Transposable elements in Escherichia coli antimicrobial resistance
Archana Iyer, Elie Barbour, Esam Azhar, Alaaeddin Ali El Salabi, Hani Mutlak A. Hassan, Ishtiaq Qadri, Adeel Chaudhary, Adel Abuzenadah, Taha Kumosani, Ghazi Damanhouri, Maha Alawi, Tarek Na’was, Afif M. Abdel Nour, Steve Harakeh
Department of Animal and Veterinary Sciences, American University of Beirut, Beirut, Lebanon.
Department of Biochemistry, King Abdulaziz University, Jeddah, KSA.
Infection Control and Antimicrobial Drug Resistance, University of Benghazi, Benghazi, Libya.
Infection Control and Environmental Health Unit, King Abdulaziz University Hospital, King Abdulaziz University, Jeddah, KSA.
King Fahd Medical Research Center, King Abdulaziz University, Jeddah, KSA.
Lebanese American University, Beirut, Lebanon.
Special Infectious Agents Unit—Biosafety Level 3, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, KSA.
DOI: 10.4236/abb.2013.43A055   PDF    HTML   XML   8,560 Downloads   15,479 Views   Citations


Transposable elements are capable of switching their positions on the genome thereby causing gene arrangements and contributing to genome evolution. The aim of this review is to specifically discuss the role of transposable elements in transferring antimicrobial resistance genes in E. coli, thus contributing to increase in virulence and conferring the possibility of multidrug resistance. Different types of transposable elements such as transposons and integrons and their profound influence on E. coli antimicrobial resistance are the focus of this review.

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Iyer, A. , Barbour, E. , Azhar, E. , Salabi, A. , Hassan, H. , Qadri, I. , Chaudhary, A. , Abuzenadah, A. , Kumosani, T. , Damanhouri, G. , Alawi, M. , Na’was, T. , Nour, A. and Harakeh, S. (2013) Transposable elements in Escherichia coli antimicrobial resistance. Advances in Bioscience and Biotechnology, 4, 415-423. doi: 10.4236/abb.2013.43A055.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Hua-Van, A., Rouzic, A.L., Boutin, T.S., Filee, J. and Capy, P. (2011) The struggle for life of the genome’s selfish architects. Biology Direct, 6, 19. doi:10.1186/1745-6150-6-19
[2] Shapiro, J.A. (2010) Mobile DNA and evolution in the 21st century. Mobile DNA, 1, 4. doi:10.1186/1759-8753-1-4
[3] Bao, W., Jurka, M.G., Kapitonov, V.V. and Jurka, J. (2009) New superfamilies of eukaryotic DNA transposons and their internal divisions. Molecular Biology and Evolution, 26, 983-993. doi:10.1093/molbev/msp013
[4] Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., Paux, E., SanMiguel, P. and Schulman A.H. (2007) A unified classification system for eukaryotic transposable elements. Nature Reviews Genetics, 8, 973-982. doi:10.1038/nrg2165
[5] Martin, S.L. and Garfinkel, D.J. (2003) Survival strategies for transposons and genomes. Genome Biology, 4, 313. doi:10.1186/gb-2003-4-4-313
[6] Kapitonov, V.V. and Jurka, J. (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nature Reviews Genetics, 9, 411-412. doi:10.1038/nrg2165-c1
[7] Madigan, M.T., Martinko, J.M. and Brock, T.D. (2006) Brock biology of microorganisms. Pearson Prentice Hall, Upper Saddle River.
[8] Feschotte, C. and Pritham, E.J. (2007) DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics, 41, 331-368. doi:10.1146/annurev.genet.40.110405.090448
[9] Wagner, A. (2006) Periodic extinctions of transposable elements in bacterial lineages: Evidence from intragenomic variation in multiple genomes. Molecular Biology and Evolution, 23, 723-733. doi:10.1093/molbev/msj085
[10] Cerveau, N., Leclerq, S., Bouchon, D. and Cordaux, R. (2011) Evolutionary dynamics and genomic impact of prokaryote transposable elements. In: Pontarotti, P., Ed., Springer, Heidelberg and New York, 291-312.
