Abstract
Horizontal gene transfer (HGT) can create tremendous genetic diversity in organisms, especially those which reproduce asexually. The three classical mechanisms for HGT in prokaryotes are transformation, conjugation, and transduction. Historically, conjugation and transformation were considered to be the major contributors to bacterial HGT, but recent studies indicate that the role of transduction has been underestimated. Bacteriophages are the most abundant biological entities on the planet and contain a vast supply of genetic diversity. Whole genome sequencing of bacterial species has demonstrated that many bacterial virulence factors are encoded by phage or phage-like elements and that often prophage sequences are the major source of variation between bacterial strains. Bacteriophage-mediated HGT occurs through either generalized or specialized transduction. Generalized transducing particles are generated by aberrant packaging of host DNA in place of the viral genome and have the potential to transfer large blocks of bacterial DNA in a single particle. Specialized transducing particles contain a hybrid DNA molecule consisting of viral genes in combination with a small fragment of bacterial DNA. The hybrid DNA molecule associated with these particles is generated by excision from the host genome of a prophage that had been integrated during its lysogenic cycle. This chapter reviews some of the history behind the discovery of transduction, provides an in-depth view of some classic examples of transducing phages, and examines the continued impact of bacteriophage-mediated HGT on current issues such as antibiotic resistance and the safety of phage therapy.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abedon ST (2012) Phage-therapy best practices. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 256–272
Abedon ST, Thomas-Abedon C (2010) Phage therapy pharmacology. Curr Pharm Biotechnol 11(1):28–47
Arber W (1974) DNA modification and restriction. Prog Nucleic Acid Res Mol Biol 14(0):1–37
Austin S, Ziese M, Sternberg N (1981) A novel role for site-specific recombination in maintenance of bacterial replicons. Cell 25(3):729–736. doi:0092-8674(81)90180-X
Bachi B, Arber W (1977) Physical mapping of BglII, BamHI, EcoRI, HindIII and PstI restriction fragments of bacteriophage P1 DNA. Mol Gen Genet 153(3):311–324
Balcazar JL (2014) Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog 10(7):e1004219. https://doi.org/10.1371/journal.ppat.1004219
Ball CA, Johnson RC (1991) Multiple effects of Fis on integration and the control of lysogeny in phage lambda. J Bacteriol 173(13):4032–4038
Beaber JW, Hochhut B, Waldor MK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427(6969):72–74. https://doi.org/10.1038/nature02241
Bearson BL, Allen HK, Brunelle BW et al (2014) The agricultural antibiotic carbadox induces phage-mediated gene transfer in Salmonella. Front Microbiol 5:52. https://doi.org/10.3389/fmicb.2014.00052
Bearson BL, Brunelle BW (2015) Fluoroquinolone induction of phage-mediated gene transfer in multidrug-resistant Salmonella. Int J Antimicrob Agents 46(2):201–204. https://doi.org/10.1016/j.ijantimicag.2015.04.008
Benson NR, Roth J (1997) A Salmonella phage-P22 mutant defective in abortive transduction. Genetics 145(1):17–27
Bertani G, Weigle JJ (1953) Host controlled variation in bacterial viruses. J Bacteriol 65(2):113–121
Billard-Pomares T, Fouteau S, Jacquet ME et al (2014) Characterization of a P1-like bacteriophage carrying an SHV-2 extended-spectrum beta-lactamase from an Escherichia coli strain. Antimicrob Agents Chemother 58(11):6550–6557. https://doi.org/10.1128/AAC.03183-14
Black LW (1989) DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43:267–292. https://doi.org/10.1146/annurev.mi.43.100189.001411
Botstein D, Matz MJ (1970) A recombination function essential to the growth of bacteriophage P22. J Mol Biol 54(3):417–440. doi:0022-2836(70)90119-1
Boulter J, Lee N (1975) Isolation of specialized transducing bacteriophage lambda carrying genes of the L-arabinose operon of Escherichia coli B/r. J Bacteriol 123(3):1043–1054
Brimacombe CA, Ding H, Beatty JT (2014) Rhodobacter capsulatus DprA is essential for RecA-mediated gene transfer agent (RcGTA) recipient capability regulated by quorum-sensing and the CtrA response regulator. Mol Microbiol 92(6):1260–1278. https://doi.org/10.1111/mmi.12628
