A novel method to discover fluoroquinolone antibiotic resistance (qnr) genes in fragmented nucleotide sequences

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Boulund, Fredrik ^a   Johnning, Anna ^b   Pereira, Mariana Buongermino ^a   Larsson, D G Joakim ^b   Kristiansson, Erik ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Antibiotic resistance; Fluoroquinolones; Hidden markov models; Metagenomics; PMQR; Qnr

Indexed keywords

NUCLEOTIDE;

ARTICLE; BACTERIAL GENE; CHROMOSOME VARIANT; GENETIC IDENTIFICATION; GENETIC VARIABILITY; METAGENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; QNR GENE; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS; SEQUENCE DATABASE;

ANTI-BACTERIAL AGENTS; BASE SEQUENCE; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI PROTEINS; FLUOROQUINOLONES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MARKOV CHAINS; METAGENOME; MODELS, GENETIC; MULTIGENE FAMILY; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS);

EID: 84870701136     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-695     Document Type: Article

References (53)

1. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 2010, 74:417-433. 10.1128/MMBR.00016-10, 2937522, 20805405.
2. Neu HC. The crisis in antibiotic resistance. Science (New York, N.Y.) 1992, 257:837-842.
3. Martinez J, Baquero F. Mutation frequencies and antibiotic resistance. Antimicrobial agents 2000, 44:1771-1777.
4. Stokes HW, Gillings MR. Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol Rev 2011, 35:790-819. 10.1111/j.1574-6976.2011.00273.x, 21517914.
5. Boucher Y, Labbate M, Koenig JE, Stokes HW. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 2007, 15:301-309. 10.1016/j.tim.2007.05.004, 17566739.
6. Gillings M, Boucher Y, Labbate M, Holmes A, Krishnan S, Holley M, Stokes HW. The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 2008, 190:5095-5100. 10.1128/JB.00152-08, 2447024, 18487337.
7. Wright GD. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 2007, 5:175-186. 10.1038/nrmicro1614, 17277795.
8. Cantón R. Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin Microbiol Infect 2009, 15(Suppl 1):20-25.
9. D'Costa VM, Griffiths E, Wright GD. Expanding the soil antibiotic resistome: exploring environmental diversity. Curr Opin Microbiol 2007, 10:481-489. 10.1016/j.mib.2007.08.009, 17951101.
10. D'Costa VM, McGrann KM, Hughes DW, Wright GD. Sampling the antibiotic resistome. Science (New York, N.Y.) 2006, 311:374-377.
11. D'Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD. Antibiotic resistance is ancient. Nature 2011, 477:457-461. 10.1038/nature10388, 21881561.
12. Martínez JL. Antibiotics and antibiotic resistance genes in natural environments. Science (New York, N.Y.) 2008, 321:365-367.
13. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 2010, 8:251-259. 10.1038/nrmicro2312, 20190823.
14. Von Groll A, Martin A, Jureen P, Hoffner S, Vandamme P, Portaels F, Palomino JC, da Silva PA. Fluoroquinolone resistance in Mycobacterium tuberculosis and mutations in gyrA and gyrB. Antimicrob Agents Chemother 2009, 53:4498-4500. 10.1128/AAC.00287-09, 2764174, 19687244.
15. Shah SQA, Nilsen H, Bottolfsen K, Colquhoun DJ, Sørum H. DNA Gyrase and Topoisomerase IV Mutations in Quinolone-Resistant Flavobacterium psychrophilum Isolated from Diseased Salmonids in Norway. Microb Drug Resist (Larchmont, N.Y.) 2012, 207-214.
16. Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet 1998, 351:797-799. 10.1016/S0140-6736(97)07322-4, 9519952.
17. Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 2006, 6:629-640. 10.1016/S1473-3099(06)70599-0, 17008172.
18. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 2009, 22:664-689. 10.1128/CMR.00016-09, 2772364, 19822894.
19. Vetting MW, Hegde SS, Fajardo JE, Fiser A, Roderick SL, Takiff HE, Blanchard JS. Pentapeptide repeat proteins. Biochemistry 2006, 45:1-10. 10.1021/bi052130w, 2566302, 16388575.
20. Bateman A, Murzin AG, Teichmann SA. Structure and distribution of pentapeptide repeats in bacteria. Protein Sci 1998, 7:1477-1480. 10.1002/pro.5560070625, 2144021, 9655353.
21. Xiong X, Bromley EHC, Oelschlaeger P, Woolfson DN, Spencer J. Structural insights into quinolone antibiotic resistance mediated by pentapeptide repeat proteins: conserved surface loops direct the activity of a Qnr protein from a gram-negative bacterium. Nucleic Acids Res 2011, 39:3917-3927. 10.1093/nar/gkq1296, 3089455, 21227918.
22. Vetting MW, Hegde SS, Wang M, Jacoby GA, Hooper DC, Blanchard JS. Structure of QnrB1, a plasmid-mediated fluoroquinolone resistance factor. J Biol Chem 2011, 286:25265-25273. 10.1074/jbc.M111.226936, 3137097, 21597116.
23. Handelsman J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 2004, 68:669. 10.1128/MMBR.68.4.669-685.2004, 539003, 15590779.
24. Kristiansson E, Hugenholtz P, Dalevi D. ShotgunFunctionalizeR: an R-package for functional comparison of metagenomes. Bioinformatics (Oxford, England) 2009, 25:2737-2738.
25. Hugenholtz P, Goebel BM, Pace NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 1998, 180:4765-4774. 107498, 9733676.
26. Streit WR, Schmitz RA. Metagenomics-the key to the uncultured microbes. Curr Opin Microbiol 2004, 7:492-498. 10.1016/j.mib.2004.08.002, 15451504.
27. Wommack KE, Bhavsar J, Ravel J. Metagenomics: read length matters. Appl Environ Microbiol 2008, 74:1453-1463. 10.1128/AEM.02181-07, 2258652, 18192407.
28. Fonseca T, Santos Freitas F, Vicente ACP. New qnr Gene Cassettes Associated with Superintegron Repeats in Vibrio cholerae O1. Emerg Infect Dis 2008, 14:1129-1131. 10.3201/eid1407.080132, 2600354, 18598639.
29. Sánchez MB, Hernández A, Rodríguez-Martínez JM, Martínez-Martínez L, Martínez JL. Predictive analysis of transmissible quinolone resistance indicates Stenotrophomonas maltophilia as a potential source of a novel family of Qnr determinants. BMC Microbiol 2008, 8:148. 10.1186/1471-2180-8-148, 2556341, 18793450.
30. Rodríguez-Martínez JM, Velasco C, Briales A, García I, Conejo MC, Pascual A. Qnr-like pentapeptide repeat proteins in gram-positive bacteria. J Antimicrob Chemother 2008, 61:1240-1243. 10.1093/jac/dkn115, 18343805.
31. qnr Numbering and Sequence http://www.lahey.org/qnrStudies.
32. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF, Rapp BA, Wheeler DL. GenBank. Nucleic Acids Res 1999, 27:12-17. 10.1093/nar/27.1.12, 148087, 9847132.
33. Seshadri R, Kravitz SA, Smarr L, Gilna P, Frazier M. CAMERA: a community resource for metagenomics. PLoS Biol 2007, 5:e75. 10.1371/journal.pbio.0050075, 1821059, 17355175.
34. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinforma 2008, 9:386.
35. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li SSS, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto J, Hansen T, Le D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Jian M, Zhou Y, Li Y, Zhang X, Guarner F, Qin N, Yang H, Wang JJ, Brunak S, Dore J, Le Paslier D, Doré J, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65. 10.1038/nature08821, 20203603.
