Efflux in the oral metagenome: The discovery of a novel tetracycline and tigecycline ABC transporter

Frontiers in Microbiology

Volumn 7, Issue DEC, 2016, Pages

  Reynolds, Liam J ^a,b   Roberts, Adam P ^a   Anjum, Muna F ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

ABC transporter; Antibiotic resistance; Fitness; Metagenomics; Tetracycline; Tigecycline

Indexed keywords

ABC TRANSPORTER; AMIKACIN; AMOXICILLIN PLUS CLAVULANIC ACID; CEFOTAXIME; CEFTAZIDIME; CIPROFLOXACIN; COTRIMOXAZOLE; DOXYCYCLINE; GENTAMICIN; METRONIDAZOLE; NALIDIXIC ACID; NEOMYCIN; TETRACYCLINE; TIGECYCLINE;

ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; DISK DIFFUSION; DNA EXTRACTION; DNA SEQUENCE; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; GENE LIBRARY; GRANULICATELLA ADIACENS; GROWTH CURVE; HUMAN; LACTOCOCCUS LACTIS; METAGENOME; METAGENOMICS; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SALIVA ANALYSIS; SEQUENCE ALIGNMENT; STREPTOCOCCUS;

EID: 85009195253     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01923     Document Type: Article

References (60)

1. Aas, J. A., Paster, B. J., Stokes, L. N., Olsen, I., and Dewhirst, F. E. (2005). Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43, 5721-5732. doi: 10.1128/JCM.43.11.5721-5732.2005
2. Achard-Joris, M., van den Berg van Saparoea, H. B., Driessen, A. J. M., and Bourdineaud, J.-P. (2005). Heterologously expressed bacterial and human multidrug resistance proteins confer cadmium resistance to Escherichia coli. Biochemistry 44, 5916-5922. doi: 10.1021/bi047700r
3. Aminov, R. I., Chee-Sanford, J. C., Garrigues, N., Teferedegne, B., Krapac, I. J., White, B. A., et al. (2002). Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl. Environ. Microbiol. 68, 1786-1793. doi: 10.1128/AEM.68.4.1786-1793.2002
4. Andrews, J. M. (2001). BSAC standardized disc susceptibility testing method. J Antimicrob Chemother. 48(Suppl. 1), 43-57. doi: 10.1093/jac/48.2.322
5. Anstead, G. M., Cadena, J., and Javeri, H. (2014). Treatment of infections due to resistant Staphylococcus aureus. Methods Mol. Biol. 1085, 259-309. doi: 10.1007/978-1-62703-664-1_16
6. Baylay, A. J., Ivens, A., and Piddock, L. J. (2015). A novel gene amplification causes upregulation of the PatAB ABC transporter and fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 59, 3098-3108. doi: 10.1128/AAC.04858-14
7. Biemans-Oldehinkel, E., Doeven, M. K., and Poolman, B. (2006). ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett. 580, 1023-1035. doi: 10.1016/j.febslet.2005.11.079
8. Bishburg, E., and Bishburg, K. (2009). Minocycline-an old drug for a new century: emphasis on methicillin-resistant Staphylococcus aureus (MRSA) and Acinetobacter baumannii. Int. J. Antimicrob. Agents 34, 395-401. doi: 10.1016/j.ijantimicag.2009.06.021
9. Cai, Y., Wang, R., Liang, B., Bai, N., and Liu, Y. (2011). Systematic review and meta-analysis of the effectiveness and safety of tigecycline for treatment of infectious disease. Antimicrob. Agents Chemother. 55, 1162-1172. doi: 10.1128/AAC.01402-10
10. Card, R. M., Warburton, P. J., MacLaren, N., Mullany, P., Allan, E., and Anjum, M. F. (2014). Application of microarray and functional-based screening methods for the detection of antimicrobial resistance genes in the microbiomes of healthy humans. PLoS ONE 9:e86428. doi: 10.1371/journal.pone.0086428
11. Chen, L., Song, Y., Wei, Z., He, H., Zhang, A., and Jin, M. (2013). Antimicrobial susceptibility, tetracycline and erythromycin resistance genes, and multilocus sequence typing of Streptococcus suis isolates from diseased pigs in China. J. Vet. Med. Sci. 75, 583-587. doi: 10.1292/jvms.12-0279
