

    CAS  PubMed  CrossRef  Google Scholar 

  • Boyd EF (2012) Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. In: Lobocka M, Szybalski WT (eds) Advances in virus research: Bacteriophages, Pt A, vol 82. Elsevier Academic Press, San Diego, pp 91–118. https://doi.org/10.1016/b978-0-12-394621-8.00014-5

    CrossRef  Google Scholar 

  • Boyd E, Waldor M (1999) Alternative mechanism of cholera toxin acquisition by Vibrio cholerae: generalized transduction of CTX phi by bacteriophage CP-T1. Infect Immun 67(11):5898–5905

    CAS  PubMed  Google Scholar 

  • Boyd EF, Waldor MK (2002) Evolutionary and functional analyses of variants of the toxin-coregulated pilus protein TcpA from toxigenic Vibrio cholerae nonO1/non-O139 serogroup isolates. Microbiology 148:1655–1666

    CAS  PubMed  CrossRef  Google Scholar 

  • Boyd E, Heilpern A, Waldor M (2000a) Molecular analyses of a putative CTX phi precursor and evidence for independent acquisition of distinct CTX phi s by toxigenic Vibrio cholerae. J Bacteriol 182(19):5530–5538

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Boyd EF, Moyer KE, Shi L, Waldor MK (2000b) Infectious CTX Phi, and the Vibrio pathogenicity island prophage in Vibrio mimicus: evidence for recent horizontal transfer between V. mimicus and V. cholerae. Infect Immun 68:1507–1513

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Brown CJ, Millstein J, Williams CJ, Wichman HA (2013) Selection affects genes involved in replication during long-term evolution in experimental populations of the bacteriophage φ. PLoS One 8(3):e60401. https://doi.org/10.1371/journal.pone.0060401

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Broecker F, Klumpp J, Moelling K (2016) Long-term microbiota and virome in a Zurich patient after fecal transplantation against Clostridium difficile infection. In: Moelling K (ed) Nutrition and the microbiome, vol 1372, pp 29–41

    Google Scholar 

  • Brüssow H, Canchaya C, Hardt W-D (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68(3):560–602

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Buchholz U, Bernard H, Werber D, Bohmer MM, Remschmidt C, Wilking H, Delere Y, an der Heiden M, Adlhoch C, Dreesman J, Ehlers J, Ethelberg S, Faber M, Frank C, Fricke G, Greiner M, Hohle M, Ivarsson S, Jark U, Kirchner M, Koch J, Krause G, Luber P, Rosner B, Stark K, Kuhne M (2011) German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 365:1763–1770

    CAS  PubMed  CrossRef  Google Scholar 

  • Buckling A, Brockhurst M (2012) Bacteria–virus coevolution. In: Soyer O (ed) Evolutionary systems biology. Advances in experimental medicine and biology, vol 751. Springer, New York

    Google Scholar 

  • Buckling A, Hodgson DJ (2007) Short-term rates of parasite evolution predict the evolution of host diversity. J Evol Biol 20(5):1682–1688. https://doi.org/10.1111/j.1420-9101.2007.01402.x

    CAS  CrossRef  PubMed  Google Scholar 

  • Buckling A, Rainey PB (2003) The role of parasites in sympatric and allopatric host diversification. Nature 421(6920):294–294. https://doi.org/10.1038/nature01349

    CAS  CrossRef  Google Scholar 

  • Buckling A, Wei Y, Massey RC, Brockhurst MA, Hochberg ME (2006) Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc R Soc B Biol Sci 273(1582):45–49

    CrossRef  Google Scholar 

  • Burns N, James CE, Harrison E (2015) Polylysogeny magnifies competitiveness of a bacterial pathogen. Evol Appl 8(4):346–351

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Calderwood S, Auclair F, Donohue-RolfE A, Keusch G, Mekalanos J (1987) Nucleotide sequence of the shiga-like toxin genes of Escherichia coli. Proc Natl Acad Sci USA 84(13):4364–4368. https://doi.org/10.1073/pnas.84.13.4364

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Calendar R (2006) The Bacteriophages, 2nd ed. Edited by Richard Calendar and Stephen T. Abedon. Oxford University Press, Oxford

    Google Scholar 

  • Calero-Caceres 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

    CAS  CrossRef  PubMed  Google Scholar 

  • Campos J, Martinez E, Marrero K, Silva Y, Rodriguez BL, Suzarte E, Ledon T, Fando R (2003) Novel type of specialized transduction for CTXÂ or its satellite phage RS1 mediated by filamentous phage VGJÂ in Vibrio cholerae. J Bacteriol 185(24):7231–7240

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Casas V, Maloy SR (2011) Role of bacteriophage-encoded exotoxins in the evolution of bacterial pathogens. Future Microbiol 6(12):1461–1473

    CAS  PubMed  CrossRef  Google Scholar 

  • Casas V, Miyake J, Balsley H, Roark J, Telles S, Leeds S, Zurita I, Breitbart M, Bartlett D, Azam F, Rohwer F (2006) Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California. FEMS Microbiol Lett 261(1):141–149. https://doi.org/10.1111/j.1574-6968.2006.00345.x

    CAS  CrossRef  PubMed  Google Scholar 

  • Casas V, Magbanua J, Sobrepeña G, Kelley ST, Maloy SR (2010) Reservoir of bacterial exotoxin genes in the environment. Int J Microbiol 2010:754368. https://doi.org/10.1155/2010/754368

    CAS  CrossRef  PubMed  Google Scholar 

  • Casas V, Sobrepena G, Rodriguez-Mueller B, AhTye J, Maloy SR (2011) Bacteriophage-encoded shiga toxin gene in atypical bacterial host. Gut Pathogens 3:7

    CrossRef  CAS  Google Scholar 

  • Casjens SR, Thuman-Commike PA (2011) Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology 411(2):393–415

    CAS  PubMed  CrossRef  Google Scholar 

  • Chambers L, Yang Y, Littier H, Ray P, Zhang T, Pruden A, Strickland M, Katharine K, Mark Ibekwe A (2015) Metagenomic analysis of antibiotic resistance genes in dairy cow feces following therapeutic administration of third generation cephalosporin. PLoS One 10(8):e0133764

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38(3):1086–1108. https://doi.org/10.2134/jeq2008.0128

    CAS  CrossRef  PubMed  Google Scholar 

  • Chiura HX (1997) Generalized gene transfer by virus-like particles from marine bacteria. Aquat Microb Ecol 13(1):75–83. https://doi.org/10.3354/ame013075

    CrossRef  Google Scholar 

  • Chouikha I, Charrier L, Filali S, Derbise A, Carniel E (2010) Insights into the infective properties of YpfΦ, the Yersinia pestis filamentous phage. Virology 407(1):43–52

    CAS  PubMed  CrossRef  Google Scholar 

  • Choi S, Dunams D, Jiang SC (2010) Transfer of cholera toxin genes from O1 to non-O1/O139 strains by vibriophages from California coastal waters. J Appl Microbiol 108:1015–1022

