Research article

Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli

  • Received: 20 July 2017 Accepted: 28 September 2017 Published: 10 October 2017
  • Bacteria undergo horizontal gene transfer via various mechanisms. We recently reported that cell-to-cell transfer of nonconjugative plasmids occurs between strains of Escherichia coli in co-cultures, and that a specific strain (CAG18439) causes frequent plasmid transfer involving a DNase-sensitive mechanism, which we termed “cell-to-cell transformation”. Here we found that CAG18439 is a type of P1 bacteriophage lysogen that continuously releases phages. We tested the ability of P1vir bacteriophage to induce horizontal plasmid transfer and demonstrated that such a horizontal plasmid transfer was caused by adding culture supernatants of P1vir-infected cells harboring plasmids to other plasmid-free cells. This plasmid transfer system also reproduced the major features of plasmid transfer involving CAG18439, suggesting that P1vir-induced plasmid transfer is equivalent or very similar to plasmid transfer involving CAG18439. We further revealed that approximately two-thirds of the P1vir-induced plasmid transfer was DNase-sensitive, but that complete abolition of plasmid transfer was observed when proteins were denatured or removed, despite the presence or absence of DNase. Therefore, we concluded that P1vir-induced plasmid transfer is largely due to the occurrence of cell-to-cell transformation, which involves the assistance of some proteinaceous factor, and partly due to the occurrence of plasmid transduction, which is mediated by phage virions. This is the first demonstration of the P1-phage-induced cell-to-cell transformation.

    Citation: Chiaki Sugiura, Saki Miyaue, Yuka Shibata, Akiko Matsumoto, Sumio Maeda. Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli[J]. AIMS Microbiology, 2017, 3(4): 784-797. doi: 10.3934/microbiol.2017.4.784

    Related Papers:

  • Bacteria undergo horizontal gene transfer via various mechanisms. We recently reported that cell-to-cell transfer of nonconjugative plasmids occurs between strains of Escherichia coli in co-cultures, and that a specific strain (CAG18439) causes frequent plasmid transfer involving a DNase-sensitive mechanism, which we termed “cell-to-cell transformation”. Here we found that CAG18439 is a type of P1 bacteriophage lysogen that continuously releases phages. We tested the ability of P1vir bacteriophage to induce horizontal plasmid transfer and demonstrated that such a horizontal plasmid transfer was caused by adding culture supernatants of P1vir-infected cells harboring plasmids to other plasmid-free cells. This plasmid transfer system also reproduced the major features of plasmid transfer involving CAG18439, suggesting that P1vir-induced plasmid transfer is equivalent or very similar to plasmid transfer involving CAG18439. We further revealed that approximately two-thirds of the P1vir-induced plasmid transfer was DNase-sensitive, but that complete abolition of plasmid transfer was observed when proteins were denatured or removed, despite the presence or absence of DNase. Therefore, we concluded that P1vir-induced plasmid transfer is largely due to the occurrence of cell-to-cell transformation, which involves the assistance of some proteinaceous factor, and partly due to the occurrence of plasmid transduction, which is mediated by phage virions. This is the first demonstration of the P1-phage-induced cell-to-cell transformation.