36. Leinonen R, Sugawara H, Shumway M. The sequence read archive. Nucleic Acids Res 2011, 39:D19-D21. 10.1093/nar/gkq1019, 3013647, 21062823.
37. Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C, Weijdegård B, Söderström H, Larsson DGJ. Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 2011, 6:e17038. 10.1371/journal.pone.0017038, 3040208, 21359229.
38. Baquirin MHC, Barlow M. Evolution and recombination of the plasmidic qnr alleles. J Mol Evol 2008, 67:103-110. 10.1007/s00239-008-9131-3, 18592295.
39. Jacoby GA, Griffin CM, Hooper DC. Citrobacter spp. as a source of qnrB Alleles. Antimicrob Agents Chemother 2011, 55:4979-4984. 10.1128/AAC.05187-11, 3195048, 21844311.
40. Wang MM, Guo Q, Xu X, Wang X, Ye X, Wu S, Hooper DC. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 2009, 53:1892-1897. 10.1128/AAC.01400-08, 2681562, 19258263.
41. Velasco C, Rodríguez-Martínez JM, Briales A, de Díaz Alba P, Calvo A, Pascual A. Smaqnr, a new chromosome-encoded quinolone resistance determinant in Serratia marcescens. J Antimicrob Chemother 2010, 65:239-242. 10.1093/jac/dkp424, 19942618.
42. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang H-Y, Cohoon M, de Crécy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005, 33:5691-5702. 10.1093/nar/gki866, 1251668, 16214803.
43. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V. Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci 2010, 108:1128-1133. 3024690, 21191099.
44. Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K, Eisen JA, Heidelberg KB, Manning G, Li W, Jaroszewski L, Cieplak P, Miller CS, Li H, Mashiyama ST, Joachimiak MP, van Belle C, Chandonia J-M, Soergel DA, Zhai Y, Natarajan K, Lee S, Raphael BJ, Bafna V, Friedman R, Brenner SE, Godzik A, Eisenberg D, Dixon JE, Taylor SS, Strausberg RL, Frazier M, Venter JC. The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol 2007, 5:e16. 10.1371/journal.pbio.0050016, 1821046, 17355171.
45. Hooper SD, Dalevi D, Pati A, Mavromatis K, Ivanova NN, Kyrpides NC. Estimating DNA coverage and abundance in metagenomes using a gamma approximation. Bioinformatics (Oxford, England) 2010, 26:295-301.
46. Gilbert JA, Dupont CL. Microbial Metagenomics: Beyond the Genome. Ann Rev Mar Sci 2011, 3:347-371. 10.1146/annurev-marine-120709-142811, 21329209.
47. Gilbert JA, Meyer F, Jansson J, Gordon J, Pace N, Ley R, Fierer N, Field D, Kyrpides N, Glöckner F. The Earth Microbiome Project: Meeting report of the " 1st EMP meeting on sample selection and acquisition " at Argonne National Laboratory October 6th 2010 2010, 249-253. 3035312, 21304728.
48. Gilbert JA, Bailey M, Field D, Fierer N, Fuhrman JA, Hu B, Jansson J, Knight R, Kowalchuk GA, Kyrpides NC, Meyer F, Stevens R. The Earth Microbiome Project: The Meeting Report for the 1st International Earth Microbiome Project Conference, Shenzhen, China, June 13th-15th 2011. Stand Genomic Sci 2011, 5:243-247.
49. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol 2011, 7:e1002195. 10.1371/journal.pcbi.1002195, 3197634, 22039361.
50. Metzker ML. Sequencing technologies - the next generation. Nat Rev Genet 2010, 11:31-46. 10.1038/nrg2626, 19997069.
51. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066. 10.1093/nar/gkf436, 135756, 12136088.
52. Rice P, Longden I, Bleasby A. The European Molecular Biology Open Software Suite EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 2000, 16:276-277. 10.1016/S0168-9525(00)02024-2, 10827456.
53. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.