12. Chollet, R., Chevalier, J., Bryskier, A., and Pagès, J.-M. (2004). The AcrAB-TolC pump is involved in macrolide resistance but not in telithromycin efflux in Enterobacter aerogenes and Escherichia coli. Antimicrob. Agents Chemother. 48, 3621-3624. doi: 10.1128/AAC.48.9.3621-3624.2004
13. Chopra, I., and Roberts, M. (2001). Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65, 232-260. doi: 10.1128/MMBR.65.2.232-260.2001
14. Connell, S. R., Tracz, D. M., Nierhaus, K. H., and Taylor, D. E. (2003). Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrob. Agents Chemother. 47, 3675-3681. doi: 10.1128/AAC.47.12.3675-3681.2003
15. Dawson, R. J., and Locher, K. P. (2006). Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185. doi: 10.1038/nature05155
16. De Luca, M., Amodio, D., Chiurchiu, S., Castelluzzo, M. A., Rinelli, G., Bernaschi, P., et al. (2013). Granulicatella bacteraemia in children: two cases and review of the literature. BMC Pediatr. 13:61. doi: 10.1186/1471-2431-13-61
17. Dean, C. R., Visalli, M. A., Projan, S. J., Sum, P.-E., and Bradford, P. A. (2003). Efflux-mediated resistance to tigecycline (GAR-936) in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 47, 972-978. doi: 10.1128/AAC.47.3.972-978.2003
18. Dukers-Muijrers, N. H., van Liere, G. A., Wolffs, P. F., Den Heijer, C., Werner, M. I., and Hoebe, C. J. (2015). Antibiotic use before chlamydia and gonorrhea genital and extragenital screening in the sexually transmitted infection clinical setting. Antimicrob. Agents Chemother. 59, 121-128. doi: 10.1128/aac.03932-14
19. EUCAST (2015). Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 5.0, 2015. Basel: European Committee on Antimicrobial Susceptibility Testing. Available at: http://www.eucast.org
20. Fluit, A. C., Florijn, A., Verhoef, J., and Milatovic, D. (2005). Presence of tetracycline resistance determinants and susceptibility to tigecycline and minocycline. Antimicrob. Agents Chemother. 49, 1636-1638. doi: 10.1128/aac.49.4.1636-1638.2005
21. Forsberg, K. J., Patel, S., Wencewicz, T. A., and Dantas, G. (2015). The tetracycline destructases: a novel family of tetracycline-inactivating enzymes. Chem. Biol. 22, 888-897. doi: 10.1016/j.chembiol.2015.05.017
22. He, F., Fu, Y., Chen, Q., Ruan, Z., Hua, X., Zhou, H., et al. (2015). Tigecycline susceptibility and the role of efflux pumps in tigecycline resistance in KPC-producing Klebsiella pneumoniae. PLoS ONE 10:e119064. doi: 10.1371/journal.pone.0119064
23. Hellmich, U. A., Lyubenova, S., Kaltenborn, E., Doshi, R., van Veen, H. W., Prisner, T. F., et al. (2012). Probing the ATP hydrolysis cycle of the ABC multidrug transporter LmrA by pulsed EPR spectroscopy. J. Am. Chem. Soc. 134, 5857-5862. doi: 10.1021/ja211007t
24. Higgins, C. F. (2001). ABC transporters: physiology, structure and mechanism-an overview. Res. Microbiol. 152, 205-210. doi: 10.1016/S0923-2508(01)01193-7
25. Hollenstein, K., Dawson, R. J., and Locher, K. P. (2007). Structure and mechanism of ABC transporter proteins. Curr. Opin. Struct. Biol. 17, 412-418. doi: 10.1016/j.sbi.2007.07.003
26. Hu, V. H., Harding-Esch, E. M., Burton, M. J., Bailey, R. L., Kadimpeul, J., and Mabey, D. C. (2010). Epidemiology and control of trachoma: systematic review. Trop. Med. Int. Health 15, 673-691. doi: 10.1111/j.1365-3156.2010.02521.x
27. Hurlimann, L. M., Corradi, V., Hohl, M., Bloemberg, G. V., Tieleman, D. P., and Seeger, M. A. (2016). The Heterodimeric ABC Transporter EfrCD mediates multidrug efflux in Enterococcus faecalis. Antimicrob. Agents Chemother. 60, 5400-5411. doi: 10.1128/AAC.00661-16
28. Jones, P. M., and George, A. M. (1999). Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179, 187-202. doi: 10.1111/j.1574-6968.1999.tb08727.x
