The Tandem Repeats Enabling Reversible Switching between the Two Phases of β-Lactamase Substrate Spectrum

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β-lactamases can adapt to new antibiotics by mutations in their genes. The original and the extended substrate spectrums of β-lactamases define two phases of catalytic activity, and the conversion by point mutations is unidirectional from the initial to the new spectrum. We describe duplication mutations that enable reversible switching between the substrate spectrums, increasing the adaptability of the bacterium. We provide evidence supporting that two distinct groups of short sequences mediated the formation of DNA duplications in β-lactamases: direct repeats and novel elements that we named, SCSs (same-strand complementary sequences). Our study suggests that DNA duplication processes mediated by both direct repeats and SCSs are not just limited to the β-lactamase genes but comprise a fundamental mechanism in bacterial genome evolution.

Vyšlo v časopise: The Tandem Repeats Enabling Reversible Switching between the Two Phases of β-Lactamase Substrate Spectrum. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004640
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004640

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Zdroje

1. GemayelR, VincesMD, LegendreM, VerstrepenKJ (2010) Variable Tandem Repeats Accelerate Evolution of Coding and Regulatory Sequences. Annual Review of Genetics 44: 445–477.

2. TreangenTJ, AbrahamA-L, TouchonM, RochaEPC (2009) Genesis, effects and fates of repeats in prokaryotic genomes. FEMS Microbiology Reviews 33: 539–571.

3. MoxonER, RaineyPB, NowakMA, LenskiRE (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Current Biology 4: 24–33.

4. van der WoudeMW, BäumlerAJ (2004) Phase and Antigenic Variation in Bacteria. Clinical Microbiology Reviews 17: 581–611.

5. ArpinC, LabiaR, AndreC, FrigoC, El HarrifZ, et al. (2001) SHV-16, a β-Lactamase with a Pentapeptide Duplication in the Omega Loop. Antimicrobial Agents and Chemotherapy 45: 2480–2485.

6. JelschC, MoureyL, MassonJM, SamamaJP (1993) Crystal structure of Escherichia coli TEM1 beta-lactamase at 1.8 A resolution. Proteins 16: 364–383.

7. NukagaM, HarutaS, TanimotoK, KogureK, TaniguchiK, et al. (1995) Molecular Evolution of a Class C -Lactamase Extending Its Substrate Specificity. Journal of Biological Chemistry 270: 5729–5735.

8. BushK, FisherJF (2011) Epidemiological Expansion, Structural Studies, and Clinical Challenges of New β-Lactamases from Gram-Negative Bacteria. Annual Review of Microbiology 65: 455–478.

9. PitoutJDD, LauplandKB (2008) Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. The Lancet Infectious Diseases 8: 159–166.

10. DrawzSM, BonomoRA (2010) Three Decades of beta-Lactamase Inhibitors. Clin Microbiol Rev 23: 160–201.

11. BrettPJ, DeShazerD, WoodsDE (1998) Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48 Pt 1: 317–320.

12. YiH, ChoK-H, ChoYS, KimK, NiermanWC, et al. (2012) Twelve Positions in a β-Lactamase That Can Expand Its Substrate Spectrum with a Single Amino Acid Substitution. PLoS ONE 7: e37585.

13. YiH, KimK, ChoK-H, JungO, KimHS (2012) Substrate Spectrum Extension of PenA in Burkholderia thailandensis with a Single Amino Acid Deletion, Glu168del. Antimicrobial Agents and Chemotherapy 56: 4005–4008.

14. TribuddharatC, MooreRA, BakerP, WoodsDE (2003) Burkholderia pseudomallei class a beta-lactamase mutations that confer selective resistance against ceftazidime or clavulanic acid inhibition. Antimicrobial Agents and Chemotherapy 47: 2082–2087.

15. PoirelL, Rodriguez-MartinezJ-M, PlésiatP, NordmannP (2009) Naturally Occurring Class A ß-Lactamases from the Burkholderia cepacia Complex. Antimicrobial Agents and Chemotherapy 53: 876–882.

16. SongH, HwangJ, YiH, UlrichRL, YuY, et al. (2010) The Early Stage of Bacterial Genome-Reductive Evolution in the Host. PLoS Pathog 6: e1000922.

17. WuthiekanunV, PeacockSJ (2006) Management of melioidosis. Expert Rev Anti Infect Ther 4: 445–455.

18. PalzkillT, LeQQ, VenkatachalamKV, LaRoccoM, OceraH (1994) Evolution of antibiotic resistance: several different amino acid substitutions in an active site loop alter the substrate profile of beta-lactamase. Mol Microbiol 12: 217–229.

19. PetrosinoJF, PalzkillT (1996) Systematic mutagenesis of the active site omega loop of TEM-1 beta- lactamase. J Bacteriol 178: 1821–1828.

