Ranking of persister genes in the same Escherichia coli genetic background demonstrates varying importance of individual persister genes in tolerance to different antibiotics

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Wu, Nan ^a   He, Lei ^a   Cui, Peng ^a   Wang, Wenjie ^a   Yuan, Youhua ^a   Liu, Shuang ^a   Xu, Tao ^a   Zhang, Shanshan ^a   Wu, Jing ^a   Zhang, Wenhong ^a   Zhang, Ying ^a,b  

^a FUDAN UNIVERSITY   (China)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Antibiotics; Escherichia coli; Knockout mutant; Persistence; Persister gene; Ranking

Indexed keywords

AMPICILLIN; ANTITOXIN; GENTAMICIN; NORFLOXACIN; TRIMETHOPRIM;

ANTIBIOTIC SENSITIVITY; ARTICLE; CLPB GENE; DNAK GENE; ESCHERICHIA COLI; GENE; GENE DELETION; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; MQSR GENE; NONHUMAN; OXYR GENE; PERSISTER GENE; RECA GENE; RELA GENE; RPOS GENE; SUCB GENE;

EID: 84946727512     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01003     Document Type: Article

References (50)

1. Amato, S. M., Fazen, C. H., Henry, T. C., Mok, W. W., Orman, M. A., Sandvik, E. L., et al. (2014). The role of metabolism in bacterial persistence. Front. Microbiol. 5:70. doi: 10.3389/fmicb.2014.00070
2. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science 305, 1622-1625. doi: 10.1126/science.1099390
3. Bigger, J. W. (1944). Treatment of staphylococcal infections with penicillin BY Intermittent Sterilisation. Lancet 244, 497-500. doi: 10.1016/S0140-6736(00)74210-3
4. Blango, M. G., and Mulvey, M. A. (2010). Persistence of uropathogenic Escherichia coli in the face of multiple antibiotics. Antimicrob. Agents Chemother. 54, 1855-1863. doi: 10.1128/AAC.00014-10
5. Buts, L., Lah, J., Dao-Thi, M. H., Wyns, L., and Loris, R. (2005). Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci. 30, 672-679. doi: 10.1016/j.tibs.2005.10.004
6. Datsenko, K. A., and Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645. doi: 10.1073/pnas.120163297
7. Debbia, E. A., Roveta, S., Schito, A. M., Gualco, L., and Marchese, A. (2001). Antibiotic persistence: the role of spontaneous DNA repair response. Microb. Drug Resist. (Larchmont, N.Y.) 7, 335-342. doi: 10.1089/10766290152773347
8. Dorr, T., Lewis, K., and Vulic, M. (2009). SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 5:e1000760. doi: 10.1371/journal.pgen.1000760
9. Dorr, T., Vulic, M., and Lewis, K. (2010). Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 8:e1000317. doi: 10.1371/journal.pbio.1000317
10. Falla, T. J., and Chopra, I. (1998). Joint tolerance to beta-lactam and fluoroquinolone antibiotics in Escherichia coli results from overexpression of hipA. Antimicrob. Agents Chemother. 42, 3282-3284.
11. Gerard, F., Dri, A. M., and Moreau, P. L. (1999). Role of Escherichia coli RpoS, LexA and H-NS global regulators in metabolism and survival under aerobic, phosphate-starvation conditions. Microbiology 145(Pt 7), 1547-1562.
12. Girgis, H. S., Harris, K., and Tavazoie, S. (2012). Large mutational target size for rapid emergence of bacterial persistence. Proc. Natl. Acad. Sci. U.S.A. 109, 12740-12745. doi: 10.1073/pnas.1205124109
13. Hansen, S., Lewis, K., and Vulic, M. (2008). Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob. Agents Chemother. 52, 2718-2726. doi: 10.1128/AAC.00144-08
14. Hengge-Aronis, R. (1996). Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol. Microbiol. 21, 887-893. doi: 10.1046/j.1365-2958.1996.511405.x