29. Lancaster, H., Bedi, R., Wilson, M., and Mullany, P. (2005). The maintenance in the oral cavity of children of tetracycline-resistant bacteria and the genes encoding such resistance. J. Antimicrob Chemother. 56, 524-531. doi: 10.1093/jac/dki259
30. Lee, E.-W., Huda, M. N., Kuroda, T., Mizushima, T., and Tsuchiya, T. (2003). EfrAB, an ABC multidrug efflux pump in Enterococcus faecalis. Antimicrob. Agents Chemother. 47, 3733-3738. doi: 10.1128/AAC.47.12.3733-3738.2003
31. Levy, S. B., McMurry, L. M., Barbosa, T. M., Burdett, V., Courvalin, P., Hillen, W., et al. (1999). Nomenclature for new tetracycline resistance determinants. Antimicrob. Agents Chemother. 43, 1523-1524.
32. Lin, S. Y., Huang, C. H., Ko, W. C., Chen, Y. H., and Hsueh, P. R. (2016). Recent developments in antibiotic agents for the treatment of complicated intra-abdominal infections. Expert Opin. Pharmacother. 17, 339-354. doi: 10.1517/14656566.2016.1122756
33. Linkevicius, M., Sandegren, L., and Andersson, D. I. (2015). Potential of tetracycline resistance proteins to evolve tigecycline resistance. Antimicrob Agents Chemother. 60, 789-796. doi: 10.1128/aac.02465-15
34. Liu, Y. Y., Wang, Y., Walsh, T. R., Yi, L. X., Zhang, R., Spencer, J., et al. (2016). Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 16, 161-168. doi: 10.1016/S1473-3099(15)00424-7
35. Lubelski, J., Mazurkiewicz, P., van Merkerk, R., Konings, W. N., and Driessen, A. J. M. (2004). ydaG and ydbA of Lactococcus lactis encode a heterodimeric ATP-binding cassette-type multidrug transporter. J. Biol. Chem. 279, 34449-34455. doi: 10.1074/jbc.M404072200
36. Lupien, A., Gingras, H., Leprohon, P., and Ouellette, M. (2015). Induced tigecycline resistance in Streptococcus pneumoniae mutants reveals mutations in ribosomal proteins and rRNA. J. Antimicrob. Chemother. 70, 2973-2980. doi: 10.1093/jac/dkv211
37. Martinez, J. L. (2009). Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157, 2893-2902. doi: 10.1016/j.envpol.2009.05.051
38. McDaniel, C., Su, S., Panmanee, W., Lau, G. W., Browne, T., Cox, K., et al. (2016). A putative ABC transporter permease is necessary for resistance to acidified nitrite and EDTA in Pseudomonas aeruginosa under aerobic and anaerobic planktonic and biofilm conditions. Front. Microbiol. 7:291. doi: 10.3389/fmicb.2016.00291
39. Mediavilla, J. R., Patrawalla, A., Chen, L., Chavda, K. D., Mathema, B., Vinnard, C., et al. (2016). Colistin-and carbapenem-resistant Escherichia coli harboring mcr-1 and blaNDM-5, causing a complicated urinary tract infection in a patient from the United States. MBio 7, e01191-e01216 doi: 10.1128/mBio.01191-16
40. Olson, M. W., Ruzin, A., Feyfant, E., Rush, T. S. III, O'Connell, J., and Bradford, P. A. (2006). Functional, biophysical, and structural bases for antibacterial activity of tigecycline. Antimicrob. Agents Chemother. 50, 2156-2166. doi: 10.1128/AAC.01499-05
41. Ramakrishnan, C., Dani, V. S., and Ramasarma, T. (2002). A conformational analysis of Walker motif A [GXXXXGKT (S)] in nucleotide-binding and other proteins. Protein Eng. 15, 783-798. doi: 10.1093/protein/15.10.783
42. Ramos, M. M. B., Gartti-Jardim, E. C., and Gaetti-Jardim Junior, E. (2009). Resistance to tetracycline and 2-lactams and distribution of resistance markers in enteric microorganisms and pseudomonads isolated from the oral cavity. J. Appl. Oral Sci. 17, 13-18. doi: 10.1590/S1678-77572009000700004
43. Roberts, M. C. (2003). Tetracycline therapy: update. Clin. Infect. Dis. 36, 462-467. doi: 10.1086/367622
44. Rubinstein, E., and Vaughan, D. (2005). Tigecycline: a novel glycylcycline. Drugs 65, 1317-1336. doi: 10.2165/00003495-200565180-00009
45. Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74, 5463-5467. doi: 10.1073/pnas.74.12.5463