    CAS  PubMed  CrossRef  Google Scholar 

  • Ciofu O, Hansen CR, Høiby N (2013) Respiratory bacterial infections in cystic fibrosis. Curr Opin Pulm Med 19(3):251–258

    PubMed  CrossRef  Google Scholar 

  • Cleary PP, LaPenta D, Vessela R, Lam H, Cue D (1998) A globally disseminated M1 subclone of Group A Streptococci differs from other subclones by 70 kilobases of prophage DNA and capacity for high-frequency intracellular invasion. Infect Immun 66:5592–5597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen SN, Miller CA (1970) Non-chromosomal antibiotic resistance in bacteria II: molecular nature of R-factors isolated from Proteus mirabilis and Escherichia coli. J Mol Biol 50:671–687

    CAS  PubMed  CrossRef  Google Scholar 

  • Cohen SN, Chang ACY, Hsu L (1972) Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69(8):2110–2114

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Coleman D, Sullivan D, Russell R, Arbuthnott J, Carey B, Pomeroy H (1989) Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of .beta.-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J Gen Microbiol 135:1679–1698

    CAS  PubMed  Google Scholar 

  • Colombo S, Arioli S, Guglielmetti S, Lunelli F, Mora D (2016) Virome-associated antibiotic-resistance genes in an experimental aquaculture facility. FEMS Microbiol Ecol 92(3). https://doi.org/10.1093/femsec/fiw003

    PubMed  CrossRef  CAS  Google Scholar 

  • 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(10):4908–4911

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Colomer-Lluch M, Jofre J, Muniesa M, Aziz R (2011b) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6(3):e17549

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Colomer-Lluch M, Jofre J, Muniesa M (2014) Quinolone resistance genes (qnrA and qnrS) in bacteriophage particles from wastewater samples and the effect of inducing agents on packaged antibiotic resistance genes. J Antimicrob Chemother 69(5):1265–1274. https://doi.org/10.1093/jac/dkt528

    CAS  CrossRef  PubMed  Google Scholar 

  • Cornick NA, Helgerson AF, Mai V, Ritchie JM, Acheson DWK (2006) In vivo transduction of an Stx-encoding phage in ruminants. Appl Environ Microbiol 72(7):5086–5088. https://doi.org/10.1128/aem.00157-06

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Costerton JW, Lam J, Lam K, Chan R (1983) The role of the microcolony mode of growth in the pathogenesis of Pseudomonas aeruginosa infections. Rev Infect Dis 5:s867–S873

    PubMed  CrossRef  Google Scholar 

  • Dammeyer T, Bagby S, Sullivan M, Chisholm S, Frankenberg-Dinkel N (2008) Efficient phage mediated pigment biosynthesis in oceanic cyanobacteria. Curr Biol 18(6):442–448

    CAS  PubMed  CrossRef  Google Scholar 

  • Das B, Pazhani GP, Sarkar A, Mukhopadhyay AK, Nair GB, Ramamurthy T (2016) Molecular evolution and functional divergence of Vibrio cholerae. Curr Opin Infect Dis 29:520–527

    CAS  PubMed  CrossRef  Google Scholar 

  • Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74(3):417–433

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Davis BM, Waldor MK (2003) Filamentous phages linked to virulence of Vibrio cholerae. Curr Opin Microbiol 6:35–42

    CAS  PubMed  CrossRef  Google Scholar 

  • Davis BM, Moyer KE, Boyd EF, Waldor MK (2000) CTX prophages in classical biotype Vibrio cholerae: Functional phage genes but dysfunctional phage genomes. J Bacteriol 182:6992–6998

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Derbise A (2014) Ypf Phi: a filamentous phage acquired by Yersinia pestis. Front Microbiol 5:701

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Diard M, Bakkeren E, Cornuault JK, Moor K, Hausmann A, Sellin ME, Loverdo C, Aertsen A, Ackermann M, De Paepe M, Slack E, Hardt WD (2017) Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355:1211–1215

    CAS  PubMed  CrossRef  Google Scholar 

  • Dumke R, Schroter-Bobsin U, Jacobs E, Roske I (2006) Detection of phages carrying the Shiga toxin 1 and 2 genes in waste water and river water samples. Lett Appl Microbiol 42:48–53

    CAS  PubMed  CrossRef  Google Scholar 

  • Dutilh BE, Thompson CC, Vicente ACP, Marin MA, Lee C, Silva GGZ, Schmieder R, Andrade BGN, Chimetto L, Cuevas D, Garza DR, Okeke IN, Aboderin AO, Spangler J, Ross T, Dinsdale EA, Thompson FL, Harkins TT, Edwards RA (2014) Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions. BMC Genomics 15:11

    CrossRef  CAS  Google Scholar 

  • Eklund M, Poysky F (1974) Interconversion of type C and D strains of Clostridium botulinum by specific bacteriophages. Appl Environ Microbiol 27:251–258

    CAS  Google Scholar 

  • Ernst RK, D’Argenio DA, Ichikawa JK, Bangera MG, Selgrade S, Burns JL, Hiatt P, McCoy K, Brittnacher M, Kas A, Spencer DH, Olson MV, Ramsey BW, Lory S, Miller SI (2003) Genome mosaicism is conserved but not unique in Pseudomonas aeruginosa isolates from the airways of young children with cystic fibrosis. Environ Microbiol 5(12):1341–1349

    CAS  PubMed  CrossRef  Google Scholar 

  • Fan X, Li Y, He R, Li Q, He W (2016) Comparative analysis of prophage-like elements in Helicobacter sp genomes. PeerJ 4:e2012

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Fancello L, Desnues C, Raoult D, Rolain JM (2011) Bacteriophages and diffusion of genes encoding antimicrobial resistance in cystic fibrosis sputum microbiota. J Antimicrob Chemother 66(11):2448–2454

    CAS  PubMed  CrossRef  Google Scholar 

  • Faruque SM, Asadulghani, Rahman MM, Waldor MK, Sack DA (2000) Sunlight-induced propagation of the lysogenic phage encoding cholera toxin. Infect Immun 68(8):4795–4801. https://doi.org/10.1128/iai.68.8.4795-4801.2000

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Gonzalez E, Backert S (2014) DNA transfer in the gastric pathogen Helicobacter pylori. J Gastroenterol 49:594–604

    CAS  PubMed  CrossRef  Google Scholar 

  • Fineran PC, Gerritzen MJH, Suarez-Diez M, Kunne T, Boekhorst J, van Hijum S, Staals RHJ, Brouns SJJ (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc Natl Acad Sci USA 111:e1629–E1638