Brimacombe CA, Ding H, Johnson JA et al (2015) Homologues of genetic transformation DNA import genes are required for rhodobacter capsulatus gene transfer agent recipient capability regulated by the response regulator CtrA. J Bacteriol 197(16):2653–2663. https://doi.org/10.1128/JB.00332-15
Brussow H (2005) Phage therapy: the Escherichia coli experience. Microbiology 151(Pt 7):2133–2140. https://doi.org/10.1099/mic.0.27849-0
Bruttin A, Brussow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49(7):2874–2878. https://doi.org/10.1128/AAC.49.7.2874-2878.2005
Bukhari AI (1976) Bacteriophage mu as a transposition element. Annu Rev Genet 10:389–412. https://doi.org/10.1146/annurev.ge.10.120176.002133
Bukhari AI, Taylor AL (1975) Influence of insertions on packaging of host sequences covalently linked to bacteriophage Mu DNA. Proc Natl Acad Sci U S A 72(11):4399–4403
Calero-Caceres W, Melgarejo A, Colomer-Lluch M et al (2014) Sludge as a potential important source of antibiotic resistance genes in both the bacterial and bacteriophage fractions. Environ Sci Technol 48(13):7602–7611. https://doi.org/10.1021/es501851s
Campbell A (1957) Transduction and segregation in Escherichia coli K12. Virology 4(2):366–384. doi:0042-6822(57)90070-3
Campbell A (1994) Comparative molecular biology of lambdoid phages. Annu Rev Microbiol 48:193–222. https://doi.org/10.1146/annurev.mi.48.100194.001205
Caro L, Berg CM (1971) P1 Transduction. Methods Enzymol 21D:444–458
Casjens S, Hayden M (1988) Analysis in vivo of the bacteriophage P22 headful nuclease. J Mol Biol 199(3):467–474. doi:0022-2836(88)90618-3
Casjens S, Sampson L, Randall S et al (1992) Molecular genetic analysis of bacteriophage P22 gene 3 product, a protein involved in the initiation of headful DNA packaging. J Mol Biol 227(4):1086–1099. doi:0022-2836(92)90523-M
Casjens SR, Gilcrease EB (2009) Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol Biol 502:91–111. https://doi.org/10.1007/978-1-60327-565-1_7
Casjens SR, Hendrix RW (2015) Bacteriophage lambda: Early pioneer and still relevant. Virology 479–480:310–330. https://doi.org/10.1016/j.virol.2015.02.010
Catalano CE, Cue D, Feiss M (1995) Virus DNA packaging: the strategy used by phage lambda. Mol Microbiol 16(6):1075–1086
Chelala CA, Margolin P (1974) Effects of deletions on cotransduction linkage in Salmonella typhimurium: evidence that bacterial chromosome deletions affect the formation of transducing DNA fragments. Mol Gen Genet 131(2):97–112
Chen J, Ram G, Penades JR et al (2015) Pathogenicity island-directed transfer of unlinked chromosomal virulence genes. Mol Cell 57(1):138–149. https://doi.org/10.1016/j.molcel.2014.11.011
Chibani-Chennoufi S, Sidoti J, Bruttin A et al (2004) In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy. Antimicrob Agents Chemother 48(7):2558–2569. https://doi.org/10.1128/AAC.48.7.2558-2569.2004
Chlebowicz MA, Maslanova I, Kuntova L et al (2014) The Staphylococcal Cassette Chromosome mec type V from Staphylococcus aureus ST398 is packaged into bacteriophage capsids. Int J Med Microbiol 304(5–6):764–774. https://doi.org/10.1016/j.ijmm.2014.05.010
Choi W, Jang S, Harshey RM (2014) Mu transpososome and RecBCD nuclease collaborate in the repair of simple Mu insertions. Proc Natl Acad Sci U S A 111(39):14112–14117. https://doi.org/10.1073/pnas.1407562111
Chung ST, Greenberg GR (1973) Loss of an essential function of Escherichia coli by deletions in the thyA region. J Bacteriol 116(3):1145–1149
Clokie MR, Millard AD, Letarov AV et al (2011) Phages in nature. Bacteriophage 1(1):31–45. https://doi.org/10.4161/bact.1.1.14942
Cohen G, Sternberg N (1989) Genetic analysis of the lytic replicon of bacteriophage P1. I Isolation and partial characterization. J Mol Biol 207(1):99–109. doi:0022-2836(89)90443-9
Colomer-Lluch M, Jofre J, Muniesa M (2011) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6(3):e17549. https://doi.org/10.1371/journal.pone.0017549
Court DL, Oppenheim AB, Adhya SL (2007) A new look at bacteriophage lambda genetic networks. J Bacteriol 189(2):298–304. https://doi.org/10.1128/JB.01215-06
Datta N, Hughes VM (1983) Plasmids of the same Inc groups in Enterobacteria before and after the medical use of antibiotics. Nature 306(5943):616–617