[11] C. Feschotte (2008) Transposable elements and the evolution of regulatory networks. Nature Reviews Genetics, 9, 397-405. doi:10.1038/nrg2337
[12] Aarestrup, F.M., Wegener, H.C. and Collignon, P. (2008) Resistance in bacteria of the food chain: Epidemiology and control strategies. Expert Review of Anti-Infective Therapy, 6, 733-750. doi:10.1586/14787210.6.5.733
[13] Levy, S.B. and Marshall, B. (2004) Antibacterial resistance worldwide: Causes, challenges and responses. Nature Medicine, 10, S122-129. doi:10.1038/nm1145
[14] von Baum, H. and Marre, R. (2005) Antimicrobial resistance of Escherichia coli and therapeutic implications. International Journal of Medical Microbiology, 295, 503511. doi:10.1016/j.ijmm.2005.07.002
[15] Erb, A., Sturmer, T., Marre, R. and Brenner, H. (2007) Prevalence of antibiotic resistance in Escherichia coli: Overview of geographical, temporal, and methodological variations. European Journal of Clinical Microbiology & Infectious Diseases, 26, 83-90. doi:10.1007/s10096-006-0248-2
[16] Hammerum, A.M. and Heuer, O.E. (2009) Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clinical Infectious Diseases, 48, 916-921. doi:10.1086/597292
[17] Adachi, F., Yamamoto, A., Takakura, K.I. and Kawahara, R. (2013) Occurrence of fluoroquinolones and fluoroquinolone-resistance genes in the aquatic environment. Science of the Total Environment, 444C, 508-514. doi:10.1016/j.scitotenv.2012.11.077
[18] Ryu, S.H., Park, S.G., Choi, S.M., Hwang, Y.O., Ham, H.J., Kim, S.U., Lee, Y.K., Kim, M.S., Park, G.Y., Kim, K.S. and Chae, Y.Z. (2012) Antimicrobial resistance and resistance genes in Escherichia coli strains isolated from commercial fish and seafood. International Journal of Medical Microbiology, 152, 14-18. doi:10.1016/j.ijfoodmicro.2011.10.003
[19] Stalder, T., Barraud, O., Casellas, M., Dagot, C. and Ploy, M.C. (2012) Integron involvement in environmental spread of antibiotic resistance. Front Microbiol, 3, 119. doi:10.3389/fmicb.2012.00119
[20] Davies, J. and Davies, D. (2010) Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74, 417-433. doi:10.1128/MMBR.00016-10
[21] Wright, G.D. (2010) Antibiotic resistance in the environment: A link to the clinic? Current Opinion in Microbiology, 13, 589-594. doi:10.1016/j.mib.2010.08.005
[22] Martinez, J.L. (2008) Antibiotics and antibiotic resistance genes in natural environments. Science, 321, 365-367. doi:10.1126/science.1159483
[23] D’Costa, V.M., McGrann, K.M., Hughes, D.W. and Wright, G.D. (2006) Sampling the antibiotic resistome. Science, 311, 374-377. doi:10.1126/science.1120800
[24] Aminov, R.I. and Mackie, R.I. (2007) Evolution and ecology of antibiotic resistance genes. FEMS Microbiology Letters, 271, 147-161. doi:10.1111/j.1574-6968.2007.00757.x
[25] Harada, S. (2012) Genetic elements involved in the acquisition of antimicrobial resistance genes in bacteria. Nihon Rinsho, 70, 329-332.