    CAS  PubMed  CrossRef  PubMed Central  Google Scholar 

  • Focazio MJ, Kolpin DW, Barnes KK, Furlong ET, Meyer MT, Zaugg SD, Barber LB, Thurman ME (2008) A national reconnaissance for pharmaceuticals and other organic wastewater contaminants in the United States II: Untreated drinking water sources. Sci Total Environ 402(2–3):201–216. https://doi.org/10.1016/j.scitotenv.2008.02.021

    CAS  CrossRef  PubMed  Google Scholar 

  • Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Muller L, King LA, Rosner B, Buchholz U, Stark K, Krause G, Team HUSI (2011) Epidemic profile of shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365:1771–1780

    CAS  PubMed  CrossRef  Google Scholar 

  • Freeman VJ (1951) Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J Bacteriol 61(6):675–688

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freer JH, Arbuthnott JP (1982) Toxins of Staphylococcus aureus. Pharmacol Ther 19:55–106

    CAS  PubMed  CrossRef  Google Scholar 

  • Fruth A, Prager R, Tietze E, Rabsch W, Flieger A (2015) Molecular epidemiological view on Shiga toxin-producing Escherichia coli causing human disease in Germany: diversity, prevalence, and outbreaks. Int J Med Microbiol 305(7):697–704. https://doi.org/10.1016/j.ijmm.2015.08.020

    CrossRef  PubMed  Google Scholar 

  • Gamage SD, Patton AK, Hanson JF, Weiss AA (2004) Diversity and host range of Shiga toxin-encoding phage. Infect Immun 72(12):7131–7139

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Garcia-Aljaro C, Muniesa M, Jofre J, Blanch AR (2006) Newly identified bacteriophages carrying the stx Shiga toxin gene isolated from Escherichia coli strains in polluted waters. FEMS Microbiol Lett 258:127–135

    CAS  PubMed  CrossRef  Google Scholar 

  • Garcia-Aljaro C, Muniesa M, Jofre J, Blanch AR (2009) Genotypic and phenotypic diversity among induced, stx(2)-carrying bacteriophages from environmental Escherichia coli strains. Appl Environ Microbiol 75:329–336

    CAS  PubMed  CrossRef  Google Scholar 

  • Goerke C, Wolz C (2010) Adaptation of Staphylococcus aureus to the cystic fibrosis lung. Int J Med Microbiol 300(8):520–525. https://doi.org/10.1016/j.ijmm.2010.08.003

    CrossRef  PubMed  Google Scholar 

  • Goh S, Hussain H, Chang BJ, Emmett W, Riley TV, Mullany P (2013) Phage phi C2 mediates transduction of Tn6215, encoding erythromycin resistance, between Clostridium difficile strains. MBio 4(6):e00840-13. https://doi.org/10.1128/mBio.00840-13

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Goldhill DH, Turner PE (2014) The evolution of life history trade-offs in viruses. Curr Opin Virol 8:79–84

    PubMed  CrossRef  Google Scholar 

  • Gomez P, Bennie J, Gaston KJ, Buckling A (2015) The impact of resource availability on bacterial resistance to phages in soil. PLoS One 10(4):e0123752. https://doi.org/10.1371/journal.pone.0123752

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Gomez P, Buckling A (2011) Bacteria-phage antagonistic coevolution in soil. Science 332(6025):106–109

    CAS  PubMed  CrossRef  Google Scholar 

  • Gorter FA, Scanlan PD, Buckling A (2016) Adaptation to abiotic conditions drives local adaptation in bacteria and viruses coevolving in heterogeneous environments. Biol Lett 12(2):20150879

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Govan JRW, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Govind R, Fralick JA, Rolfe RD (2011) In vivo lysogenization of a Clostridium difficile bacteriophage Phi CD119. Anaerobe 17(3):125–129

    PubMed Central  CrossRef  CAS  Google Scholar 

  • Groman N (1953) The relation of bacteriophage to the change of Corynebacterium diphtheriae from avirulence to virulence. Science 117:297–299

    CAS  PubMed  CrossRef  Google Scholar 

  • Guinane CM, Kent RM, Norberg S, Hill C, Fitzgerald GF, Stanton C, Ross RP (2011) Host specific diversity in Lactobacillus johnsonii as evidenced by a major chromosomal inversion and phage resistance mechanisms. PLoS One 6(4):e18740

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Guy L, Nystedt B, Toft C, Zaremba-Niedzwiedzka K, Berglund EC, Granberg F, Naslund K, Eriksson AS, Andersson SGE (2013) A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella. PLoS Genet 9:22

    CrossRef  CAS  Google Scholar 

  • Haaber J, Leisner JJ, Cohn MT, Catalan-Moreno A, Nielsen JB, Westh H, Penadés JR, Ingmer H (2016) Bacterial viruses enable their host to acquire antibiotic resistance genes from neighbouring cells. Nat Commun 7:13333

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Hall AR, Scanlan PD, Morgan AD, Buckling A (2011) Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol Lett 14(7):635–642

    PubMed  CrossRef  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108. https://doi.org/10.1038/nrmicro821

    CAS  CrossRef  PubMed  Google Scholar 

  • Hammerl JA, Al Dahouk S, Nöckler K, Göllner C, Appel B, Hertwig S (2014) F1 and Tbilisi are closely related Brucellaphages exhibiting some distinct nucleotide variations which determine the host specificity. Genome Announc 2(1):e01250-01213

    CrossRef  Google Scholar 

  • Hammerl JA, Göllner C, AlDahouk S, Nöckler K, Reetz J, Hertwig S (2016) Analysis of the first temperate broad host range Brucellaphage (BiPBO1) isolated from B. inopinata. Front Microbiol 7:24. https://doi.org/10.3389/fmicb.2016.00024

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Hannigan GD, Meisel JS, Tyldsley AS, Zheng Q, Hodkinson BP, SanMiguel AJ, Minot S, Bushman FD, Grice EA (2015) The Human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. mBio 6(5):e01578-15. https://doi.org/10.1128/mBio.01578-15

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Haramoto E, Katayama H, Oguma K, Yamashita H, Tajima A, Nakajima H, Ohgaki S (2006) Seasonal profiles of human Noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Sci Technol 54:301–308

    CAS  PubMed  CrossRef  Google Scholar 

  • Hawkey PM, Jones AM (2009) The changing epidemiology of resistance. J Antimicrob Chemother 64(Supplement 1):i3–i10

    CAS  PubMed  CrossRef  Google Scholar 

  • Hazen TH, Pan L, Gu JD, Sobecky PA (2010) The contribution of mobile genetic elements to the evolution and ecology of Vibrios. FEMS Microbiol Ecol 74:485–499

    CAS  PubMed  CrossRef  Google Scholar 

  • Helbin WM, Polakowska K, Miedzobrodzki J (2012) Phage-related virulence factors of Staphylococcus aureus. Postepy Mikrobiologii 51:291–298

    CAS  Google Scholar 

  • Heler R, Marraffini LA, Bikard D (2014) Adapting to new threats: the generation of memory by CRISPR-Cas immune systems. Mol Microbiol 93:1–9