Davis BD (1950) Nonfiltrability of the agents of genetic recombination in Escherichia coli. J Bacteriol 60(4):507–508
D'Costa VM, King CE, Kalan L et al (2011) Antibiotic resistance is ancient. Nature 477(7365):457–461. https://doi.org/10.1038/nature10388
Drexler H, Christensen JR (1979) Transduction of bacteriophage lambda by bacteriophage T1. J Virol 30(2):543–550
Ebel-Tsipis J, Botstein D, Fox MS (1972a) Generalized transduction by phage P22 in Salmonella typhimurium. I. Molecular origin of transducing DNA. J Mol Biol 71(2):433–448. doi:0022-2836(72)90361-0
Ebel-Tsipis J, Fox MS, Botstein D (1972b) Generalized transduction by bacteriophage P22 in Salmonella typhimurium. II. Mechanism of integration of transducing DNA. J Mol Biol 71(2):449–469. doi:0022-2836(72)90362-2
Echols H, Court DL (1971) The role of helper phage in gal transduction. In: Hershey AD (ed) The bacteriophage. Lambda The Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 701–710
Echols H, Guarneros G (1983) Control of integration and excision. In: Hendrix RW, Roberts JW, Stahl FW et al (eds) Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 75–92
Enault F, Briet A, Bouteille L et al (2016) Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses. ISME J 11(1):237–247. https://doi.org/10.1038/ismej.2016.90
Feiss M, Fisher RA, Crayton MA et al (1977) Packaging of the bacteriophage lambda chromosome: effect of chromosome length. Virology 77(1):281–293
Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78(2):737–756
Fletcher S (2015) Understanding the contribution of environmental factors in the spread of antimicrobial resistance. Environ Health Prev Med 20(4):243–252. https://doi.org/10.1007/s12199-015-0468-0
Gaze WH, Krone SM, Larsson DG et al (2013) Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg Infect Dis 19(7). https://doi.org/10.3201/eid1907.120871
Genthner FJ, Wall JD (1984) Isolation of a recombination-deficient mutant of Rhodopseudomonas capsulata. J Bacteriol 160(3):971–975
Gill JJ, Hyman P (2010) Phage choice, isolation, and preparation for phage therapy. Curr Pharm Biotechnol 11(1):2–14
Gilmore BF (2012) Bacteriophages as anti-infective agents: recent developments and regulatory challenges. Expert Rev Anti-Infect Ther 10(5):533–535. https://doi.org/10.1586/eri.12.30
Gorski A, Miedzybrodzki R, Borysowski J et al (2009) Bacteriophage therapy for the treatment of infections. Curr Opin Investig Drugs 10(8):766–774
Gottesman ME, Weisberg RA (2004) Little lambda, who made thee? Microbiol Mol Biol Rev 68(4):796–813. https://doi.org/10.1128/MMBR.68.4.796-813.2004
Griffith F (1928) The significance of pneumococcal types. J Hyg (Lond) 27(2):113–159
Groenen MA, van de Putte P (1985) Mapping of a site for packaging of bacteriophage Mu DNA. Virology 144(2):520–522
Hanks MC, Newman B, Oliver IR et al (1988) Packaging of transducing DNA by bacteriophage P1. Mol Gen Genet 214(3):523–532
Harel J, Duplessis L, Kahn JS et al (1990) The cis-acting DNA sequences required in vivo for bacteriophage Mu helper-mediated transposition and packaging. Arch Microbiol 154(1):67–72
Harriman PD (1972) A single-burst analysis of the production of P1 infectious and transducing particles. Virology 48(2):595–600. doi:0042-6822(72)90071-2
Harshey RM (1988) Phage Mu. In: Calendar R (ed) The bacteriophages, vol 1. Plenum Press, New York, pp 193–234
Harshey RM (2012) The Mu story: how a maverick phage moved the field forward. Mob DNA 3(1):21-8753-3-21. https://doi.org/10.1186/1759-8753-3-21
Harshey RM (2014) Transposable phage Mu. Microbiol Spectr 2(5). https://doi.org/10.1128/microbiolspec.MDNA3-0007-2014
Harshey RM, Bukhari AI (1983) Infecting bacteriophage mu DNA forms a circular DNA-protein complex. J Mol Biol 167(2):427–441
Hendrix RW, Roberts J, Stahl F et al (eds) (1983) Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor
Hendrix RW (2003) Bacteriophage genomics. Curr Opin Microbiol 6(5):506–511. doi:S1369527403001152
Hershey AD, Burgi E (1965) Complementary structure of interacting sites at the ends of lambda DNA molecules. Proc Natl Acad Sci U S A 53:325–328
Hershey AD, Burgi E, Ingraham L (1963) Cohesion of DNA molecules isolated from phage lambda. Proc Natl Acad Sci U S A 49(5):748–755
Howe MM (1973) Transduction by bacteriophage MU-1. Virology 55(1):103–117