20. HayesF, HalletB, CaoY (1997) Insertion Mutagenesis as a Tool in the Modification of Protein Function. Journal of Biological Chemistry 272: 28833–28836.

21. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.

22. SarovichDS, PriceEP, Von SchulzeAT, CookJM, MayoM, et al. (2012) Characterization of Ceftazidime Resistance Mechanisms in Clinical Isolates of Burkholderia pseudomallei from Australia. PLoS ONE 7: e30789.

23. WangX, MinasovG, ShoichetBK (2002) Evolution of an Antibiotic Resistance Enzyme Constrained by Stability and Activity Trade-offs. Journal of Molecular Biology 320: 85–95.

24. SalverdaML, De VisserJA, BarlowM (2010) Natural evolution of TEM-1 beta-lactamase: experimental reconstruction and clinical relevance. FEMS Microbiol Rev 34: 1015–1036.

25. AnderssonDI, HughesD (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Micro 8: 260–271.

26. BicharaM, WagnerJ, LambertIB (2006) Mechanisms of tandem repeat instability in bacteria. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 598: 144–163.

27. CirzRT, ChinJK, AndesDR, de Crécy-LagardV, CraigWA, et al. (2005) Inhibition of Mutation and Combating the Evolution of Antibiotic Resistance. PLoS Biol 3: e176.

28. BeaberJW, HochhutB, WaldorMK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427: 72–74.

29. GardnerTS, CantorCR, CollinsJJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339–342.

30. MirkinSM (2007) Expandable DNA repeats and human disease. Nature 447: 932–940.

31. van de SandeJ, RamsingN, GermannM, ElhorstW, KalischB, et al. (1988) Parallel stranded DNA. Science 241: 551–557.

32. CuberoE, AviñóA, de la TorreBG, FriedenM, EritjaR, et al. (2002) Hoogsteen-Based Parallel-Stranded Duplexes of DNA. Effect of 8-Amino-purine Derivatives. Journal of the American Chemical Society 124: 3133–3142.

33. ParvathyVR, BhaumikSR, CharyKVR, GovilG, LiuK, et al. (2002) NMR structure of a parallel-stranded DNA duplex at atomic resolution. Nucleic Acids Research 30: 1500–1511.

34. NikolovaEN, KimE, WiseAA, O'BrienPJ, AndricioaeiI, et al. (2011) Transient Hoogsteen base pairs in canonical duplex DNA. Nature 470: 498–502.

35. TchurikovNA (1992) Natural DNA sequences complementary in the same direction: evidence for parallel biosynthesis? Genetica 87: 113–117.

36. BallEV, StensonPD, AbeysingheSS, KrawczakM, CooperDN, et al. (2005) Microdeletions and microinsertions causing human genetic disease: common mechanisms of mutagenesis and the role of local DNA sequence complexity. Human Mutation 26: 205–213.

37. KimHS, YiH, MyungJ, PiperKR, FarrandSK (2008) Opine-Based Agrobacterium Competitiveness: Dual Expression Control of the Agrocinopine Catabolism (acc) Operon by Agrocinopines and Phosphate Levels. J Bacteriol 190: 3700–3711.

38. JoyceLF, DownesJ, StockmanK, AndrewJH (1992) Comparison of five methods, including the PDM Epsilometer test (E test), for antimicrobial susceptibility testing of Pseudomonas aeruginosa. J Clin Microbiol 30: 2709–2713.

39. WiegandI, HilpertK, HancockREW (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protocols 3: 163–175.

40. KeenNT, TamakiS, KobayashiD, TrollingerD (1988) Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70: 191–197.

41. ThongdeeM, GallagherLA, SchellM, DharakulT, SongsivilaiS, et al. (2008) Targeted mutagenesis of Burkholderia thailandensis and Burkholderia pseudomallei through natural transformation of PCR fragments. Appl Environ Microbiol

42. Simon R, Priefer U, Puhler A (1983) Vector plasmids for in vivo and in vitro manipulations of gram-negative bacteria. Springer-Verlag KG, Berlin, Germany.

43. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

44. MerriamJJ, MathurR, Maxfield-BoumilR, IsbergRR (1997) Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Infection and Immunity 65: 2497–2501.

45. SongH, HwangJ, MyungJ, SeoH, YiH, et al. (2009) Simple sequence repeat (SSR)-based gene diversity in Burkholderia pseudomallei and Burkholderia mallei. Mol Cells 27: 237–241.

46. CaporasoJG, BittingerK, BushmanFD, DeSantisTZ, AndersenGL, et al. (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266–267.

47. AmblerRP, CoulsonAF, FrereJM, GhuysenJM, JorisB, et al. (1991) A standard numbering scheme for the class A beta-lactamases. Biochem J 276(Pt 1): 269–270.