15. Hobby, G. L., Meyer, K., and Chaffee, E. (1942). Observations on the mechanism of action of penicillin. Proc. Soc. Exp. Biol. Med. 50, 281-285. doi: 10.3181/00379727-50-13773
16. Hong, S. H., Wang, X., O'Connor, H. F., Benedik, M. J., and Wood, T. K. (2012). Bacterial persistence increases as environmental fitness decreases. Microb. Biotechnol. 5, 509-522. doi: 10.1111/j.1751-7915.2011.00327.x
17. Itsko, M., and Schaaper, R. M. (2014). dGTP starvation in Escherichia coli provides new insights into the thymineless-death phenomenon. PLoS Genet. 10:e1004310. doi: 10.1371/journal.pgen.1004310
18. Kaspy, I., Rotem, E., Weiss, N., Ronin, I., Balaban, N. Q., and Glaser, G. (2013). HipA-mediated antibiotic persistence via phosphorylation of the glutamyl-tRNA-synthetase. Nat. Commun. 4, 3001. doi: 10.1038/ncomms4001
19. Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K. (2004). Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172-8180. doi: 10.1128/JB.186.24.8172-8180.2004
20. Kim, Y., Wang, X., Zhang, X. S., Grigoriu, S., Page, R., Peti, W., et al. (2010). Escherichia coli toxin/antitoxin pair MqsR/MqsA regulate toxin CspD. Environ. Microbiol. 12, 1105-1121. doi: 10.1111/j.1462-2920.2009.02147.x
21. Kint, C. I., Verstraeten, N., Fauvart, M., and Michiels, J. (2012). New-found fundamentals of bacterial persistence. Trends Microbiol. 20, 577-585. doi: 10.1016/j.tim.2012.08.009
22. Konno, T., Takahashi, T., Kurita, D., Muto, A., and Himeno, H. (2004). A minimum structure of aminoglycosides that causes an initiation shift of trans-translation. Nucleic Acids Res. 32, 4119-4126. doi: 10.1093/nar/gkh750
23. Korch, S. B., Henderson, T. A., and Hill, T. M. (2003). Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50, 1199-1213. doi: 10.1046/j.1365-2958.2003.03779.x
24. Levin, B. R., Concepcion-Acevedo, J., and Udekwu, K. I. (2014). Persistence: a copacetic and parsimonious hypothesis for the existence of non-inherited resistance to antibiotics. Curr. Opin. Microbiol. 21C, 18-21. doi: 10.1016/j.mib.2014.06.016
25. Lewis, K. (2010). Persister cells. Annu. Rev. Microbiol. 64, 357-372. doi: 10.1146/annurev.micro.112408.134306
26. Li, J., Ji, L., Shi, W., Xie, J., and Zhang, Y. (2013). Trans-translation mediates tolerance to multiple antibiotics and stresses in Escherichia coli. J. Antimicrob. Chemother. 68, 2477-2481. doi: 10.1093/jac/dkt231
27. Li, Y., and Zhang, Y. (2007). PhoU is a persistence switch involved in persister formation and tolerance to multiple antibiotics and stresses in Escherichia coli. Antimicrob. Agents Chemother. 51, 2092-2099. doi: 10.1128/AAC.00052-07
28. Luidalepp, H., Joers, A., Kaldalu, N., and Tenson, T. (2011). Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. J. Bacteriol. 193, 3598-3605. doi: 10.1128/JB.00085-11
29. Ma, C., Sim, S., Shi, W., Du, L., Xing, D., and Zhang, Y. (2010). Energy production genes sucB and ubiF are involved in persister survival and tolerance to multiple antibiotics and stresses in Escherichia coli. FEMS Microbiol. Lett. 303, 33-40. doi: 10.1111/j.1574-6968.2009.01857.x
30. Maisonneuve, E., Shakespeare, L. J., Jorgensen, M. G., and Gerdes, K. (2011). Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U.S.A. 108, 13206-13211. doi: 10.1073/pnas.1100186108
31. Matsuoka, Y., and Shimizu, K. (2011). Metabolic regulation in Escherichia coli in response to culture environments via global regulators. Biotechnol. J. 6, 1330-1341. doi: 10.1002/biot.201000447
32. Michel, B. (2005). After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol. 3:e255. doi: 10.1371/journal.pbio.0030255