Howe MM, Bade EG (1975) Molecular biology of bacteriophage mu. Science 190(4215):624–632
Hraiech S, Bregeon F, Rolain JM (2015) Bacteriophage-based therapy in cystic fibrosis-associated Pseudomonas aeruginosa infections: rationale and current status. Drug Des Devel Ther 9:3653–3663. https://doi.org/10.2147/DDDT.S53123
Huang H, Masters M (2014) Bacteriophage P1 pac sites inserted into the chromosome greatly increase packaging and transduction of Escherichia coli genomic DNA. Virology 468–470:274–282. https://doi.org/10.1016/j.virol.2014.07.029
Hynes AP, Mercer RG, Watton DE et al (2012) DNA packaging bias and differential expression of gene transfer agent genes within a population during production and release of the Rhodobacter capsulatus gene transfer agent, RcGTA. Mol Microbiol 85(2):314–325. https://doi.org/10.1111/j.1365-2958.2012.08113.x
Iida S, Arber W (1977) Plaque forming specialized transducing phage P1: isolation of P1CmSmSu, a precursor of P1Cm. Mol Gen Genet 153(3):259–269
Iida S, Hanni C, Echarti C et al (1981) Is the IS1-flanked r-determinant of the R plasmid NR1 a transposon? J Gen Microbiol 126(2):413–425. https://doi.org/10.1099/00221287-126-2-413
Iida S, Meyer J, Arber W (1978) The insertion element IS1 is a natural constituent of coliphage P1 DNA. Plasmid 1(3):357–365. doi:0147-619X(78)90051-3
Ikeda H, Shimizu H, Ukita T et al (1995) A novel assay for illegitimate recombination in Escherichia coli: stimulation of lambda bio transducing phage formation by ultra-violet light and its independence from RecA function. Adv Biophys 31:197–208. doi:0065227X95993923
Ikeda H, Tomizawa J (1968) Prophage P1, and extrachromosomal replication unit. Cold Spring Harb Symp Quant Biol 33:791–798
Ikeda H, Tomizawa JI (1965a) Transducing fragments in generalized transduction by phage P1. I. Molecular origin of the fragments. J Mol Biol 14(1):85–109
Ikeda H, Tomizawa JI (1965b) Transducing fragments in generalized transduction by phage P1. II. Association of DNA and protein in the fragments. J Mol Biol 14(1):110–119
Jacob F, Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318–356
Jain A, Srivastava P (2013) Broad host range plasmids. FEMS Microbiol Lett 348(2):87–96. https://doi.org/10.1111/1574-6968.12241
Kallmeyer J, Pockalny R, Adhikari RR et al (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 109(40):16213–16216. https://doi.org/10.1073/pnas.1203849109
Katz L (1970) Selection of araB and araC mutants of Escherichia coli B-r by resistance to ribitol. J Bacteriol 102(2):593–595
Kenzaka T, Tamaki S, Yamaguchi N et al (2005) Recognition of individual genes in diverse microorganisms by cycling primed in situ amplification. Appl Environ Microbiol 71(11):7236–7244. https://doi.org/10.1128/AEM.71.11.7236-7244.2005
Kenzaka T, Tani K, Nasu M (2010) High-frequency phage-mediated gene transfer in freshwater environments determined at single-cell level. ISME J 4(5):648–659. https://doi.org/10.1038/ismej.2009.145
Kenzaka T, Tani K, Sakotani A et al (2007) High-frequency phage-mediated gene transfer among Escherichia coli cells, determined at the single-cell level. Appl Environ Microbiol 73(10):3291–3299. https://doi.org/10.1128/AEM.02890-06
Klumpp J, Dorscht J, Lurz R et al (2008) The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of gram-positive bacteria. J Bacteriol 190(17):5753–5765. https://doi.org/10.1128/JB.00461-08
Knapp CW, Dolfing J, Ehlert PA et al (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44(2):580–587. https://doi.org/10.1021/es901221x
Kondo E, Mitsuhashi S (1964) Drug resistance of enteric bacteria. Iv. Active transducing bacteriophage P1 Cm produced by the combination of R factor with bacteriophage P1. J Bacteriol 88:1266–1276
Kutter E, De Vos D, Gvasalia G et al (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11(1):69–86
Kwoh DY, Kemper J (1978) Bacteriophage P22-mediated specialized transduction in Salmonella typhimurium: high frequency of aberrant prophage excision. J Virol 27(3):519–534
Lang AS, Zhaxybayeva O, Beatty JT (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol 10(7):472–482. https://doi.org/10.1038/nrmicro2802
Lederberg EM (1951) Lysogeny in E. coli K-12. Genetics 36:560
Lederberg EM, Lederberg J (1953) Genetic studies of lysogenicity in Escherichia coli. Genetics 38(1):51–64