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Horne MT (1970) Coevolution of Escherichia coli and bacteriophages in chemostat culture. Science 168:992–993

    CAS  PubMed  CrossRef  Google Scholar 

  • Horvath P, Barrangou R (2011) Protection against foreign DNA. In: Storz G, Hengge R (eds) Bacterial stress responses, 2nd edn. ASM Press, Washington, DC, pp 333–348

    CrossRef  Google Scholar 

  • Huang S, Zhang S, Jiao N, Chen F (2015) Comparative genomic and phylogenomic analyses reveal a conserved core genome shared by estuarine and oceanic cyanopodoviruses. PLoS One 10(11):e0142962. https://doi.org/10.1371/journal.pone.0142962

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Hurwitz BL, Brum JR, Sullivan MB (2015) Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean virome. ISME J 9:472–484

    CAS  PubMed  CrossRef  Google Scholar 

  • Hynes AP, Villion M, Moineau S (2014) Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages. Nat Commun 5:4399. https://doi.org/10.1038/ncomms5399

    CAS  CrossRef  PubMed  Google Scholar 

  • Inoue K, Iida H (1970) Conversion of toxigenicity in Clostridium botulinum type C. Jpn J Microbiol 14(1):87–89

    CAS  PubMed  CrossRef  Google Scholar 

  • Ivanov YV, Shariat N, Register KB, Linz B, Rivera I, Hu K, Dudley EG, Harvill ET (2015) A newly discovered Bordetella species carries a transcriptionally active CRISPR-Cas with a small Cas9 endonuclease. BMC Genomics 16:863. https://doi.org/10.1186/s12864-015-2028-9

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Jacob AE, Hobbs SJ (1974) Conjugal transfer of plasmid-borne multiple antibiotic-resistance in Streptococcus-faecalis var zymogenes. J Bacteriol 117:360–372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang SC, Paul JH (1996) Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar Ecol Prog Ser 142(1–3):27–38

    CrossRef  Google Scholar 

  • Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64(8):2780–2787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jjemba PK (2002a) The potential impact of veterinary and human therapeutic agents in manure and biosolids on plants grown on arable land: a review. Agric Ecosyst Environ 93(1–3):267–278. https://doi.org/10.1016/s0167-8809(01)00350-4

    CrossRef  Google Scholar 

  • Jjemba PK (2002b) The effect of chloroquine, quinacrine, and metronidazole on both soybean plants and soil microbiota. Chemosphere 46(7):1019–1025

    CAS  PubMed  CrossRef  Google Scholar 

  • Johnson L, Schlievert P (1984) Group A streptococcal phage T12 carries the structural gene for pyrogenic exotoxin type A. Mol Gen Genet 194(1–2):52–56

    CAS  PubMed  CrossRef  Google Scholar 

  • Kashiwagi A, Yomo T, Casadesús J (2011) Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage QÎ2 and Escherichia coli. PLoS Genet 7(8):e1002188

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Karmali MA (2017) Emerging public health challenges of shiga toxin-producing Escherichia coli related to changes in the pathogen, the population, and the environment. Clin Infect Dis 64(3):371–376. https://doi.org/10.1093/cid/ciw708

    CrossRef  PubMed  Google Scholar 

  • Karpe YA, Kanade GD, Pingale KD, Arankalle VA, Banerjee K (2016) Genomic characterization of Salmonella bacteriophages isolated from India. Virus Genes 52(1):117–126

    CAS  PubMed  CrossRef  Google Scholar 

  • Karataev GI, Moskivina IL, Ryabinina OP, Miller GG, Mebel SM, Lapaeva IA (1988) Isolation and characterization of bacteriophage from the vaccine strain Tohama Phase I. Mol Genet Microbiol Virol 4:22–25

    Google Scholar 

  • Kay P, Blackwell PA, Boxall ABA (2004) Fate of veterinary antibiotics in a macroporous tile drained clay soil. Environ Toxicol Chem 23(5):1136–1144. https://doi.org/10.1897/03-374

    CAS  CrossRef  PubMed  Google Scholar 

  • Kelly WJ, Altermann E, Lambie SC, Leahy SC (2013) Interaction between the genomes of Lactococcus lactis and phages of the P335 species. Front Microbiol 4:257

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8(1):1–13. https://doi.org/10.1016/j.ecolind.2007.06.002

    CAS  CrossRef  Google Scholar 

  • Kim MS, Bae JW (2016) Spatial disturbances in altered mucosal and luminal gut viromes of diet-induced obese mice. Environ Microbiol 18:1498–1510

    CAS  PubMed  CrossRef  Google Scholar 

  • Kim EJ, Lee CH, Nair GB, Kim DW (2015) Whole-genome sequence comparisons reveal the evolution of Vibrio cholerae O1. Trends Microbiol 23:479–489

    CAS  PubMed  CrossRef  Google Scholar 

  • Koonin EV, Makarova KS, Wolf YI (2017) Evolutionary genomics of defense systems in archaea and bacteria. Annu Rev Microbiol 71(1):233–261

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Koskella B (2013) Phage-mediated selection on microbiota of a long-lived host. Curr Biol 23:1256–1260

    CAS  PubMed  CrossRef  Google Scholar 

  • Koskella B, Meaden S (2013) Understanding bacteriophage specificity in natural microbial communities. Viruses 5(3):806–823. PMC. Web. 20 July 2018

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Koskella B, Lin DM, Buckling A, Thompson JN (2012) The costs of evolving resistance in heterogeneous parasite environments. Proc R Soc B Biol Sci 279(1735):1896–1903

    CrossRef  Google Scholar 

  • Krahn T, Wibberg D, Maus I, Winkler A, Bontron S, Sczyrba A, Nordmann P, Puehler A, Poirel L, Schlueter A (2016) Intraspecies transfer of the chromosomal Acinetobacter baumannii bla(NDM-1) carbapenemase gene. Antimicrob Agents Chemother 60(5):3032–3040

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Kraushaar B, Hammerl JA, Kienol M, Heinig ML, Sperling N, Thanh MD, Reetz J, Jakel C, Fetsch A, Hertwig S (2017) Acquisition of virulence factors in livestock-associated MRSA: lysogenic conversion of CC398 strains by virulence gene-containing phages. Sci Rep 7. https://doi.org/10.1038/s41598-017-02175-4

  • L’Abee-Lund TM, Jorgensen HJ, O’Sullivan K, Bohlin J, Ligard G, Granum PE, Lindback T (2012) The highly virulent 2006 Norwegian EHEC O103:H25 outbreak strain is related to the 2011 German O104:H4 outbreak strain. PLoS One 7(3):e31413. https://doi.org/10.1371/journal.pone.0031413

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Lachmayr KL, Kerkhof LJ, DiRienzo AG, Cavanaugh CM, Ford TE (2009) Quantifying nonspecific TEM beta-lactamase (bla(TEM)) genes in a wastewater stream. Appl Environ Microbiol 75:203–211