[26] Roberts, A.P., Chandler, M., Courvalin, P., Guedon, G., Mullany, P., Pembroke, T., Rood, J.I., Smith, C.J., Summers, A.O., Tsuda, M. and Berg, D.E. (2008) Revised nomenclature for transposable genetic elements. Plasmid, 60, 167-173. doi:10.1016/j.plasmid.2008.08.001
[27] Reznikoff, W.S. (2003) Tn5 as a model for understanding DNA transposition. Molecular Microbiology, 47, 1199-1206. doi:10.1046/j.1365-2958.2003.03382.x
[28] Kopecko, D.J. and Cohen, S.N. (1975) Site specific recA— independent recombination between bacterial plasmids: Involvement of palindromes at the recombinational loci. Proceedings of the National Academy of Sciences of the United States of America, 72, 1373-1377. doi:10.1073/pnas.72.4.1373
[29] Berg, D.E., Davies, J., Allet, B. and Rochaix, J.D. (1975) Transposition of R factor genes to bacteriophage lambda. Proceedings of the National Academy of Sciences of the United States of America, 72, 3628-3632. doi:10.1073/pnas.72.9.3628
[30] Barth, P.T., Datta, N., Hedges, R.W. and Grinter, N.J. (1976) Transposition of a deoxyribonucleic acid sequence encoding trimethoprim and streptomycin resistances from R483 to other replicons. Journal of Bacteriology, 125, 800-810.
[31] Gottesman, M.M. and Rosner, J.L. (1975) Acquisition of a determinant for chloramphenicol resistance by coliphage lambda. Proceedings of the National Academy of Sciences of the United States of America, 72, 5041-5045. doi:10.1073/pnas.72.12.5041
[32] Foster, T.J., Howe, T.G. and Richmond, K.M. (1975) Translocation of the tetracycline resistance determinant from R100-1 to the Escherichia coli K-12 chromosome. Journal of Bacteriology, 124, 1153-1158.
[33] Oka, A., Sugisaki, H. and Takanami, M. (1981) Nucleotide sequence of the kanamycin resistance transposon Tn903. Journal of Molecular Biology, 147, 217-226. doi:10.1016/0022-2836(81)90438-1
[34] So, M. and McCarthy, B.J. (1980) Nucleotide sequence of the bacterial transposon Tn1681 encoding a heat-stable (ST) toxin and its identification in enterotoxigenic Escherichia coli strains. Proceedings of the National Academy of Sciences of the United States of America, 77, 4011-4015. doi:10.1073/pnas.77.7.4011
[35] Rice, L.B. (1998) Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrobial Agents and Chemotherapy, 42, 18711-877.
[36] Enne, V.I., Delsol, A.A., Davis, G.R., Hayward, S.L., Roe, J.M. and Bennett, P.M. (2005) Assessment of the fitness impacts on Escherichia coli of acquisition of antibiotic resistance genes encoded by different types of genetic element. Journal of Antimicrobial Chemotherapy, 56, 544-551. doi:10.1093/jac/dki255
[37] Reznikoff, W.S. (2008) Transposon Tn5. Annual Review of Genetics, 42, 269-286. doi:10.1146/annurev.genet.42.110807.091656
[38] Cambray, G., Guerout, A.M. and Mazel, D. (2010) Integrons. Annual Review of Genetics, 44, 141-166. doi:10.1146/annurev-genet-102209-163504
[39] Labar, A.S., Millman, J.S., Ruebush, E., Opintan, J.A., Bishar, R.A., Aboderin, A.O., Newman, M.J., Lamikanra, A. and Okeke, I.N. (2012) Regional dissemination of a trimethoprim-resistance gene cassette via a successful transposable element. PLoS One, 7, Article ID: e38142. doi:10.1371/journal.pone.0038142
[40] Fluit, A.C. and Schmitz, F.J. (2004) Resistance integrons and super-integrons. Clinical Microbiology and Infection, 10, 272-288. doi:10.1111/j.1198-743X.2004.00858.x
[41] Ploy, M.C., Lambert, T., Couty, J.P. and Denis, F. (2000) Integrons: An antibiotic resistance gene capture and expression system. Clinical Chemistry and Laboratory Medicine, 38, 483-487. doi:10.1515/CCLM.2000.070