46. Segata, N., Haake, S. K., Mannon, P., Lemon, K. P., Waldron, L., Gevers, D., et al. (2012). Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 13:R42. doi: 10.1186/gb-2012-13-6-r42
47. Seville, L. A., Patterson, A. J., Scott, K. P., Mullany, P., Quail, M. A., Parkhill, J., et al. (2009). Distribution of tetracycline and erythromycin resistance genes among human oral and fecal metagenomic DNA. Microb. Drug Resist. 15, 159-166. doi: 10.1089/mdr.2009.0916
48. Shen, F., Han, Q., Xie, D., Fang, M., Zeng, H., and Deng, Y. (2015). Efficacy and safety of tigecycline for the treatment of severe infectious diseases: an updated meta-analysis of RCTs. Int. J. Infect. Dis. 39, 25-33. doi: 10.1016/j.ijid.2015.08.009
49. Someya, Y., Yamaguchi, A., and Sawai, T. (1995). A novel glycylcycline, 9-(N, N-dimethylglycylamido)-6-demethyl-6-deoxytetracycline, is neither transported nor recognized by the transposon Tn10-encoded metal-tetracycline/H+ antiporter. Antimicrob. Agents Chemother. 39, 247-249. doi: 10.1128/AAC.39.1.247
50. Torres, C., Galian, C., Freiberg, C., Fantino, J. R., and Jault, J. M. (2009). The YheI/YheH heterodimer from Bacillus subtilis is a multidrug ABC transporter. Biochim. Biophys. Acta 1788, 615-622. doi: 10.1016/j.bbamem.2008.12.012
51. Vaara, M. (1993). Outer membrane permeability barrier to azithromycin, clarithromycin, and roxithromycin in gram-negative enteric bacteria. Antimicrob. Agents Chemother. 37, 354-356. doi: 10.1128/AAC.37.2.354
52. Van Berkel, M. A., Twilla, J. D., and England, B. S. (2016). Emergency department management of a myasthenia gravis patient with community-acquired pneumonia: does initial antibiotic choice lead to cure or crisis? J. Emerg. Med. 50, 281-285. doi: 10.1016/j.jemermed.2015.04.019
53. Villa, L., Feudi, C., Fortini, D., Garcia-Fernandez, A., and Carattoli, A. (2014). Genomics of KPC-producing Klebsiella pneumoniae sequence type 512 clone highlights the role of RamR and ribosomal S10 protein mutations in conferring tigecycline resistance. Antimicrob. Agents Chemother. 58, 1707-1712. doi: 10.1128/aac.01803-13
54. Villedieu, A., Diaz-Torres, M. L., Hunt, N., McNab, R., Spratt, D. A., Wilson, M., et al. (2003). Prevalence of tetracycline resistance genes in oral bacteria. Antimicrob. Agents Chemother. 47, 878-882. doi: 10.1128/AAC.47.3.878-882.2003
55. Warburton, P. J., Ciric, L., Lerner, A., Seville, L. A., Roberts, A. P., Mullany, P., et al. (2013). TetAB46, a predicted heterodimeric ABC transporter conferring tetracycline resistance in Streptococcus australis isolated from the oral cavity. J. Antimicrob. Chemother. 68, 17-22. doi: 10.1093/jac/dks351
56. Wu, N., Qiao, M., Zhang, B., Cheng, W. D., and Zhu, Y. G. (2010). Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ. Sci. Technol. 44, 6933-6939. doi: 10.1021/es1007802
57. Yang, W., Moore, I. F., Koteva, K. P., Bareich, D. C., Hughes, D. W., and Wright, G. D. (2004). TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. J. Biol. Chem. 279, 52346-52352. doi: 10.1074/jbc.M409573200
58. Yao, X., Doi, Y., Zeng, L., Lv, L., and Liu, J.-H. (2016). Carbapenem-resistant and colistin-resistant Escherichia coli co-producing NDM-9 and MCR-1. Lancet Infect. Dis. 16, 288-289. doi: 10.1016/S1473-3099(16)00057-8
59. Zheng, X., Freeman, A. F., Villafranca, J., Shortridge, D., Beyer, J., Kabat, W., et al. (2004). Antimicrobial susceptibilities of invasive pediatric Abiotrophia and Granulicatella isolates. J. Clin. Microbiol. 42, 4323-4326. doi: 10.1128/JCM.42.9.4323-4326.2004
60. Zhong, X., Xu, H., Chen, D., Zhou, H., Hu, X., and Cheng, G. (2014). First emergence of acrAB and oqxAB mediated tigecycline resistance in clinical isolates of Klebsiella pneumoniae pre-dating the use of tigecycline in a Chinese hospital. PLoS ONE 9:e115185. doi: 10.1371/journal.pone.0115185