Genome-Wide Screen for Escherichia coli Genes Involved in Repressing Cell-To-Cell Transfer of a Nonconjugative pSC101-Derived Plasmid
American Journal of Life Sciences
Volume 2, Issue 6, December 2014, Pages: 345-350
Received: Nov. 5, 2014; Accepted: Nov. 18, 2014; Published: Nov. 21, 2014
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Authors
Yuka Shibata, Graduate School of Humanities and Sciences, Nara Women's University, Nara, Japan
Akiko Matsumoto, Graduate School of Humanities and Sciences, Nara Women's University, Nara, Japan
Mutsumi Horino, Faculty of Human Life and Environment, Nara Women's University, Nara, Japan
Akiko Hirabayashi, Faculty of Human Life and Environment, Nara Women's University, Nara, Japan
Kozue Shirota, Faculty of Human Life and Environment, Nara Women's University, Nara, Japan
Chinatsu Kawano, Faculty of Human Life and Environment, Nara Women's University, Nara, Japan
Sumio Maeda, Graduate School of Humanities and Sciences, Nara Women's University, Nara, Japan; Faculty of Human Life and Environment, Nara Women's University, Nara, Japan
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Abstract
Acquiring new genetic traits by lateral gene transfer is a bacterial strategy for environmental adaptations. We previously showed that Escherichia coli laterally transmits nonconjugative plasmids in cocultures that contain strains with or without the plasmid. Using a pMB1-derived plasmid and the Keio collection, a comprehensive library of E. coli knockout mutants for nonessential genes, we recently screened for genes responsible for promoting or repressing cell-to-cell plasmid transfer in recipient cells. In this study, we used a pSC101-derived plasmid, instead of a pMB1-derived plasmid, to screen for repressing genes and identified 29 “transfer-up” mutants. Among these, four mutants are common to those previously screened using a pMB1-derived plasmid. Although the roles of the 29 gene products in plasmid transfer mechanism remain uncertain, it is interesting that 28 of the 29 screened genes map to two limited regions on the E. coli chromosome: 18 genes at 34.25–35.31 min and 10 genes at 12.62–13.35 min. Because these two regions commonly contain termination (Ter) sites for DNA replication (TerC: 34.64 min and TerH: 12.91 min), it is possible that chromosomal mutations around specific Ter sites may affect plasmid acquisition in the recipient cells.
Keywords
Lateral Gene Transfer, Keio Collection, pSC101-Derived Plasmid, Ter Site, Escherichia coli
To cite this article
Yuka Shibata, Akiko Matsumoto, Mutsumi Horino, Akiko Hirabayashi, Kozue Shirota, Chinatsu Kawano, Sumio Maeda, Genome-Wide Screen for Escherichia coli Genes Involved in Repressing Cell-To-Cell Transfer of a Nonconjugative pSC101-Derived Plasmid, American Journal of Life Sciences. Vol. 2, No. 6, 2014, pp. 345-350. doi: 10.11648/j.ajls.20140206.13
References
[1]
F. Bushman, Lateral DNA Transfer, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 2002.
[2]
M. G. Lorenz and W. Wackernagel, “Bacterial gene transfer by natural transformation in the environment,” Microbiol Rev, vol. 58, pp. 563–602, 1994.
[3]
C. M. Thomas and K. M. Nielsen, “Mechanisms of, and barriers to, horizontal gene transfer between bacteria,” Nat Rev Microbiol, vol. 9, pp. 711–721, 2005.
[4]
P. S. Duggan, P. A. Chambers, J. Heritage, and J. M. Forbes, “Survival of free DNA encoding antibiotic resistance from transgenic maize and the transformation activity of DNA in ovine saliva, ovine rumen fluid and silage effluent,” FEMS Microbiol Lett, vol. 191, pp. 71–77, 2000.
[5]
P. Keese, “Risks from GMOs due to horizontal gene transfer,” Environ Biosafety Res, vol. 7, pp. 123–149, 2008.
[6]
B. G. Kelly, A. Vespermann, and D. J. Bolton, “Gene transfer events and their occurrence in selected environments,” Food Chem Toxicol doi:10.1016/j.fct.2008.06.012, 2008.
