Rapid evolution of silver nanoparticle resistance in Escherichia coli

Frontiers in Genetics

Volumn 5, Issue FEB, 2015, Pages

  Graves, Joseph L ^a   Tajkarimi, Mehrdad ^a   Cunningham, Quincy ^a   Campbell, Adero ^b   Nonga, Herve ^c   Harrison, Scott H ^a   Barrick, Jeffrey E ^d  

^a NORTH CAROLINA A AND T STATE UNIVERSITY   (United States)

^b BENNETT COLLEGE   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Adaptation; AgNPs; E. Coli; ENPs; Genomics

Indexed keywords

BIOCIDE; PROTEIN HISTIDINE KINASE; RNA POLYMERASE BETA SUBUNIT; SILVER NANOPARTICLE; SILVER NITRATE;

ARTICLE; BACTERIAL GROWTH; COLONY FORMING UNIT; CONTROLLED STUDY; DRUG RESPONSE; ESCHERICHIA COLI; GENOMICS; MINIMUM INHIBITORY CONCENTRATION; MUTATION; NONHUMAN; OPTICAL DENSITY; PHENOTYPE; SILVER NANOPARTICLE RESISTANCE; SINGLE NUCLEOTIDE POLYMORPHISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84923550695     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00042     Document Type: Article

References (41)

