Survival and Evolution of a Large Multidrug Resistance Plasmid in New Clinical Bacterial Hosts

Molecular Biology and Evolution

Volumn 33, Issue 11, 2016, Pages 2860-2873

  Porse, Andreas ^a   Schønning, Kristian ^b,c   Munck, Christian ^a   Sommer, Morten O A ^a  

^a Chalmers University of Technology   (Denmark)

^b HVIDOVRE HOSPITAL   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

antibiotic resistance; clinical isolates; ESBL plasmid evolution; experimental evolution; horizontal gene transfer; IS26 restructuring

Indexed keywords

ESCHERICHIA COLI; GENE DELETION; GENE INSERTION SEQUENCE; HORIZONTAL GENE TRANSFER; HOST RANGE; KLEBSIELLA PNEUMONIAE; MULTIDRUG RESISTANCE; NONHUMAN; PLASMID; PLASTICITY; POPULATION MODEL; SPECIES; STATISTICAL MODEL; VERTICAL TRANSMISSION; ADAPTATION; ANTIBIOTIC RESISTANCE; BACTERIUM CONJUGATION; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR EVOLUTION; TRANSPOSON;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; TRANSPOSON;

ADAPTATION, BIOLOGICAL; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CONJUGATION, GENETIC; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MICROBIAL; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; KLEBSIELLA PNEUMONIAE; MICROBIAL SENSITIVITY TESTS; PLASMIDS;

EID: 84994494351     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw163     Document Type: Article

References (60)