Lederberg J, Tatum EL (1946) Gene recombination in Escherichia coli. Nature 158(4016):558
Lindahl G, Sironi G, Bialy H et al (1970) Bacteriophage lambda; abortive infection of bacteria lysogenic for phage P2. Proc Natl Acad Sci U S A 66(3):587–594
Lindsay JA, Holden MT (2006) Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Funct Integr Genomics 6(3):186–201. https://doi.org/10.1007/s10142-005-0019-7
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(2):527–543
Łobocka M, Hejnowicz MS, Gągała U et al (2014) The first step to bacteriophage therapy – how to choose the correct phage. In: Borysowski J, Międzybrodzki R, Górski A (eds) Phage therapy: current research and applications. Caister Academic Press, Norfolk, pp 23–67
Lobocka MB, Rose DJ, Plunkett G 3rd et al (2004) Genome of bacteriophage P1. J Bacteriol 186(21):7032–7068. https://doi.org/10.1128/JB.186.21.7032-7068.2004
Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1(2):111–114. https://doi.org/10.4161/bact.1.2.14590
Lu SD, Lu D, Gottesman M (1989) Stimulation of IS1 excision by bacteriophage P1 ref function. J Bacteriol 171(6):3427–3432
Maiques E, Ubeda C, Campoy S et al (2006) beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J Bacteriol 188(7):2726–2729. https://doi.org/10.1128/JB.188.7.2726-2729.2006
Marrs B (1974) Genetic recombination in Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A 71(3):971–973
Marti E, Variatza E, Balcazar JL (2014a) Bacteriophages as a reservoir of extended-spectrum beta-lactamase and fluoroquinolone resistance genes in the environment. Clin Microbiol Infect 20(7):O456-9. https://doi.org/10.1111/1469-0691.12446
Marti E, Variatza E, Balcazar JL (2014b) The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol 22(1):36–41. https://doi.org/10.1016/j.tim.2013.11.001
Masters M (1977) The frequency of P1 transduction of the genes of Escherichia coli as a function of chromosomal position: preferential transduction of the origin of replication. Mol Gen Genet 155(2):197–202
Masters M (1996) Generalized transduction. In: Neidhardt FC, Curtiss R III, Ingraham JJ et al (eds) Escherichia coli and salmonella typhimurium: cellular and molecular biology, 2nd edn. American Society for Microbiology, Washington DC, pp 2421–2448
Masters M (2004) Transduction: host DNA transfer by bacteriophages. In: Schaechter M (ed) The desk encyclopedia of microbiology. Elsevier/Academic Press, London, pp 1000–1012
McDaniel LD, Young EC, Ritchie KB et al (2012) Environmental factors influencing gene transfer agent (GTA) mediated transduction in the subtropical ocean. PLoS One 7(8):e43506. https://doi.org/10.1371/journal.pone.0043506
Mise K, Arber W (1976) Plaque-forming transducing bacteriophage P1 derivatives and their behaviour in lysogenic conditions. Virology 69(1):191–205. doi:0042-6822(76)90206-3
Morse ML, Lederberg EM, Lederberg J (1956a) Transduction in Escherichia coli K-12. Genetics 41(1):142–156
Morse ML, Lederberg EM, Lederberg J (1956b) Transductional heterogenotes in Escherichia coli. Genetics 41(5):758–779
Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2–9
Nash HA (1981) Integration and excision of bacteriophage lambda: the mechanism of conservation site specific recombination. Annu Rev Genet 15:143–167. https://doi.org/10.1146/annurev.ge.15.120181.001043
Newman BJ, Masters M (1980) The variation in frequency with which markers are transduced by phage P1 is primarily a result of discrimination during recombination. Mol Gen Genet 180(3):585–589
Novick RP (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49(2):93–105. doi:S0147619X02001579
Novick RP, Ram G (2016) The Floating (Pathogenicity) Island: A Genomic Dessert. Trends Genet 32(2):114–126. https://doi.org/10.1016/j.tig.2015.11.005
Paul JH (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2(6):579–589. https://doi.org/10.1038/ismej.2008.35
Pedulla ML, Ford ME, Houtz JM et al (2003) Origins of highly mosaic mycobacteriophage genomes. Cell 113(2):171–182. doi:S0092867403002332
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
Penades JR, Christie GE (2015) The phage-inducible chromosomal Islands: a family of highly evolved molecular parasites. Annu Rev Virol 2(1):181–201. https://doi.org/10.1146/annurev-virology-031413-085446