1. Barrick, J. E., Yu, D. S., Yoon, S. H., Jeong, H., Oh, T. K., Schneider, D., et al. (2009). Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243-1249. doi: 10.1038/nature08480
2. Conrad, T. M., Frazier, M., Joyce, A. R., Cho, B.-K, Knight, E. M., Lewis, N. E., et al. (2010). RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proc. Natl. Acad. Sci. U.S.A. 107, 20500-20505. doi: 10.1073/pnas.0911253107
3. Conrad, T. M., Lewis, N. E., and Palsson, B. O. (2011). Microbial laboratory evolution in the era of genome-scale science. Mol. Syst. Biol. 7:509. doi: 10.1038/msb.2011.42
4. Cramer, P., Bushnell, D. A., and Kornberg, R. D. (2001). Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292, 1863-1876. doi: 10.1126/science.1059493
5. Deatherage, D. E., and Barrick, J. E. (2014). Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol. Biol. 1151, 165-188. doi: 10.1007/978-1-4939-0554-6_12
6. Duncan, T. V. (2011). Application of nanotechnology in food packaging and food safety: barrier materials, antimicrobials, and sensors. J. Colloid. Interface Sci. 363, 1-24. doi: 10.1016/j.jcis.2011.07.017
7. El Badawy, A. M., Silva, R. G., Morris, B., Scheckel, K. G., Suidan, M. T., and Tolaymat, T. M. (2011). Surface charge dependent toxicity of silver nanoparticles. Environ. Sci. Technol. 45, 283-287. doi: 10.1021/es1034188
8. Feng, Q. L., Wu, J., Chen, G. Q., Cui, F. Z., Kim, T. N., and Kim, J. O. (2000). A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52, 662-668. doi: 10.1002/1097-4636(20001215)52:4<662::AID-JBM10>3.0.CO;2-3
9. Franke, S., Grass, G., and Nies, D. H. (2001). The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147, 965-972.
10. GE Health Life Sciences. (2014). Avaliable online at: http://www.gelifesciences.com/webapp/wcs/stores/servlet/catalog/en/GELifeSciences-US/applications/nucleic-acid-sample-preparation/
11. Gottschalk, F., Sonderer, T., Scholz, R. W., and Nowack, B. (2009). Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, Fullerenes) for different regions. Environ. Sci. Technol. 43, 9216-9922. doi: 10.1021/es9015553
12. Graves, J. L. (2014). A grain of salt: metallic and metallic oxide nanoparticles as the new antimicrobials. JSM Nanotechnol. Nanomed. 2:1026.
13. Gudipathy, S., and McEvoy, M. M. (2014). The histidine kinase CusS senses silver ions through direct binding by its sensor domain. Biochimica et Biophysica Acta. 1844, 1656-1661. doi: 10.1016/j.bbapap.2014.06.001
14. Gupta, A., Phung, L. T., Taylor, D. E., and Silver, S. (2001). Diversity of resistance genes in IncH incompatibility group plasmids. Microbiology 147, 3393-3402.
15. Gupta, A., and Silver, S. (1998). Silver as a biocide: will resistance become a problem? Nat. Biotechnol. 16:868. doi: 10.1038/nbt1098-888
16. Kedziora, A., Gerasymchuk, Y., Sroka, E., Bugla-Ploskonska, G., Doroszkiewicz, W., Rybak, Z., et al. (2013). Use of the materials based on partially reduced graphene-oxide with silver nanoparticle as bacteriostatic and bactericidal agent. Polim. Med. 43, 129-134.
17. Klasen, H. J. (2000). A historical review of the use of silver in the treatment of burns. Part I early uses. Burns 30, 1-9.
18. Li, Y., Bahti, P., Shaw, N., Song, G., Chen, S., Zhang, X., et al. (2008). Crystal structure of a novel non-Pfam protein AF1514 from Archeoglogus fulgidus DSM 4304 solved by S-SAD using a Cr X-ray source. Proteins 71, 2109-2113. doi: 10.1002/prot.22025
19. Li, C., Kappock, T. J., Stubbe, J., Weaver, T. M., and Ealick, S. E. (1999). X-ray crystal structure of aminoimidazole ribonucleotide synthetase (PurM), from Escherichia coli purine biosynthetic pathway at 2.5 A resolution. Struct. Fold Des. 7, 1155-1166. doi: 10.1016/S0969-2126(99)80182-8
20. Li, X. Z., Nikaido, H., and Williams, K. E. (1997). Silver-resistant mutants of Escherichia coli display active efflux of Ag+ and are deficient in porins. Bacteriol. 179, 6127-6132.
21. Li, Y., Leung, P., Yao, L., Song, Q. W., and Newton, E. (2006). Antimicrobial effect of surgical masks coated with nanoparticles. J. Hosp. Infect. 62, 58-63. doi: 10.1016/j.jhin.2005.04.015
22. Liau, S. Y., Read, D. C., Pugh, W. J., Furr, J. R., and Russell, A. D. (1997). Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett. Appl. Microbiol. 25, 279-283. doi: 10.1046/j.1472-765X.1997.00219.x