[7]
B. G. Kelly, A. Vespermann, and D. J. Bolton, “Horizontal gene transfer of virulence determinants in selected bacterial foodborne pathogens,” Food Chem Toxicol doi:10.1016/j.fct.2008.02.007, 2008.
[8]
A. Pontiroli, A. Rizzi, P. Simonet, D. Daffonchio, T. M. Vogel, and J. M. Mnier, “Visual evidence of horizontal gene transfer between plants and bacteria in the phytosphere of transplastomic Tobacco,” Appl Environ Microbiol, vol. 75, pp. 3314–3322, 2009.
[9]
I. Chen and D. Dubnau, “DNA uptake during bacterial trans formation,” Nat Rev Microbiol, vol. 3, pp. 241–249, 2004
[10]
D. Dubnau, “DNA uptake in bacteria,” Annu Rev Microbiol, vol. 53, pp. 217–244, 1999.
[11]
D. Hanahan, “Studies on transformation of Escherichia coli with plasmids,” J Mol Biol, vol. 166, pp. 557–580, 1983.
[12]
M. Mandel and A. Higa, “Calcium-dependent bacteriophage DNA infection.” J Mol Biol, vol. 53, pp. 159–162, 1970.
[13]
F. Bauer, C. Hertel, and W. P. Hammes, “Transformation of Escherichia coli in foodstuffs,” Syst Appl Microbiol, vol. 22, pp. 161–168, 1999.
[14]
B. Baur, K. Hanselmann, W. Schlimme, and B. Jenni, “Genetic transformation in freshwater: Escherichia coli is able to develop natural competence,” Appl Environ Microbiol, vol. 62, pp. 3673–3678, 1996.
[15]
Y. Ishimoto, S. Kato, and S. Maeda, “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, vol. 24, pp. 2731–2735, 2008.
[16]
S. Maeda, N. Kakihara, and Y. Koishi, “Competency development of Escherichia coli in foodstuffs,” Microbes Environ, vol. 18, 100–103, 2003.
[17]
S. Maeda, A. Sawamura, and A. Matsuda, “Transformation of colonial Escherichia coli on solid media,” FEMS Microbiol Lett, vol. 236, pp. 61–64, 2004.
[18]
D. Sun, Y. Zhang, Y. Mei, H. Jiang, Z. Xie, H. Liu, X. Chen, and P. Shen, “Escherichia coli is naturally transformable in a novel transformation system,” FEMS Microbiol Lett, vol. 265, pp. 249–255, 2006.
[19]
S. D. Tsen, S. S. Fang, M. J. Chen, J. Y. Chien, C. C. Lee, and D. H. Tsen, “Natural plasmid transformation in Escherichia coli,” J Biomed Sci, vol. 9, pp. 246–252, 2002.
[20]
M. Woegerbauer, B. Jenni, F. Thalhammer, W. Graninger, and M. Burgmann, “Natural genetic transformation of clinical isolates of Escherichia coli in urine and water,” Appl Environ Micobiol, vol. 68, pp. 440–443, 2002.
[21]
S. Maeda, M. Ito, T. Ando, Y. Ishimoto, Y. Fujisawa, H. Takahashi, A. Matsuda, A. Sawamura, and S. Kato, “Horizontal transfer of nonconjugative plasmids in a colony biofilm of Escherichia coli,” FEMS Microbiol Lett, vol. 255, pp. 115–120, 2006.
[22]
T. Ando, S. Itakura, K. Uchii, R. Sobue, and S. Maeda, “Horizontal transfer of non-conjugative plasmid in colony biofilm of Escherichia coli on food-based media,” World J Microbiol Biotechnol, vol. 25, pp. 1865–1869, 2009.
[23]
R. Etchuuya, M. Ito, S. Kitano, F. Shigi, R. Sobue, and S. Maeda, “Cell-to-cell transformation in Escherichia coli: a novel type of natural transformation involving cell-derived DNA and a putative promoting pheromone, PLoS ONE, vol. 6, e16355, 2011.
[24]
N. Kurono, A. Matsuda, R. Etchuya, R. Sobue, Y. Sasaki, M. Ito, T. Ando, and S. Maeda, “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 Biophys Res Commun, vol. 421, pp. 119–123, 2012.