Perron GG, Whyte L, Turnbaugh PJ et al (2015) Functional characterization of bacteria isolated from ancient arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLoS One 10(3):e0069533. https://doi.org/10.1371/journal.pone.0069533
Perry J, Waglechner N, Wright G (2016) The prehistory of antibiotic resistance. Cold Spring Harb Perspect Med 6(6). https://doi.org/10.1101/cshperspect.a025197
Perry JA, Westman EL, Wright GD (2014) The antibiotic resistome: what's new? Curr Opin Microbiol 21:45–50. https://doi.org/10.1016/j.mib.2014.09.002
Petrova M, Gorlenko Z, Mindlin S (2009) Molecular structure and translocation of a multiple antibiotic resistance region of a Psychrobacter psychrophilus permafrost strain. FEMS Microbiol Lett 296(2):190–197. https://doi.org/10.1111/j.1574-6968.2009.01635.x
Poteete AR (1988) Bacteriophage P22. In: Calendar R (ed) The bacteriophages, vol 2. Plenum Press, New York, pp 647–681
Puspurs AH, Trun NJ, Reeve JN (1983) Bacteriophage Mu DNA circularizes following infection of Escherichia coli. EMBO J 2(3):345–352
Quiles-Puchalt N, Carpena N, Alonso JC et al (2014a) Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. Proc Natl Acad Sci U S A 111(16):6016–6021. https://doi.org/10.1073/pnas.1320538111
Quiles-Puchalt N, Martinez-Rubio R, Ram G et al (2014b) Unravelling bacteriophage varphi11 requirements for packaging and transfer of mobile genetic elements in Staphylococcus aureus. Mol Microbiol 91(3):423–437. https://doi.org/10.1111/mmi.12445
Ram G, Chen J, Kumar K et al (2012) Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. Proc Natl Acad Sci U S A 109(40):16300–16305. https://doi.org/10.1073/pnas.1204615109
Ram G, Chen J, Ross HF et al (2014) Precisely modulated pathogenicity island interference with late phage gene transcription. Proc Natl Acad Sci U S A 111(40):14536–14541. https://doi.org/10.1073/pnas.1406749111
Raya RR, H'bert EM (2009) Isolation of phage via induction of lysogens. Methods Mol Biol 501:23–32. https://doi.org/10.1007/978-1-60327-164-6_3
Reyes A, Haynes M, Hanson N et al (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466(7304):334–338. https://doi.org/10.1038/nature09199
Roberts JW, Devoret R (1983) Lysogenic induction. In: Hendrix RW, Roberts JW, Stahl FW et al (eds) Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 123–144
Roberts MD, Drexler H (1981a) Isolation and genetic characterization of T1-transducing mutants with increased transduction frequency. Virology 112(2):662–669
Roberts MD, Drexler H (1981b) T1 mutants with increased transduction frequency are defective in host chromosome degradation. Virology 112(2):670–677
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
Rutkai E, Gyorgy A, Dorgai L et al (2006) Role of secondary attachment sites in changing the specificity of site-specific recombination. J Bacteriol 188(9):3409–3411. https://doi.org/10.1128/JB.188.9.3409-3411.2006
Ruzin A, Lindsay J, Novick RP (2001) Molecular genetics of SaPI1–a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol 41(2):365–377. doi:mmi2488
Sander M, Schmieger H (2001) Method for Host-Independent Detection of Generalized Transducing Bacteriophages in Natural Habitats. Appl Environ Microbiol 67(4):1490–3
Sandri RM, Berger H (1980) Bacteriophage P1-mediated generalized transduction in Escherichia coli: fate of transduced DNA in rec+ and recA- recipients. Virology 106(1):14–29
Sandulache R, Prehm P, Kamp D (1984) Cell wall receptor for bacteriophage Mu G(+). J Bacteriol 160(1):299–303
Sarker SA, McCallin S, Barretto C et al (2012) Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology 434(2):222–232. https://doi.org/10.1016/j.virol.2012.09.002
Sato K, Campbell A (1970) Specialized transduction of galactose by lambda phage from a deletion lysogen. Virology 41(3):474–487. doi:0042-6822(70)90169-8
Schmieger H (1970) The molecular structure of the transducing particles of Salmonella phage P22. II. Density gradient analysis of DNA. Mol Gen Genet 109(4):323–337
Schmieger H (1972) Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119(1):75–88
Schroeder W, Bade EG, Delius H (1974) Participation of Escherichia coli DNA in the replication of temperate bacteriophage Mu1. Virology 60(2):534–542
Segev N, Laub A, Cohen G (1980) A circular form of bacteriophage P1 DNA made in lytically infected cells of Escherichia coli. Characterization and kinetics of formation. Virology 101(1):261–271