1. Aziz RK, Bartels D, Best A., DeJongh M, Disz T, Edwards R., Formsma K, Gerdes S, Glass EM, Kubal M, et al. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75.
2. Bergstrom CT, Lipsitch M, Levin BR. 2000. Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155:1505-1519.
3. Bouma J, Lenski R. 1988. Evolution of a bacteria/plasmid association. Nature 335:
4. Bradley DE, Taylor DE, Cohen DR. 1980. Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J Bacteriol. 143:1466-1470.
5. Bush K, Fisher JF. 2011. Epidemiological expansion, structural studies, and clinical challenges of new b-lactamases from Gram-negative bacteria. Annu Rev Microbiol. 65:455-478.
6. Carattoli A. 2009. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother. 53:2227-2238.
7. Carattoli A. 2013. Plasmids and the spread of resistance. Int J Med Microbiol. 303:298-304.
8. Conlan S, Thomas PJ, Deming C, Park M, Lau AF, Dekker JP, Snitkin ES, Clark TA, Luong K, Song Y, et al. 2014. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-pro-ducing Enterobacteriaceae. Sci Transl Med. 6:254ra126.
9. Cullik A, Pfeifer Y, Prager R, Von Baum H, Witte W. 2010. A novel IS26 structure surrounds blaCTX-M genes in different plasmids from German clinical Escherichia coli isolates. J Med Microbiol. 59:580-587.
10. Curiao T, Canton R, Garcillan-Barcia MP, De La Cruz F, Baquero F, Coque TM. 2011. Association of composite IS26-sul3 elements with highly transmissible IncI1 plasmids in extended-spectrum-b-lactamase-producing Escherichia coli clones from humans. Antimicrob Agents Chemother. 55:2451-2457.
11. Dahlberg C, Chao L. 2003. Amelioration of the cost of conjugative plasmid carriage in Escherichia coli K12. Genetics 165:1641-1649.
12. Datsenko K, Wanner BL. 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.
13. Davies J, Davies D. 2010. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 74:417-433.
14. De Gelder L, Ponciano JM, Joyce P, Top EM. 2007. Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 153:452-463.
15. De Gelder L, Williams JJ, Ponciano JM, Sota M, Top EM. 2008. Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid. Genetics 178:2179-2190.
16. Dhillon RH-P, Clark J. 2012. ESBLs: a clear and present danger? Crit Care Res Pract. 2012:625170.
17. Dionisio F, Conceição IC, Marques CR, Fernandes L, Gordo I. 2005. The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol Lett. 1:250-252.
18. Doyle M, Fookes M, Ivens A, Mangan MW, Wain J, Dorman CJ. 2007. An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315:251-252.
19. Eikmeyer F, Hadiati A, Szczepanowski R, Wibberg D, Schneiker-Bekel S, Rogers LM, Brown CJ, Top EM, Pühler A, Schlüter A. 2012. The complete genome sequences of four new IncN plasmids from wastewater treatment plant effluent provide new insights into IncN plasmid diversity and evolution. Plasmid 68:13-24.
20. Fernandez-Lopez R, del Campo I, Revilla C, Cuevas A, de la Cruz F. 2014. Negative feedback and transcriptional overshooting in a regulatory network for horizontal gene transfer. PLoS Genet. 10.
21. Frost LS, Leplae R, Summers AO, Toussaint A 2005. Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol. 3:722-732.
22. Ghigo JM. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442-445.
23. Gordon DM, Riley M. 1992. A theoretical and experimental analysis of bacterial growth in the bladder. Mol Microbiol. 6:555-562.
24. Guynet C, Cuevas A, Moncalian G, de la Cruz F. 2011. The stb operon balances the requirements for vegetative stability and conjugative transfer of plasmid R388. PLoS Genet. 7:e1002073.
25. Harmer CJ, Moran R, Hall RM, Harmer CJ, Moran R Hall RM. 2014 Movement of IS 26 -associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS 26 and preferentially inserts adjacent to another IS 26. 5:1-9.
26. Harrison E, Brockhurst M. 2012. Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol. 20:262-267.
27. Harrison E, Guymer D, Spiers AJ, Paterson S, Brockhurst MA. 2015. Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Curr Biol. 25:2034-2039.
28. He S, Hickman B, Varani AM, Siguier P, Chandler M, Dekker J P. 2015. Insertion sequence IS 26 reorganizes plasmids in clinically isolated multidrug-resistant bacteria by replicative transposition. MBio 6:1-14.
29. Heuer H, Fox RE, Top EM. 2007. Frequent conjugative transfer accelerates adaptation of a broad-host-range plasmid to an unfavorable Pseudomonas putida host. FEMS Microbiol Ecol. 59:738-748.
30. Jain A, Srivastava P. 2013. Broad host range plasmids. FEMS Microbiol Lett. 348:87-96.
31. Labat F, Pradillon O, Garry L, Peuchmaur M, Fantin B, Denamur E 2005. Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. FEMS Immunol Med Microbiol. 44:317-321.