    CAS  PubMed  CrossRef  Google Scholar 

  • Lainhart W, Stolfa G, Koudelka G (2009) Shiga toxin as a bacterial defense against a eukaryotic predator, Tetrahymena thermophila. J Bacteriol 191(16):5116–5122

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Lam J, Chan R, Lam K, Costerton JW (1980) Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect Immun 28(2):546–556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lan S-F, Huang C-H, Chang C-H, Liao W-C, Lin I-H (2009) Characterization of a new plasmid-like prophage in a pandemic. Appl Environ Microbiol 75(9):2659–2667

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Lapaeva IA, Mebel SM, Pereverzev NA, Sinyashina LN (1980) Bordetella pertussis bacteriophage. Zh Mikrobiol Epidemiol Immunobiol 5:85–90

    Google Scholar 

  • Latino L, Essoh C, Blouin Y, Thien HV, Pourcel C (2014) A novel Pseudomonas aeruginosa bacteriophage, Ab31, a chimera formed from temperate phage PAJU2 and P. putida lytic phage AF: characteristics and mechanism of bacterial resistance. PLoS One 9(4):e93777. https://doi.org/10.1371/journal.pone.0093777

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Levin BR, Guttman DS (2010) Nasty viruses, costly plasmids, population dynamics, and the conditions for establishing and maintaining CRISPR-mediated adaptive immunity in bacteria. PLoS Genet 6(10):e1001171

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Lee YD, Park JH (2016) Phage conversion for beta-lactam antibiotic resistance of Staphylococcus aureus from foods. J Microbiol Biotechnol 26(2):263–269

    CAS  PubMed  CrossRef  Google Scholar 

  • Lee JY, Li ZQ, Miller ES (2017) Vibrio phage KVP40 encodes a functional NAD+ salvage pathway. J Bacteriol 199(9):e00855-16. https://doi.org/10.1128/JB.00855-16

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Lemieux A-A, Jeukens J, Kukavica-Ibrulj I, Fothergill JL, Boyle B, Laroche J, Tucker NP, Winstanley C, Levesque RC (2016) Genes required for free phage production are essential for Pseudomonas aeruginosa chronic lung infections. J Infect Dis 213(3):395–402

    CAS  PubMed  CrossRef  Google Scholar 

  • Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10:1–44

    CAS  Google Scholar 

  • Lenski RE, Levin BR (1985) Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am Nat 125(4):585–602

    CrossRef  Google Scholar 

  • Lindsay J, Ruzin A, Ross H, Kurepina N, Novick R (1998) The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29(2):527–543

    CAS  PubMed  CrossRef  Google Scholar 

  • Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO, Alt DP, Henrissat B, Stanton TB (2014) Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J 8(8):1566–1576. https://doi.org/10.1038/ismej.2014.12

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Los JM, Los M, Wegrzyn A, Wegrzyn G (2013) Altruism of shiga toxin-producing Escherichia coli: recent hypothesis versus experimental results. Front Cell Infect Microbiol 3:166. https://doi.org/10.3389/fcimb.2012.00166

    CrossRef  Google Scholar 

  • Lupo A, Coyne S, Berendonk TU (2012) Origin and evolution of antibiotic resistance: the common mechanisms of emergence and spread in water bodies. Front Microbiol 3:13

    CrossRef  Google Scholar 

  • Mai-Prochnow A, Hui JGK, Kjelleberg S, Rakonjac J, McDougald D, Rice SA (2015) Big things in small packages: the genetics of filamentous phage and effects on fitness of their host. FEMS Microbiol Rev 39(4):465–487. https://doi.org/10.1093/femsre/fuu007

    CrossRef  PubMed  Google Scholar 

  • Maloy SR, Stewart VJ, Taylor RK (1996) Genetic analysis of pathogenic bacteria: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Marti R, Muniesa M, Schmid M, Ahrens CH, Naskova J, Hummerjohann J (2016) Short communication: heat-resistant Escherichia coli as potential persistent reservoir of extended-spectrum beta-lactamases and Shiga toxin-encoding phages in dairy. J Dairy Sci 99(11):8622–8632. https://doi.org/10.3168/jds.2016-11076

    CAS  CrossRef  PubMed  Google Scholar 

  • McGavin MJ, Arsic B, Nickerson NN (2012) Evolutionary blueprint for host- and niche-adaptation in Staphylococcus aureus clonal complex CC30. Front Cell Infect Microbiol 2:48. https://doi.org/10.3389/fcimb.2012.00048

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • McGee LW, Aitchison EW, Brian Caudle S, Morrison AJ, Zheng L, Yang W, Rokyta DR, Worobeg M (2014) Payoffs, not tradeoffs, in the adaptation of a virus to ostensibly conflicting selective pressures. PLoS Genet 10(10):e1004611

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • McLaughlin MR, Rose JB (2006) Application of Bacteroides fragilis phage as an alternative indicator of sewage pollution in Tampa Bay, Florida. Estuar Coasts 29(2):246–256

    CrossRef  Google Scholar 

  • Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT, Lenski RE (2012) Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335:428–432

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Miao XS, Bishay F, Chen M, Metcalfe CD (2004) Occurrence of antimicrobials in the final effluents of wastewater treatment plants in Canada. Environ Sci Technol 38(13):3533–3541. https://doi.org/10.1021/es030653q

    CAS  CrossRef  PubMed  Google Scholar 

  • Michel-Briand Y, Baysse C (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84(5–6):499–510

    CAS  PubMed  CrossRef  Google Scholar 

  • Morris P, Marinelli LJ, Jacobs-Sera D, Hendrix RW, Hatfull GF (2008) Genomic characterization of mycobacteriophage giles: evidence for phage acquisition of host DNA by illegitimate recombination. J Bacteriol 190(6):2172–2182

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Moce-Llivina L, Muniesa M, Pimenta-Vale H, Lucena F, Jofre J (2003) Survival of bacterial indicator species and bacteriophages after thermal treatment of sludge and sewage. Appl Environ Microbiol 69:1452–1456

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219–222

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Mookerjee S, Batabyal P, Sarkar M, Palit A (2015) Seasonal prevalence of enteropathogenic Vibrio and their phages in the riverine estuarine ecosystem of South Bengal. PLoS One 10(9):13

    CrossRef  CAS  Google Scholar 

  • Moon BY, Park JY, Hwang SY, Robinson DA, Thomas JC, Fitzgerald JR, Park YH, Seo KS (2015) Phage-mediated horizontal transfer of a Staphylococcus aureus virulence-associated genomic island. Sci Rep 5(1):9784. https://doi.org/10.1038/srep09784

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Mora A, Herrera A, Lopez C, Dahbi G, Mamani R, Pita JM, Alonso MP, Llovo J, Bernardez MI, Blanco JE, Blanco M, Blanco J (2011) Characteristics of the Shiga-toxin-producing enteroaggregative Escherichia coli O104:H4 German outbreak strain and of STEC strains isolated in Spain. Int Microbiol 14:121–141