33. Moyed, H. S., and Bertrand, K. P. (1983). hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155, 768-775.
34. Muffler, A., Traulsen, D. D., Lange, R., and Hengge-Aronis, R. (1996). Posttranscriptional osmotic regulation of the sigma(s) subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 178, 1607-1613.
35. Shi, W., Zhang, X., Jiang, X., Yuan, H., Lee, J. S., Barry, C. E., et al. (2011). Pyrazinamide inhibits trans-translation in Mycobacterium tuberculosis. Science 333, 1630-1632. doi: 10.1126/science.1208813
36. Singh, R., Ray, P., Das, A., and Sharma, M. (2009). Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J. Med. Microbiol. 58, 1067-1073. doi: 10.1099/jmm.0.009720-0
37. Singh, V. K., Utaida, S., Jackson, L. S., Jayaswal, R. K., Wilkinson, B. J., and Chamberlain, N. R. (2007). Role for dnaK locus in tolerance of multiple stresses in Staphylococcus aureus. Microbiology 153, 3162-3173. doi: 10.1099/mic.0.2007/009506-0
38. Squires, C. L., Pedersen, S., Ross, B. M., and Squires, C. (1991). ClpB is the Escherichia coli heat shock protein F84.1. J. Bacteriol. 173, 4254-4262.
39. Straus, D., Walter, W., and Gross, C. A. (1990). DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 4, 2202-2209.
40. Szabo, A., Langer, T., Schroder, H., Flanagan, J., Bukau, B., and Hartl, F. U. (1994). The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. U.S.A. 91, 10345-10349. doi: 10.1073/pnas.91.22.10345
41. Tashiro, Y., Kawata, K., Taniuchi, A., Kakinuma, K., May, T., and Okabe, S. (2012). RelE-mediated dormancy is enhanced at high cell density in Escherichia coli. J. Bacteriol. 194, 1169-1176. doi: 10.1128/JB.06628-11
42. Tilly, K., McKittrick, N., Zylicz, M., and Georgopoulos, C. (1983). The dnaK protein modulates the heat-shock response of Escherichia coli. Cell 34, 641-646. doi: 10.1016/0092-8674(83)90396-3
43. Vazquez-Laslop, N., Lee, H., and Neyfakh, A. A. (2006). Increased persistence in Escherichia coli caused by controlled expression of toxins or other unrelated proteins. J. Bacteriol. 188, 3494-3497. doi: 10.1128/JB.188.10.3494-3497.2006
44. Vega, N. M., Allison, K. R., Khalil, A. S., and Collins, J. J. (2012). Signaling-mediated bacterial persister formation. Nat. Chem. Biol. 8, 431-433. doi: 10.1038/nchembio.915
45. Wang, J. H., Singh, R., Benoit, M., Keyhan, M., Sylvester, M., Hsieh, M., et al. (2014). Sigma S-dependent antioxidant defense protects stationary-phase Escherichia coli against the bactericidal antibiotic gentamicin. Antimicrob. Agents Chemother. 58, 5964-5975. doi: 10.1128/AAC.03683-14
46. Wang, X., Lord, D. M., Hong, S. H., Peti, W., Benedik, M. J., Page, R., et al. (2013). Type II toxin/antitoxin MqsR/MqsA controls type V toxin/antitoxin GhoT/GhoS. Environ. Microbiol. 15, 1734-1744. doi: 10.1111/1462-2920.12063
47. Wang, X., and Wood, T. K. (2011). Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol. 77, 5577-5583. doi: 10.1128/AEM.05068-11
48. Yeh, J. I., Chinte, U., and Du, S. (2008). Structure of glycerol-3-phosphate dehydrogenase, an essential monotopic membrane enzyme involved in respiration and metabolism. Proc. Natl. Acad. Sci. U.S.A. 105, 3280-3285. doi: 10.1073/pnas.0712331105
49. Zhang, Y. (2014). Persisters, persistent infections and the Yin-Yang model. Emerg. Microbes Infect. 3, e3. doi: 10.1038/emi.2014.3
50. Zhang, Y., Yew, W. W., and Barer, M. R. (2012). Targeting persisters for tuberculosis control. Antimicrob. Agents Chemother. 56, 2223-2230. doi: 10.1128/AAC.06288-11