[42] Naas, T., Mikami, Y., Imai, T., Poirel, L. and Nordmann, P. (2001) Characterization of In53, a class 1 plasmidand composite transposon-located integron of Escherichia coli which carries an unusual array of gene cassettes. Journal of Bacteriology, 183, 235-249. doi:10.1128/JB.183.1.235-249.2001
[43] Partridge, S.R., Tsafnat, G., Coiera, E. and Iredell, J.R. (2009) Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiology Reviews, 33, 757-784. doi:10.1111/j.1574-6976.2009.00175.x
[44] Skurnik, D., Menac’h A.L., Zurakowski, D., Mazel, D., Courvalin, P., Denamur, E., Andremont, A. and Ruimy, R. (2005) Integron-associated antibiotic resistance and phylogenetic grouping of Escherichia coli isolates from healthy subjects free of recent antibiotic exposure. Antimicrobial Agents and Chemotherapy, 49, 3062-3065. doi:10.1128/AAC.49.7.3062-3065.2005
[45] Luo, Y., Mao, D., Rysz, M., Zhou, Q., Zhang, H., Xu, L. and Pedro, J.J.A. (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environmental Science & Technology, 44, 7220-7225. doi:10.1021/es100233w
[46] Kristiansson, E., Fick, J., Janzon, A., Grabic, R., Rutgersson, C., Weijdegard, B., Soderstrom, H. and Larsson, D.G. (2011) Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One, 6, Article ID: e17038. doi:10.1371/journal.pone.0017038
[47] Daikos, G.L., Kosmidis, C., Tassios, P.T., Petrikkos, G., Vasilakopoulou, A., Psychogiou, M., Stefanou, I., Avlami, A. and Katsilambros, N. (2007) Enterobacteriaceae bloodstream infections: presence of integrons, risk factors, and outcome. Antimicrobial Agents and Chemotherapy, 51, 2366-2372. doi:10.1128/AAC.00044-07
[48] Barlow, R.S., Fegan, N. and Gobius, K.S. (2009) Integroncontaining bacteria in faeces of cattle from different production systems at slaughter. Journal of Applied Microbiology, 107, 540-545. doi:10.1111/j.1365-2672.2009.04240.x
[49] Guerin, E., Cambray, G., Sanchez-Alberola, N., Campoy, S., Erill, I., Da Re, S., Gonzalez-Zorn, B., Barbe, J., Ploy, M.C. and Mazel, D. (2009) The SOS response controls integron recombination. Science, 324, 1034. doi:10.1126/science.1172914
[50] Cambray, G., Sanchez-Alberola, N., Campoy, S., Guerin, E., Da Re, S., Gonzalez-Zorn, B., Ploy, M.C., Barbe, J., Mazel, D. and Erill, I. (2011) Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mobile DNA, 2, 6. doi:10.1186/1759-8753-2-6
[51] Baharoglu, Z., Bikard, D. and Mazel, D. (2010) Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLOS Genetics, 6, Article ID: e1001165. doi:10.1371/journal.pgen.1001165
[52] Laroche, E., Pawlak, B., Berthe, T., Skurnik, D. and Petit, F. (2009) Occurrence of antibiotic resistance and class 1, 2 and 3 integrons in Escherichia coli isolated from a densely populated estuary (Seine, France). FEMS Microbiology Ecology, 68, 118-130. doi:10.1111/j.1574-6941.2009.00655.x
[53] Chen, B., Zheng, W., Yu, Y., Huang, W., Zheng, S., Zhang, Y., Guan, X., Zhuang, Y., Chen, N. and Topp, E. (2011) Class 1 integrons, selected virulence genes, and antibiotic resistance in Escherichia coli isolates from the Minjiang river, Fujian province, China. Applied and Environmental Microbiology, 77, 148-155. doi:10.1128/AEM.01676-10
[54] Su, H.C., Ying, G.G., Tao, R., Zhang, R.Q., Zhao, J.L. and Liu, Y.S. (2012) Class 1 and 2 integrons, sul resistance genes and antibiotic resistance in Escherichia coli isolated from Dongjiang River, South China. Environmental Pollution, 169, 42-49. doi:10.1016/j.envpol.2012.05.007
[55] Koczura, R., Mokracka, J., Jablonska, L., Gozdecka, E., Kubek, M. and Kaznowski, A. (2012) Antimicrobial resistance of integron-harboring Escherichia coli isolates from clinical samples, wastewater treatment plant and river water. Science of the Total Environment, 414, 680685. doi:10.1016/j.scitotenv.2011.10.036