    CAS  PubMed  Google Scholar 

  • Morgan AD, Bonsall MB, Buckling A (2010) Impact of bacterial mutation rate on coevolutionary dynamics between bacteria and phages. Evolution 64(10):2980–2987. https://doi.org/10.1111/j.1558-5646.2010.01037.x

    CrossRef  PubMed  Google Scholar 

  • Motlagh AM, Bhattacharjee AS, Coutinho FH, Dutilh BE, Casjens SR, Goel RK (2017) Insights of phage-host interaction in hypersaline ecosystem through metagenomics analyses. Front Microbiol 8:15

    CrossRef  Google Scholar 

  • Muniesa M, Jofre J (2004) Abundance in sewage of bacteriophages infecting Escherichia coli O157:H7. Public Health Microbiol Methods Protocols 268:79–88

    CAS  CrossRef  Google Scholar 

  • Muniesa M, Serra-Moreno R, Jofre J (2004) Free Shiga toxin bacteriophages isolated from sewage showed diversity although the stx genes appeared conserved. Environ Microbiol 6:716–725

    CAS  PubMed  CrossRef  Google Scholar 

  • Murugaiyan S, Bae JY, Wu J, Lee SD, Um HY, Choi HK, Chung E, Lee JH, Lee SW (2011) Characterization of filamentous bacteriophage PE226 infecting Ralstonia solanacearum strains. J Appl Microbiol 110:296–303

    CAS  PubMed  CrossRef  Google Scholar 

  • Nasu H, Iida T, Sugahara T, Yamaichi Y, Park K, Yokoyama K, Makino K, Shinagawa H, Honda T (2000) A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3:K6 strains. J Clin Microbiol 38(6):2156–2161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nedialkova LP, Sidstedt M, Koeppel MB, Spriewald S, Ring D, Gerlach RG, Bossi L, Stecher B (2016) Temperate phages promote colicin-dependent fitness of serovar Typhimurium. Environ Microbiol 18(5):1591–1603

    CAS  PubMed  CrossRef  Google Scholar 

  • Novick RP, Christie GE, Penades JR (2010) The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541–551

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Nyambe S, Burgess C, Whyte P, Bolton D (2016a) Survival studies of a temperate and lytic bacteriophage in bovine faeces and slurry. J Appl Microbiol 121(4):1144–1151

    CAS  PubMed  CrossRef  Google Scholar 

  • Nyambe S, Burgess C, Whyte P, Bolton D (2016b) The survival of a temperate vtx bacteriophage and an anti-verocytotoxigenic O157 lytic phage in water and soil samples. Zoonoses Public Health 63(8):632–640

    CAS  PubMed  CrossRef  Google Scholar 

  • Obeng N, Pratama AA, van Elsas JD (2016) The significance of mutualistic phages for bacterial ecology and evolution. Trends Microbiol 24(6):440–449

    CAS  PubMed  CrossRef  Google Scholar 

  • O’Brien AD, Newland JW, Miller SF, Holmes RK, Smith HW, Formal SB (1984) Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226(4675):694–696

    PubMed  CrossRef  Google Scholar 

  • O’Brien S, Rodrigues AMM, Buckling A (2013) The evolution of bacterial mutation rates under simultaneous selection by interspecific and social parasitism. Proc R Soc B Biol Sci 280(1773):20131913

    PubMed  CrossRef  PubMed Central  Google Scholar 

  • Okuda J, Ishibashi M, Hayakawa E, Nishino T (1997) Emergence of a Unique O3:K6 Clone of Vibrio parahaemolyticus. J Clin Microbiol 35(12):3150–3155

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Shea YA, Fidelma Boyd E (2002) Mobilization of the pathogenicity island between isolates mediated by CP-T1 generalized transduction. FEMS Microbiol Lett 214(2):153–157

    PubMed  CrossRef  Google Scholar 

  • Pal C, Macia MD, Oliver A, Schachar I, Buckling A (2007) Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450(7172):1079–1081. https://doi.org/10.1038/nature06350

    CAS  CrossRef  PubMed  Google Scholar 

  • Park MO, Ikenaga H, Watanabe K (2007) Phage diversity in a methanogenic digester. Microb Ecol 53:98–103

    CAS  PubMed  CrossRef  Google Scholar 

  • Park D, Stanton E, Ciezki K, Parrell D, Bozile M, Pike D, Forst SA, Jeong KC, Ivanek R, Dopfer D, Kaspar CW (2013) Evolution of the stx2-encoding prophage in persistent bovine Escherichia coli O157:H7 strains. Appl Environ Microbiol 79:1563–1572

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR, Quail M, Smith F, Walker D, Libberton B, Fenton A, Hall N, Brockhurst MA (2010) Antagonistic coevolution accelerates molecular evolution. Nature 464(7286):275–278

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Paton A, Paton J (1996) Enterobacter cloacae producing a shiga-like toxin II-related cytotoxin associated with a case of hemolytic-uremic syndrome. J Clin Microbiol 34(2):463–465

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paul JH, Sullivan MB, Segall AM, Rohwer F (2002) Marine phage genomics. Comp Biochem Physiol B Biochem Mol Biol 133:463–476

    PubMed  CrossRef  Google Scholar 

  • Payne M, Oakey J, Owens L (2004) The ability of two different Vibrio spp. bacteriophages to infect Vibrio harveyi, Vibrio cholerae and Vibrio mimicus. J Appl Microbiol 97:663–672

    CAS  PubMed  CrossRef  Google Scholar 

  • Pearson GDN, Woods A, Chiang SL, Mekalanos JJ (1993) Ctx genetic element encodes a site-specific recombination system and an intestinal colonization factor. Proc Natl Acad Sci USA 90:3750–3754

    CAS  PubMed  CrossRef  PubMed Central  Google Scholar 

  • Penadés JR, Christie GE (2015) The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. In: Enquist LW (ed) Annual review of virology, vol 2, pp 181–201. https://doi.org/10.1146/annurev-virology-031413-085446

    CrossRef  Google Scholar 

  • Perez G, Thierauf A, Maloy S (2009) Generalized transduction. In: Bacteriophages: methods in molecular biology. Humana Press, New York, pp 267–286

    Google Scholar 

  • Perry EB, Barrick JE, Bohannan BJM (2015) The molecular and genetic basis of repeatable coevolution between Escherichia coli and bacteriophage T3 in a laboratory microcosm. PLoS One 10(6):e0130639

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Petridis M, Bagdasarian M, Waldor MK, Walker E (2006) Horizontal transfer of Shiga toxin and antibiotic resistance genes among Escherichia coli strains in house fly (Diptera: Muscidae) gut. J Med Entomol 43(2):288–295