Servick K (2016) DRUG DEVELOPMENT. Beleaguered phage therapy trial presses on. Science 352(6293):1506. https://doi.org/10.1126/science.352.6293.1506
Shanado Y, Kato J, Ikeda H (1997) Fis is required for illegitimate recombination during formation of lambda bio transducing phage. J Bacteriol 179(13):4239–4245
Shimada K, Weisberg RA, Gottesman ME (1972) Prophage lambda at unusual chromosomal locations. I. Location of the secondary attachment sites and the properties of the lysogens. J Mol Biol 63(3):483–503. doi:0022-2836(72)90443-3
Shimada K, Weisberg RA, Gottesman ME (1973) Prophage lambda at unusual chromosomal locations. II. Mutations induced by bacteriophage lambda in Escherichia coli K12. J Mol Biol 80(2):297–314. doi:0022-2836(73)90174-5
Shimada K, Weisberg RA, Gottesman ME (1975) Prophage lambda at unusual chromosomal locations. III. The components of the secondary attachment sites. J Mol Biol 93(4):415–429. doi:0022-2836(75)90237-5
Skurnik M, Pajunen M, Kiljunen S (2007) Biotechnological challenges of phage therapy. Biotechnol Lett 29(7):995–1003. https://doi.org/10.1007/s10529-007-9346-1
Smith HW (1972) Ampicillin resistance in Escherichia coli by phage infection. Nat New Biol 238(85):205–206
Sternberg N (1986) The production of generalized transducing phage by bacteriophage lambda. Gene 50(1–3):69–85. doi:0378-1119(86)90311-2
Sternberg N (1990) Bacteriophage P1 cloning system for the isolation, amplification, and recovery of DNA fragments as large as 100 kilobase pairs. Proc Natl Acad Sci U S A 87(1):103–107
Sternberg N, Cohen G (1989) Genetic analysis of the lytic replicon of bacteriophage P1. II. Organization of replicon elements. J Mol Biol 207(1):111–133. doi:0022-2836(89)90444-0
Sternberg N, Coulby J (1987) Recognition and cleavage of the bacteriophage P1 packaging site (pac). II. Functional limits of pac and location of pac cleavage termini. J Mol Biol 194(3):469–479. doi:0022-2836(87)90675-9
Sternberg N, Hoess R (1983) The molecular genetics of bacteriophage P1. Annu Rev Genet 17:123–154. https://doi.org/10.1146/annurev.ge.17.120183.001011
Sternberg N, Weisberg R (1975) Packaging of prophage and host DNA by coliphage lambda. Nature 256(5513):97–103
Sternberg NL, Maurer R (1991) Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol 204:18–43. doi:0076-6879(91)04004-8
Streisinger G, Emrich J, Stahl MM (1967) Chromosome structure in phage t4, iii. Terminal redundancy and length determination. Proc Natl Acad Sci U S A 57(2):292–295
Stresinger G, Edgar RS, Denhardt GH (1964) Chromosome structure in phage T4. I. Circularity of the linkage map. Proc Natl Acad Sci U S A 51:775–779
Sulakvelidze A, Alavidze Z, Morris JG Jr (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45(3):649–659. https://doi.org/10.1128/AAC.45.3.649-659.2001
Susskind MM, Botstein D (1978) Molecular genetics of bacteriophage P22. Microbiol Rev 42(2):385–413
Takahaski S (1975) Physiological transition of a coliphage lambda DNA replication. Biochim Biophys Acta 395(3):306–313
Tavares P, Zinn-Justin S, Orlova EV (2012) Genome gating in tailed bacteriophage capsids. Adv Exp Med Biol 726:585–600. https://doi.org/10.1007/978-1-4614-0980-9_25
Taylor AL (1963) Bacteriophage-Induced Mutation in Escherichia Coli. Proc Natl Acad Sci U S A 50:1043–1051
Thiel K (2004) Old dogma, new tricks–21st Century phage therapy. Nat Biotechnol 22(1):31–36. https://doi.org/10.1038/nbt0104-31
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
Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3(9):711–721. https://doi.org/10.1038/nrmicro1234
Thurber RV, Haynes M, Breitbart M et al (2009) Laboratory procedures to generate viral metagenomes. Nat Protoc 4(4):470–483. https://doi.org/10.1038/nprot.2009.10
Tormo MA, Ferrer MD, Maiques E et al (2008) Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J Bacteriol 190(7):2434–2440. https://doi.org/10.1128/JB.01349-07
Tye BK, Huberman JA, Botstein D (1974) Non-random circular permutation of phage P22 DNA. J Mol Biol 85(4):501–528. doi:0022-2836(74)90312-X
Ubeda C, Maiques E, Barry P et al (2008) SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol Microbiol 67(3):493–503. https://doi.org/10.1111/j.1365-2958.2007.06027.x
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(3):836–844. https://doi.org/10.1111/j.1365-2958.2005.04584.x