[25]
A. Matsuda, N. Kurono, C. Kawano, K. Shirota, A. Hirabayashi, M. Horino, R. Etchuya, R. Sobue, Y. Sasaki, S. Miyaue, A. Sekoguchi, C. Sugiura, Y. Shibata, M. Ito, T. Ando, and S. Maeda, “Genome-wide screen for Escherichia coli genes involved in repressing cell-to-cell transfer of non-conjugative plasmids,” Biochem Biophys Res Commun, vol. 482, pp. 445–450, 2012.
[26]
T. Baba, T. Ara, H. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. Datsenko, M. Tomita, B. L. Wanner, and H. Mori, “Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection,” Mol Syst Biol, vol. 2, 2006.0008, 2006.
[27]
T. Inoue, R. Shingaki, S. Hirose, K. Waki, H. Mori, and K. Fukui, “Genome-wide screening of genes required for swarming motility in Escherichia coli K-12,” J Bacteriol, vol. 189, pp. 950–957, 2007.
[28]
V. Sanchez-Torres, T. Maeda, and T. K. Wood, “Global regulator H-NS and lipoprotein NlpI influence production of extracellular DNA in Escherichia coli,” Biochem Biophys Res Commun, vol. 401, pp. 197–202, 2010.
[29]
O. Sharma, K. A. Datsenko, S. C. Ess, M. V. Zhalnina, B. L. Wanner, and W. A. Cramer, “Genome-wide screens: novel mechanisms in colicin import and cytotoxicity,” Mol Microbiol, vol. 73, pp. 571–585, 2009.
[30]
D. Manen, M. Pougeon, P. Damay, and J. J. Geiselmann, “A sensitive reporter gene system using bacterial luciferase based on a series of plasmid cloning vectors compatible with derivatives of pBR322,” Gene, vol. 186, pp. 197–200, 1997.
[31]
R. Sobue, N. Kurono, R. Etchuya, and S. Maeda, “Identification of a novel DNA element that promotes cell-to-cell transformation in Escherichia coli,” FEBS Lett, vol. 585, pp. 2223–2228, 2011.
[32]
M. Singer, T. A. Baker, G. Schnitzler, S. M. Deischel, M. Goel, W. Dove, K. J. Jaacks, A. D. Grossman, J. W. Erickson, and C. A. Gross, “A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli,” Microbiol Rev, vol. 53, pp. 6408–6411, 1989.
[33]
J. Sambrook, E. F. Fritsch, and T. Maniatis, Molecular Cloning: a Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 1989.
[34]
T. L. Povolotsky and R. Hengge, “Life-style' control networks in Escherichia coli: signaling by the second messenger c-di-GMP,” J Biotechnol, vol. 160, pp. 10–16, 2012.
[35]
H. Sondermann, N. J. Shikuma, and F. H. Yildiz, “You've come a long way: c-di-GMP signaling,” Curr Opin Microbiol, vol. 15, pp. 140–146, 2012.
[36]
W. R. Galloway, J. T. Hodgkinson, S. D. Bowden, M. Welch, and D. R. Spring, “Quorum sensing in Gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways,” Chem Rev, vol. 111, pp. 28–67, 2011.
[37]
C. S. Pereira, J. A. Thompson, and K. B. Xavier, “AI-2-mediated signalling in bacteria,” FEMS Microbiol Rev, vol. 37, 156–181, 2013.
[38]
E. Esnault, M. Valens, O. Espe´ li, and F. Boccard, “Chromosome structuring limits genome plasticity in Escherichia coli,” PLoS Genet, vol. 3, e226, 2007.
[39]
C. Neylon, A. V. Kralicek, T. M. Hill, and N. E. Dixon, “Replication termination in Escherichia coli: structure and antihelicase activity of the Tus-Ter complex,” Microbiol Mol Biol Rev, vol. 69, pp. 501–526, 2005.
[40]
A. Thiel, M. Valens, I. Vallet-Gely, O. Espeli, and F. Boccard, “Long-range chromosome organization in E. coli: a site-specific system isolates the Ter macrodomain,” PLoS Genet, vol 8, e1002672, 2012.
[41]
R. S. Scheurmann, S. Tam, P. M. Burgers, C. Lu, and H. Echols, “Identification of the E-subunit of Escherichia coli DNA polymerase III holoenzyme as the dnaQ gene product: a fidelity subunit for DNA replication,” Proc Natl Acad Sci USA, vol. 80, pp. 7085–7089, 1983
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