    CAS  PubMed  CrossRef  Google Scholar 

  • Picozzi C, Volponi G, Vigentini I, Grassi S, Foschino R (2012) Assessment of transduction of Escherichia coli stx2-encoding phage in dairy process conditions. Int J Food Microbiol 153:388–394

    CAS  PubMed  CrossRef  Google Scholar 

  • Plunkett G, Rose D, Durfee T, Blattner F (1999) Sequence of shiga toxin 2 phage 933w from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J Bacteriol 181(6):1767–1778

    CAS  PubMed  PubMed Central  Google Scholar 

  • Popoff MR, Bouvet P (2013) Genetic characteristics of toxigenic Clostridia and toxin gene evolution. Toxicon 75:63–89

    CAS  PubMed  CrossRef  Google Scholar 

  • Potts SB, Roggli VL, Spock A (1995) Immunohistologic quantification of Pseudomonas aeruginosa in the tracheobronchial tree from patients with cystic-fibrosis. Pediatr Pathol Lab Med 15:707–721

    CAS  PubMed  CrossRef  Google Scholar 

  • Puxty R, Millard A, Evans D, Scanlan D (2015) Shedding new light on viral photosynthesis. Photosynth Res 12(1):71–97

    CrossRef  CAS  Google Scholar 

  • Rohwer F, Thurber RV (2009) Viruses manipulate the marine environment. Nature 459(7244):207–212. https://doi.org/10.1038/nature08060

    CAS  CrossRef  PubMed  Google Scholar 

  • Rolain J, Fancello L, Desnues C, Raoult D (2011) Bacteriophages as vehicles of the resistome in cystic fibrosis. J Antimicrob Chemother 66(11):2444–2447

    CAS  PubMed  CrossRef  Google Scholar 

  • Ross J, Topp E (2015) Abundance of antibiotic resistance genes in bacteriophage following soil fertilization with dairy manure or municipal biosolids, and evidence for potential transduction. Appl Environ Microbiol 81(22):7905–7913. https://doi.org/10.1128/aem.02363-15

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65(5):725–759. https://doi.org/10.1016/j.chemosphere.2006.03.026

    CAS  CrossRef  PubMed  Google Scholar 

  • Sarris PF, Ladoukakis ED, Panopoulos NJ, Scoulica EV (2014) A phage tail-derived element with wide distribution among both prokaryotic domains: a comparative genomic and phylogenetic study. Genome Biol Evol 6(7):1739–1747

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Scanlan PD, Hall AR, Lopez-Pascua LDC, Buckling A (2011) Genetic basis of infectivity evolution in a bacteriophage. Mol Ecol 20:981–989

    PubMed  CrossRef  Google Scholar 

  • Scott J, Nguyen SV, King CJ, Hendrickson C, McShan WM (2012) Phage-like Streptococcus pyogenes chromosomal islands (SpyCI) and mutator phenotypes: control by growth state and rescue by a SpyCI-encoded promoter. Front Microbiol 3:317. https://doi.org/10.3389/fmicb.2012.00317

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Shapiro JW, Williams E, Turner PE (2016) Evolution of parasitism and mutualism between filamentous phage M13 and Escherichia coli. PeerJ 4:e2060. https://doi.org/10.7717/peerj.2060

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Sharma P, Gupta SK, Rolain JM (2014) Whole genome sequencing of bacteria in cystic fibrosis as a model for bacterial genome adaptation and evolution. Expert Rev Anti-Infect Ther 12(3):343–355. https://doi.org/10.1586/14787210.2014.887441

    CAS  CrossRef  PubMed  Google Scholar 

  • Sinton LW, Hall CH, Lynch PA, Davies-Colley RJ (2002) Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl Environ Microbiol 68:1122–1131

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Smith DL, Rooks DJ, Fogg PCM, Darby AC, Thomson NR, McCarthy AJ, Allison HE (2012) Comparative genomics of Shiga toxin encoding bacteriophages. BMC Genomics 13(1):311

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Solheim M, Brekke MC, Snipen LG, Willems RJL, Nes IF, Brede DA (2011) Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis. BMC Microbiol 11:3. https://doi.org/10.1186/1471-2180-11-3

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Solheim HT, Sekse C, Urdahl AM, Wasteson Y, Nesse LL (2013) Biofilm as an environment for dissemination of stx genes by transduction. Appl Environ Microbiol 79:896–900

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Sommer MOA, Dantas G, Church GM (2009) Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325:1128–1131

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Strockbine N, Marques L, Newland J et al (1986) Two toxin-converting phages from Escherichia coli O157:H7 strain 933 encode antigenically distinct toxins with similar biological activities. Infect Immun 53(1):135–140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steinberg KM, Levin BR (2007) Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophage. Proc R Soc B Biol Sci 274(1621):1921–1929

    CrossRef  Google Scholar 

  • Subirats J, Sanchez-Melsio A, Borrego CM, Balcazar JL, Simonet P (2016) Metagenomic analysis reveals that bacteriophages are reservoirs of antibiotic resistance genes. Int J Antimicrob Agents 48(2):163–167. https://doi.org/10.1016/j.ijantimicag.2016.04.028

    CAS  CrossRef  PubMed  Google Scholar 

  • Sugiyama H (1980) Clostridium botulinum neurotoxin. Microbiol Rev 44(3):419–448

    CAS  PubMed  PubMed Central  Google Scholar 

  • Summer EJ, Gonzalez CF, Bomer M, Carlile T, Embry A, Kucherka AM, Lee J, Mebane L, Morrison WC, Mark L, King MD, LiPuma JJ, Vidaver AK, Young R (2005) Divergence and mosaicism among virulent soil phages of the Burkholderia cepacia complex. J Bacteriol 188(1):255–268

    CrossRef  CAS  Google Scholar 

  • Tanji Y, Mizoguchi K, Yoichi M, Morita M, Kijima N, Kator H, Unno H (2003) Seasonal change and fate of coliphages infected to Escherichia coli O157:H7 in a wastewater treatment plant. Water Res 37:1136–1142

    CAS  PubMed  CrossRef  Google Scholar 

  • Timms AR, Cambray-Young J, Scott AE, Petty NK, Connerton PL, Clarke L, Seeger K, Quail M, Cummings N, Maskell DJ, Thomson NR, Connerton IF (2010) Evidence for a lineage of virulent bacteriophages that target Campylobacter. BMC Genomics 11(1):214

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Tozzoli R, Grande L, Michelacci V, Ranieri P, Maugliani A, Caprioli A, Morabito S (2014) Shiga toxinconverting phages and the emergence of new pathogenic Escherichia coli: a world in motion. Front Cell Infect Microbiol 4:80

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Uyaguari MI, Fichot EB, Scott GI, Norman RS (2011) Characterization and quantitation of a novel β-lactamase gene found in a wastewater treatment facility and the surrounding coastal ecosystem. Appl Environ Microbiol 77(23):8226–8233