Ubeda C, Maiques E, Tormo MA et al (2007) SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol Microbiol 65(1):41–50. https://doi.org/10.1111/j.1365-2958.2007.05758.x
van Schaik W (2015) The human gut resistome. Philos Trans R Soc Lond Ser B Biol Sci 370(1670):20140087. https://doi.org/10.1098/rstb.2014.0087
Varga M, Kuntova L, Pantucek R et al (2012) Efficient transfer of antibiotic resistance plasmids by transduction within methicillin-resistant Staphylococcus aureus USA300 clone. FEMS Microbiol Lett 332(2):146–152. https://doi.org/10.1111/j.1574-6968.2012.02589.x
Viertel TM, Ritter K, Horz HP (2014) Viruses versus bacteria-novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J Antimicrob Chemother 69(9):2326–2336. https://doi.org/10.1093/jac/dku173
von Wintersdorff CJ, Penders J, van Niekerk JM et al (2016) Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front Microbiol 7:173. https://doi.org/10.3389/fmicb.2016.00173
Waddell TE, Franklin K, Mazzocco A et al (2009) Generalized transduction by lytic bacteriophages. Methods Mol Biol 501:293–303. https://doi.org/10.1007/978-1-60327-164-6_25
Wang BM, Liu L, Groisman EA et al (1987) High frequency generalized transduction by miniMu plasmid phage. Genetics 116(2):201–206
Weber-Dabrowska B, Jonczyk-Matysiak E, Zaczek M et al (2016) Bacteriophage procurement for therapeutic purposes. Front Microbiol 7:1177. https://doi.org/10.3389/fmicb.2016.01177
Weigle J, Meselson M, Paigen K (1959) Density alterations associated with transducing ability in bacteriophage lambda. J Mol Biol 1:379
Weigle JJ, Bertani G (1953) Variations of bacteriophage conditioned by host bacteria. Ann Inst Pasteur (Paris) 84(1):175–179
Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6(1):1–11. doi:539 [pii]
Weisberg RA (1987) Specialized transduction. In: Niedhardt FC (ed) Escherichia coli and Salmonella: cellular and molecular biology, 1st edn. American Society for Microbiology, Washington DC, pp 1169–1176
Weisberg RA (1996) Specialized transduction. In: Neidhardt FC (ed) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn, vol 2. ASM Press, Washington DC, pp 2442–2448
Weisberg RA, Gottesman ME (1969) The integration and excision defect of bacteriophage lambda-dg. J Mol Biol 46(3):565–580. doi:0022-2836(69)90196-X
Wilson GG, Young KY, Edlin GJ et al (1979) High-frequency generalised transduction by bacteriophage T4. Nature 280(5717):80–82
Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5(1):226–235. https://doi.org/10.4161/viru.25991
Wolf RE Jr (1980) Integration of specialized transducing bacteriophage lambda cI857 St68 h80 dgnd his by an unusual pathway promotes formation of deletions and generates a new translocatable element. J Bacteriol 142(2):588–602
Wollman EL (1953) Sur le déterminisme génétique de la lysogénie. Ann. Inst. Pasteur (Paris) 84:281–293
Wollman EL, Jacob F, Hayes W (1956) Conjugation and genetic recombination in Escherichia coli K-12. Cold Spring Harb Symp Quant Biol 21:141–162
Wu H, Sampson L, Parr R et al (2002) The DNA site utilized by bacteriophage P22 for initiation of DNA packaging. Mol Microbiol 45(6):1631–1646. doi:3114 [pii]
Yarmolinsky MB, Sternberg N (1988) Bacteriophage P1. In: Calendar R (ed) The bacteriophages, vol 1. Plenum Publishing Corporation, New York, pp 291–438
Yen HC, Hu NT, Marrs BL (1979) Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata. J Mol Biol 131(2):157–168. doi:0022-2836(79)90071-8
Young KK, Edlin GJ, Wilson GG (1982) Genetic analysis of bacteriophage T4 transducing bacteriophages. J Virol 41(1):345–347
Young R, Gill JJ (2015) MICROBIOLOGY. Phage therapy redux–what is to be done? Science 350(6265):1163–1164. https://doi.org/10.1126/science.aad6791
Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. J Bacteriol 64(5):679–699
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this entry
Cite this entry
Schneider, C.L. (2021). Bacteriophage-Mediated Horizontal Gene Transfer: Transduction. In: Harper, D.R., Abedon, S.T., Burrowes, B.H., McConville, M.L. (eds) Bacteriophages. Springer, Cham. https://doi.org/10.1007/978-3-319-41986-2_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-41986-2_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-41985-5
Online ISBN: 978-3-319-41986-2
eBook Packages: Biomedical and Life SciencesReference Module Biomedical and Life Sciences