23. Lok, C. N., Ho, C. M., Chen, R., Tam, P. K., Chiu, J. F., and Che, C. M. (2008). Proteomic identification of the Cus system as a major determinant of constitutive Escherichia coli silver resistance of chromosomal origin. J. Proteome Res. 7, 2351-2356. doi: 10.1021/pr700646b
24. McHugh, G. L., Moellering, R. C., Hopkins, C. C., and Swartz, M. N. (1975). Salmonella typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet 1, 235-240. doi: 10.1016/S0140-6736(75)91138-1
25. Mijnendonckx, K., Leys, N., Mahillon, J., Silver, S., and Von Houdt, R. (2013). Antimicrobial silver: uses, toxicity, and the potential for resistance. Biometals 26, 609-621. doi: 10.1007/s10534-9645-z
26. Momtaz, H., Safarpoor Dehkordi, F., Taktaz, T., Rezvani, A., and Yarali, S. (2012). Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: serogroups, virulence factors, and antibiotic resistance properties. ScientificWorld Journal 2012:618709. doi: 10.1100/2012/618709
27. Nahku, R., Peebo, K., Valgepea, K., Barrick, J. E., Adamberg, K., and Vilu, R. (2011). Stock culture heterogeneity rather than new mutational variation complicates short-term cell physiology studies of Escherichia coli K-12 MG1655 in continuous culture. Microbiology 157, 2604-2610. doi: 10.1099/mic.0.050658-0
28. Quinn, H., Cameron, A. D. S., and Dorman, C. J. (2014). Bacterial regulon evolution: distinct responses and roles for the identical OmpR proteins of Salmonella Typhimurium and Escherichia coli in the acid stress response. PLoS Genetics 10:e1004215. doi: 10.1371/journal.pgen.1004215
29. Rai, M., Yadav, A., and Gade, A. (2009). Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76-83. doi: 10.1016/j.biotechadv.2008.09.002
30. Rai, M. K., Deshmukh, S. D., Ingle, A. P., and Gade, A. K. (2012). Silver nanoparticles: the powerful nanoweapon against multi-drug resistant bacteria. J. Appl. Microbiol. 112, 841-852. doi: 10.1111/j.1365-2672.2012.05253.x
31. Rhee, J. E., Sheng, W., Morgan, L. K., Nolet, R., Liao, X., and Kenney, L. J. (2008). Amino acids important for DNA recognition by the response regulator OmpR. J. Biol. Chem. 13, 8864-8677. doi: 10.1074/jbc.M705550200
32. Riley, M., Abe, T., Arnaud, M. B., Berlyn, M. K., Blattner, F. R., Chaudhuri, R. R., et al. (2006). Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res. 34, 1-9. doi: 10.1093/nar/gkj405
33. Sampei, G., and Mizobuchi, K. (1989). The organization of the purl gene encoding 5'-Phosphoribosylformylglycinamide aminotransferase of Escherichia coli. J. Biol. Chem. 264, 21230-21238.
34. Scheutz, F., and Strockbine, N. A. (2005). "Genus I. Escherichia, castellani and chalmers 1919," in Bergey's Manual of Systematic Bacteriology, Vol. 2, The Proteobacteria, eds G. M. Garrity, D. J. Brenner, N. R. Kreig, and J. R. Staley (New York, NY: Springer), 607-624.
35. Silver, S. (2003). Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol. Rev. 27, 341-353.
36. Siqueira, M. C., Coelho, G. F., de Moura, M. R., Bresolin, J. D., Hubinger, S. Z., Marconcini, J. M., et al. (2014). Evaluation of antimicrobial activity of silver nanoparticles for carboxymethylcellulose film applications in food packaging. J. Nanosci. Nanotechnol. 14, 5512-5517. doi: 10.1166/jnn.2014.8991
37. Tadesse, D. A., Zhao, S., Tong, E., Ayers, S., Singh, A., Bartholomew, M. J., et al. (2012). Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerg. Infect. Dis. 18, 741-749. doi: 10.3201/eid1805.111153
38. Tajkarimi, M., Iyer, D., Tarannum, M., Cunningham, Q., Sharpe, I., Harrison, S. H., et al. (2014). The effect of silver nanoparticle size and coating on Escherichia coli. JSM Nanotechnol. Nanomed. 2:1025.
39. Xia, L. N., Tao, X. Q., Shen, J. Z., Dai, L., Wang, Y., Chen, X., et al. (2011). A survey of β-lactamase and 16S rRNA methylase genes among fluoroquinolone-resistant Escherichia coli isolates and their horizontal transmission in Shandong, China. Foodborne Pathog Dis. 8, 1241-1248. doi: 10.1089/fpd.2011.0868
40. Xiu, Z. M., Zhang, Q. B., Puppala, H. L., Colvin, V. L., and Alvarez, P. J. (2012). Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. 12, 4271-4275. doi: 10.1021/nl301934w
41. Yamanaka, M., Hara, K., and Kudo, J. (2005). Bactericidal actions of a silver ion solution on Escherichia coli, studied by energy-filtering transmission electron microscopy and proteomic analysis. Appl. Environ. Microbiol. 71, 7589-7593. doi: 10.1128/AEM.71.11.7589-7593.2005