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • van Overbeek LS, van Doorn J, Wichers JH, van Amerongen A, van Roermund HJW, Willemsen PTJ (2014) The arable ecosystem as battleground for emergence of new human pathogens. Front Microbiol 5:104

    PubMed  PubMed Central  Google Scholar 

  • Varga M, Kuntova L, Pantucek R, Maslanova I, Ruzickova V, Doskar J (2012) Efficient transfer of antibiotic resistance plasmids by transduction within methicillin-resistant Staphylococcus aureus USA300 clone. FEMS Microbiol Lett 332:146–152

    CAS  PubMed  CrossRef  Google Scholar 

  • Varga M, Pantucek R, Ruzickova V, Doskar J (2016) Molecular characterization of a new efficiently transducing bacteriophage identified in methicillin-resistant Staphylococcus aureus. J Gen Virol 97:258–267

    CAS  PubMed  CrossRef  Google Scholar 

  • Vasse M, Torres-Barceló C, Hochberg ME (2015) Phage selection for bacterial cheats leads to population decline. Proc R Soc B Biol Sci 282(1818):20152207

    CrossRef  CAS  Google Scholar 

  • Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther 40(4):277–283

    Google Scholar 

  • Veses-Garcia M, Liu X, Rigden DJ, Kenny JG, McCarthy AJ, Allison HE (2015) Transcriptomic analysis of shiga-toxigenic bacteriophage carriage reveals a profound regulatory effect on acid resistance in Escherichia coli. Appl Environ Microbiol 81(23):8118–8125. https://doi.org/10.1128/aem.02034-15

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Vishwakarma V, Periaswamy B, Pati NB, Slack E, Hardt WD, Suar M (2012) A novel phage element of Salmonella enterica serovar enteritidis p125109 contributes to accelerated type III secretion system 2-dependent early inflammation kinetics in a mouse colitis model. Infect Immun 80:3236–3246

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Wagner PL, Waldor MK (2002) Bacteriophage control of bacterial virulence. Infect Immun 70:3985–3993

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Waksman S (1961) Role of Antibiotics in Nature. Perspect Biol Med 4(3):271

    CrossRef  Google Scholar 

  • Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272(5270):1910–1914

    CAS  PubMed  CrossRef  Google Scholar 

  • Wang YQ, Zhang XB (2010) Genome analysis of deep-sea thermophilic phage D6E. Appl Environ Microbiol 76:7861–7866

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Wang CH, Chuan CN, Kuo HT, Zheng PX, Tsou CC, Wang SY, Tsai PJ, Chuang WJ, Lin YS, Liu CC, Wu JJ (2013a) Peroxide responsive regulator perR of Group A Streptococcus is required for the expression of phage-associated DNAse Sda1 under oxidative stress. PLoS One 8(12):e81882. https://doi.org/10.1371/journal.pone.0081882

    CAS  CrossRef  PubMed  PubMed Central  Google Scholar 

  • Wang QY, Kan BA, Wang RB (2013b) Isolation and characterization of the new mosaic filamentous phage VFJ phi of Vibrio cholerae. PLoS One 8:9

    CrossRef  Google Scholar 

  • Weeks C, Ferretti J (1984) The gene for type A Streptococcal exotoxin (erythrogenic toxin) is located in bacteriophage T12. Infect Immun 46(2):531–536

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei RC, Ge F, Huang SY, Chen M, Wang R (2011) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82(10):1408–1414. https://doi.org/10.1016/j.chemosphere.2010.11.067

    CAS  CrossRef  PubMed  Google Scholar 

  • Wei YZ, Chesne MT, Terns RM, Terns MP (2015) Sequences spanning the leader-repeat junction mediate CRISPR adaptation to phage in Streptococcus thermophilus. Nucleic Acids Res 43:1749–1758

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Weinbauer MG, Suttle CA (1999) Lysogeny and prophage induction in coastal and offshore bacterial communities. Aquat Microb Ecol 18:217–225

    CrossRef  Google Scholar 

  • Willner D, Furlan M (2010) Deciphering the role of phage in the cystic fibrosis airway. Virulence 1(4):309–313. https://doi.org/10.4161/viru.1.4.12071

    CrossRef  PubMed  Google Scholar 

  • Willner D, Furlan M, Haynes M, Schmieder R, Angly F, Silva J, Tammadoni S, Nosrat B, Conrad D, Rohwer F (2009) Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS One 4(10):e7370

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Xia GQ, Wolz C (2014) Phages of Staphylococcus aureus and their impact on host evolution. Infect Genet Evol 21:593–601

    CAS  PubMed  CrossRef  Google Scholar 

  • Yamaguchi T, Hayashi T, Takami H, Nakasone K, Ohnishi M, Nakayama K, Yamada S, Sugai M (2000) Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol Microbiol 38(4):694–705

    CAS  PubMed  CrossRef  Google Scholar 

  • Yan YX, Shi YB, Cao DM, Meng XP, Xia LM, Sun JH (2011) Prevalence of stx phages in environments of a pig farm and lysogenic infection of the field E. coli O157 isolates with a recombinant converting phage. Curr Microbiol 62:458–464

    CAS  PubMed  CrossRef  Google Scholar 

  • Yeroshenko GA, Smirnova NI (2004) Role of temperate bacteriophage 139 in changing cholera toxin production in Vibrio cholerae classical biovar. Russ J Genet 40:348–355

    CAS  CrossRef  Google Scholar 

  • Yoshida M, Yoshida-Takashima Y, Nunoura T, Takai K (2015) Identification and genomic analysis of temperate Pseudomonas bacteriophage PstS-1 from the Japan trench at a depth of 7000 m. Res Microbiol 166:668–676

    CAS  PubMed  CrossRef  Google Scholar 

  • Yu C, Ferretti J (1991) Molecular characterization of new group A streptococcal bacteriophages containing the gene for streptococcal erythrogenic toxin (speA). Mol Gen Genet 231:161–168

    CAS  PubMed  CrossRef  Google Scholar 

  • Zabriskie J (1964) The role of temperate bacteriophage in the production of erythrogenic toxin by Group A Streptococci. J Exp Med 119:761–780

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Zhao L, Dong YH, Wang H (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408(5):1069–1075. https://doi.org/10.1016/j.scitotenv.2009.11.014

    CAS  CrossRef  PubMed  Google Scholar 

  • Zhou Y, Sugiyama H, Johnson E (1993) Transfer of neurotoxigenicity from Clostridium butyricum to a nontoxigenic Clostridium botulinum type E-like strain. Appl Environ Microbiol 59(11):3825–3831

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Veronica Casas or Stanley Maloy .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Verify currency and authenticity via CrossMark

Cite this chapter

Casas, V., Maloy, S. (2018). The Role of Phage in the Adaptation of Bacteria to New Environmental Niches. In: Rampelotto, P. (eds) Molecular Mechanisms of Microbial Evolution. Grand Challenges in Biology and Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-69078-0_11

Download citation