[56] Soufi, L., Abbassi, M.S., Saenz, Y., Vinue, L., Somalo, S., Zarazaga, M., Abbas, A., Dbaya, R., Khanfir, L., Ben Hassen, A., Hammami, S. and Torres, C. (2009) Prevalence and diversity of integrons and associated resistance genes in Escherichia coli isolates from poultry meat in Tunisia. Foodborne Pathogens and Disease, 6, 1067-1073. doi:10.1089/fpd.2009.0284
[57] Kadlec, K. and Schwarz, S. (2008) Analysis and distribution of class 1 and class 2 integrons and associated gene cassettes among Escherichia coli isolates from swine, horses, cats and dogs collected in the BfT-GermVet monitoring study. Journal of Antimicrobial Chemotherapy, 62, 469-473. doi:10.1093/jac/dkn233
[58] Wu, R.B., Alexander, T.W., Li, J.Q., Munns, K., Sharma, R. and McAllister, T.A. (2011) Prevalence and diversity of class 1 integrons and resistance genes in antimicrobial-resistant Escherichia coli originating from beef cattle administered subtherapeutic antimicrobials. Journal of Applied Microbiology, 111, 511-523. doi:10.1111/j.1365-2672.2011.05066.x
[59] Najibi, S., Bakhshi, B., Fallahzad, S., Pourshafie, M.R., Katouli, M., Sattari, M., Alebouyeh, M. and Tajbakhsh, M. (2012) Distribution of class 1 integrons among enteropathogenic Escherichia coli. Canadian Journal of Microbiology, 58, 637-643. doi:10.1139/w2012-035
[60] Bakhshi, B., Fallahzad, S. and Pourshafie, M.R. (2012) The occurrence of atypical enteropathogenic Escherichia coli strains among children with diarrhea in Iran. Journal of Infection and Chemotherapy. doi:10.1007/s10156-012-0526-0
[61] Vinue, L., Saenz, Y., Somalo, S., Escudero, E., Moreno, M.A., Ruiz-Larrea, F. and Torres, C. (2008) Prevalence and diversity of integrons and associated resistance genes in faecal Escherichia coli isolates of healthy humans in Spain. Journal of Antimicrobial Chemotherapy, 62, 934-937. doi:10.1093/jac/dkn331
[62] Toleman, M.A., Bennett, P.M. and Walsh, T.R. (2006) ISCR elements: Novel gene-capturing systems of the 21st century? Microbiology and Molecular Biology Reviews, 70, 296-316. doi:10.1128/MMBR.00048-05
[63] Toleman, M.A., Bennett, P.M. and Walsh, T.R. (2006) Common regions e.g. orf513 and antibiotic resistance: IS91like elements evolving complex class 1 integrons. Journal of Antimicrobial Chemotherapy, 58, 1-6. doi:10.1093/jac/dkl204
[64] Deng, Y., Zeng, Z., Liu, J. and Chen, Z. (2009) Insertion sequence common region element: A novel gene-capturing system in bacteria—a review. Acta microbiologica Sinica, 49, 987-993.
[65] Call, D.R., Singer, R.S., Meng, D., S.L. Broschat, L.H. Orfe, J.M. Anderson, D.R. Herndon, L.S. Kappmeyer, J. B. Daniels and T.E. Besser (2010) BlaCMY-2-positive IncA/C plasmids from Escherichia coli and Salmonella enterica are a distinct component of a larger lineage of plasmids. Antimicrobial Agents and Chemotherapy, 54, 590-596. doi:10.1128/AAC.00055-09
[66] Toleman, M.A. and Walsh, T.R. (2010) ISCR elements are key players in IncA/C plasmid evolution. Antimicrobial Agents and Chemotherapy, 54, 35-34. doi:10.1128/AAC.00383-10
[67] Tadesse, D.A., Zhao, S., Tong, E., Ayers, S., Singh, A., Bartholomew, M.J. and McDermott, P.F. (2012) Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerging Infectious Diseases, 18, 741-749. doi:10.3201/eid1805.111153
[68] FDA (2010) National antimicrobial resistance monitoring system enteric bacteria (NARMS): 2008 executive report. System/default.htm

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