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    [1] Bushman F (2002) Lateral DNA Transfer, New York: Cold Spring Harbor.
    [2] Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural transformation in the environment. Microbiol Rev 58: 563–602.
    [3] Richards TA, Archibald JM (2011) Cell evolution: gene transfer agents and the origin of mitochondria. Curr Biol 21: R112–R114. doi: 10.1016/j.cub.2010.12.036
    [4] Yaron S, Kolling GL, Simon L, et al. (2000) Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microb 66: 4414–4420. doi: 10.1128/AEM.66.10.4414-4420.2000
    [5] Ishimoto Y, Kato S, Maeda S (2008) Freeze-thaw-induced lateral transfer of non-conjugative plasmids by in situ transformation in Escherichia coli in natural waters and food extracts. World J Microbiol Biotechnol 24: 2731–2735. doi: 10.1007/s11274-008-9761-z
    [6] Calender R (2006) The Bacteriophages, 2 Eds., New York: Oxford University Press.
    [7] Dagert M, Jones I, Goze A, et al. (1984) Replication functions of pC194 are necessary for efficient plasmid transduction by M13 phage. EMBO J 3: 81–86.
    [8] Schmidt C, Schmieger H (1984) Selective transduction of recombinant plasmids with cloned pac sites by Salmonella phage P22. Mol Gen Genet 196: 123–128. doi: 10.1007/BF00334103
    [9] Iida S, Meyer J, Arber W (1981) Cointegrates between bacteriophage P1 DNA and plasmid pBR322 derivatives suggest molecular mechanisms for P1-mediated transduction of small plasmids. Mol Gen Genet 184: 1–10. doi: 10.1007/BF00271186
    [10] Kittleson JT, DeLoache W, Cheng HY, et al. (2012) Scalable plasmid transfer using engineered P1-based phagemids. ACS Synth Biol 1: 583–589. doi: 10.1021/sb300054p
    [11] Salmond GP, Fineran PC (2015) A century of the phage: past, present and future. Nat Rev Microbiol 13: 777–786. doi: 10.1038/nrmicro3564
    [12] Branda SS, Vik A, Friedman L, et al. (2005) Biofilms: the matrix revisited. Trends Microbiol 13: 20–26. doi: 10.1016/j.tim.2004.11.006
    [13] Ando T, Itakura S, Uchii K, et al. (2009) Horizontal transfer of non-conjugative plasmid in colony biofilm of Escherichia coli on food-based media. World J Microbiol Biotechnol 25: 1865–1869. doi: 10.1007/s11274-009-0070-y
    [14] Maeda S, Ito M, Ando T, et al. (2006) Horizontal transfer of nonconjugative plasmids in a colony biofilm of Escherichia coli. FEMS Microbiol Lett 255: 115–120. doi: 10.1111/j.1574-6968.2005.00072.x
    [15] Etchuuya R, Ito M, Kitano S, et al. (2011) Cell-to-cell transformation in Escherichia coli: a novel type of natural transformation involving cell-derived DNA and a putative promoting pheromone. PLoS One 6: e16355. doi: 10.1371/journal.pone.0016355
    [16] Sobue R, Kurono N, Etchuya R, et al. (2011) Identification of a novel DNA element that promotes cell-to-cell transformation in Escherichia coli. FEBS Lett 585: 2223–2228. doi: 10.1016/j.febslet.2011.05.040
    [17] Kurono N, Matsuda A, Etchuya R, et al. (2012) Genome-wide screening of Escherichia coli genes involved in execution and promotion of cell-to-cell transfer of non-conjugative plasmids: rodZ (yfgA) is essential for plasmid acceptance in recipient cells. Biochem Bioph Res Co 421: 119–123. doi: 10.1016/j.bbrc.2012.03.127
    [18] Matsuda A, Kurono N, Kawano C, et al. (2012) Genome-wide screen for Escherichia coli genes involved in repressing cell-to-cell transfer of non-conjugative plasmids. Biochem Bioph Res Co 482: 445–450.
    [19] Shibata Y, Matsumoto A, Horino M, et al. (2014) Genome-wide screen for Escherichia coli genes involved in repressing cell-to-cell transfer of a nonconjugative pSC101-derived plasmid. Am J Life Sci 2: 345–350. doi: 10.11648/j.ajls.20140206.13
    [20] Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557–580. doi: 10.1016/S0022-2836(83)80284-8
    [21] Bachmann BJ (1996) Derivations and genotypes of some mutant derivatives of Escherichia coli K-12, In: Neidhardt FC, Curtiss R, Ingraham JL, et al., Escherichia coli and Salmonella: cellular and molecular biology, 2 Eds., Washington: ASM Press, 2460–2488.
    [22] Boyer HW, Roulland-Dussoix D (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41: 459–472. doi: 10.1016/0022-2836(69)90288-5
    [23] Casadaban MJ (1976) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104: 541–555. doi: 10.1016/0022-2836(76)90119-4
    [24] Singer M, Baker TA, Schnitzler G, et al. (1989) A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev 53: 6408–6411.
    [25] Baba T, Ara T, Hasegawa M, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
    [26] Takeshita S, Sato M, Toba M, et al. (1987) High-copy-number and low-copy-number plasmid vectors for lacZα-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61: 63–74. doi: 10.1016/0378-1119(87)90365-9
    [27] Cohen G, Zimmer Z (1974) Transfection of Escherichia coli by Bacteriophage P1 DNA. Mol Gen Genet 128: 183–186. doi: 10.1007/BF02654490
    [28] Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: a Laboratory Manual, 2 Eds., New York: Cold Spring Harbor.
    [29] Ikeda H, Tomizawa JI (1965) Transducing fragments in generalized transduction by phage P1: I. Molecular origin of the fragments. J Mol Biol 14: 85–109.
    [30] Matsumoto A, Sekoguchi A, Imai J, et al. (2016) Natural Escherichia coli strains undergo cell-to-cell plasmid transformation. Biochem Bioph Res Co 481: 59–62. doi: 10.1016/j.bbrc.2016.11.018
    [31] Shibata Y, Ugumori C, Takahashi A, et al. (2014) Survey of lysogenic phages in the 72 strains of Escherichia coli collection of reference (ECOR) and identification of a phage derived from the ECOR52 strain. Am J Biosci 2: 32–37.
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