32. Loftie-Eaton W, Yano H, Burleigh S, Simmons RS, Hughes JM, Rogers LM, Hunter SS, Settles ML, Forney LJ, Ponciano JM, et al. 2015. Evolutionary paths that expand plasmid host-range: implications for spread of antibiotic resistance. Mol Biol Evol. 33:885-897.
33. Mazodier P, Davies J. 1991. Gene transfer between distantly related bacteria. Annu Rev Genet. 25:147-171.
34. Miriagou V, Papagiannitsis CC, Kotsakis SD, Loli a, Tzelepi E, Legakis NJ, Tzouvelekis LS. 2010. Sequence of pNL194, a 79.3-kilobase IncN plasmid carrying the blaVIM-1 metallo-beta-lactamase gene in Klebsiella pneumoniae. Antimicrob Agents Chemother. 54:4497-4502.
35. Modi RI, Wilke CM, Rosenzweig RF, Adams J. 1991. Plasmid macro-evolution: selection of deletions during adaptation in a nutrient-limited environment. Genetica 84:195-202.
36. More MI, Pohlman RF, Winans SC 1996. Genes encoding the pKM101 conjugal mating pore are negatively regulated by the plasmid-encoded KorA and KorB proteins. J Bacteriol. 178:4392-4399.
37. Mruk I, Kobayashi I. 2014. To be or not to be: regulation of restriction-modification systems and other toxin-antitoxin systems. Nucleic Acids Res. 42:70-86.
38. Nilsson AI, Berg OG, Aspevall O, Andersson DI, Kahlmeter G. 2003. Biological costs and mechanisms of fosfomycin resistance in Escherichia coli. Society 47:2850-2858.
39. Norman A Hansen LH, Sørensen SJ. 2009. Conjugative plasmids: vessels of the communal gene pool. Philos Trans R Soc Lond B Biol Sci. 364:2275-2289.
40. Partridge SR Zong Z, Iredell JR 2011. Recombination in IS26 and Tn2 in the evolution of multiresistance regions carrying blaCTX-M-15 on conjugative IncF plasmids from Escherichia coli. Antimicrob Agents Chemother. 55:4971-4978.
41. Proctor GN. 1994. Mathematics of microbial plasmid instability and subsequent differential growth of plasmid-free and plasmid-containing cells, relevant to the analysis of experimental colony number data. Plasmid 32:101-130.
42. Qi Q, Toll-Riera M, Heilbron K, Preston GM, MacLean RC 2016. The genomic basis of adaptation to the fitness cost of rifampicin resistance in Pseudomonas aeruginosa. Proc R Soc B Biol Sci. 283:20152452.
43. Rodriguez-Beltran J, Tourret J. 2015. High recombinant frequency in extraintestinal pathogenic Escherichia coli strains. Mol Biol Evol. 32:1708-1716.
44. San Millan A Pena-Miller R Toll-Riera M, Halbert ZV, McLean R Cooper BS, MacLean RC. 2014. Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids. Nat Commun. 5:5208.
45. San Millan A Toll-Riera M, Qi Q, MacLean RC. 2015. Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa. Nat Commun. 6:6845.
46. Shiga Y, Sekine Y, Kano Y, Ohtsubo E 2001. Involvement of H-NS in transpositional recombination mediated by IS1. J Bacteriol. 183:2476-2484
47. Shintani M, Sanchez ZK, Kimbara K. 2015. Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front Microbiol. 6:1-16.
48. Shoemaker NB, Vlamakis H, Hayes K, Salyers AA 2001. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol. 67:561-568.
49. Simonsen L 1991. The existence conditions for bacterial plasmids: theory and reality. Microb Ecol. 187-205.
50. Smillie C, Garcillan-Barcia MP, Francia MV, Rocha EPC, de la Cruz F. 2010. Mobility of plasmids. Microbiol Mol Biol Rev. 74:434-452.
51. Sommer MO, Dantas G 2011. Antibiotics and the resistant microbiome. Curr Opin Microbiol. 14:556-563.
52. Sommer MO, Dantas G, Church GM. 2009. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325:1128-1131.
53. Sota M, Yano H, Hughes JM, Daughdrill GW, Abdo Z, Forney LJ, Top EM 2010. Shifts in the host range of a promiscuous plasmid through parallel evolution of its replication initiation protein. ISMEJ. 4:1568-1580.
54. Soucy SM, HuangJ, Gogarten JP. 2015. Horizontal gene transfer: building the web of life. Nat Rev Genet. 16:472-482
55. Tamminen M, Virta M, Fani R Fondi M. 2012 Large-scale analysis of plasmid relationships through gene-sharing networks. Mol Biol Evol. 29:1225-1240.
56. Turner P, Cooper V, Lenski R 1998. Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution (N. Y.) 52:315-329.
57. World Health Organization. 2014. Antimicrobial resistance: global report on surveillance 2014. Geneva: WHO Press. Available from: Error! Hyperlink reference not valid..
58. Wiegand I, Hilpert K, Hancock REW. 2008 Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 3:163-175.
59. Yu D, Ellis HM, Lee EC, Jenkins N, Copeland NG, Court DL 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA. 97:5978-5983.
60. Zahrl D, Wagner M, Bischof K, Koraimann G 2006. Expression and assembly of a functional type IV secretion system elicit extracyto-plasmic and cytoplasmic stress responses in Escherichia coli. J Bacteriol. 188:6611-6621.