Small-plasmid-mediated antibiotic resistance is enhanced by increases in plasmid copy number and bacterial fitness

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 6, 2015, Pages 3335-3341

  Millan, Alvaro San ^a,c   Santos Lopez, Alfonso ^a   Ortega Huedo, Rafael ^a   Bernabe Balas, Cristina ^a   Kennedy, Sean P ^b,d   Gonzalez Zorn, Bruno ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b University of Paris Saclay   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BETA LACTAM ANTIBIOTIC; CHLORAMPHENICOL; TETRACYCLINE; ANTIINFECTIVE AGENT;

ADAPTATION; ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; GENE DOSAGE; HAEMOPHILUS INFLUENZAE; HOST; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PENICILLIN RESISTANCE; PLASMID; PRIORITY JOURNAL; COPY NUMBER VARIATION; DRUG EFFECTS; GENETICS; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; DNA COPY NUMBER VARIATIONS; DRUG RESISTANCE, MICROBIAL; HAEMOPHILUS INFLUENZAE; PLASMIDS;

EID: 84938755324     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00235-15     Document Type: Article

References (36)

1. CDC. 2013. Antibiotic resistance threats in the United States. http://www.cdc.gov/drugresistance/threat-report-2013/.
2. Gonzalez Zorn B, Escudero JA. 2012. Ecology of antimicrobial resistance: humans, animals, food and environment. Int Microbiol 15:101-109. http://dx.doi.org/10.2436/20.1501.01.163.
3. Gogarten JP, Townsend JP. 2005. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679-687. http://dx.doi.org/10.1038/nrmicro1204.
4. Nikaido H. 2009. Multidrug resistance in bacteria. Annu Rev Biochem 78: 119-146. http://dx.doi.org/10.1146/annurev.biochem.78.082907.145923.
5. Vogwill T, MacLean RC. 2015. The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach. Evol Appl 8:284-295. http://dx.doi.org/10.1111/eva.12202.
6. Harrison E, Brockhurst MA. 2012. Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol 20:262-267. http://dx.doi.org/10.1016/j.tim.2012.04.003.
7. Bouma JE, Lenski RE. 1988. Evolution of a bacteria/plasmid association. Nature 335:351-352. http://dx.doi.org/10.1038/335351a0.
8. San Millan A, Peña-Miller R, Toll-Riera M, Halbert ZV, McLean AR, Cooper BS, MacLean RC. 2014. Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids. Nat Commun 5:5208. http://dx.doi.org/10.1038/ncomms6208.
9. Tristram S, Jacobs MR, Appelbaum PC. 2007. Antimicrobial resistance in Haemophilus influenzae. Clin Microbiol Rev 20:368-389. http://dx.doi.org/10.1128/CMR.00040-06.
10. ROB-1. Antimicrob Agents Chemother 51:2260-2264. http://dx.doi.org/10.1128/AAC.00242-07.
11. Alvarado A, Garcillán-Barcia MP, de la Cruz F. 2012. A degenerate primer MOB typing (DPMT) method to classify gamma-proteobacterial plasmids in clinical and environmental settings. PLoS One 7:e40438. http://dx.doi.org/10.1371/journal.pone.0040438.
12. Cao V, Lambert T, Courvalin P. 2002. ColE1-like plasmid pIP843 of Klebsiella pneumoniae encoding extended-spectrum beta-lactamase CTXM-17. Antimicrob Agents Chemother 46:1212-1217. http://dx.doi.org/10.1128/AAC.46.5.1212-1217.2002.
13. Zioga A, Whichard JM, Kotsakis SD, Tzouvelekis LS, Tzelepi E, Miriagou V. 2009. CMY-31 and CMY-36 cephalosporinases encoded by ColE1-like plasmids. Antimicrob Agents Chemother 53:1256-1259. http://dx.doi.org/10.1128/AAC.01284-08.
14. Pallecchi L, Riccobono E, Sennati S, Mantella A, Bartalesi F, Trigoso C, Gotuzzo E, Bartoloni A, Rossolini GM. 2010. Characterization of small ColE-like plasmids mediating widespread dissemination of the qnrB19 gene in commensal enterobacteria. Antimicrob Agents Chemother 54: 678-682. http://dx.doi.org/10.1128/AAC.01160-09.
15. Chen CY, Lindsey RL, Strobaugh TP, Frye JG, Meinersmann RJ. 2010. Prevalence of ColE1-like plasmids and kanamycin resistance genes in Salmonella enterica serovars. Appl Environ Microbiol 76:6707-6714. http://dx.doi.org/10.1128/AEM.00692-10.
16. Kehrenberg C, Hopkins KL, Threlfall EJ, Schwarz S. 2007. Complete nucleotide sequence of a small qnrS1-carrying plasmid from Salmonella enterica subsp. enterica Typhimurium DT193. J Antimicrob Chemother 60:903-905. http://dx.doi.org/10.1093/jac/dkm283.
17. San Millan A, Escudero JA, Gutierrez B, Hidalgo L, Garcia N, Llagostera M, Dominguez L, Gonzalez-Zorn B. 2009. Multiresistance in Pasteurella multocida is mediated by coexistence of small plasmids. Antimicrob Agents Chemother 53:3399-3404. http://dx.doi.org/10.1128/AAC.01522-08.
18. ROB-1: fitness cost and interspecies dissemination. Antimicrob Agents Chemother 54:1506-1511. http://dx.doi.org/10.1128/AAC.01489-09.
19. San Millan A, Giufré M, Escudero JA, Hidalgo L, Gutierrez B, Cerquetti M, Gonzalez-Zorn B. 2011. Contribution of ROB-1 and PBP3 mutations to the resistance phenotype of a β-lactamase-positive amoxicillin/clavulanic acid-resistant Haemophilus influenzae carrying plasmid pB1000 in Italy. J Antimicrob Chemother 66:96-99. http://dx.doi.org/10.1093/jac/dkq392.
20. ROB-1 presence on pB1000 in Haemophilus influenzae is widespread, and variable cefaclor resistance is associated with altered penicillin-binding proteins. Antimicrob Agents Chemother 54:4945-4947. http://dx.doi.org/10.1128/AAC.00263-10.
21. Lancashire JF, Terry TD, Blackall PJ, Jennings MP. 2005. Plasmidencoded TetB tetracycline resistance in Haemophilus parasuis. Antimicrob Agents Chemother 49:1927-1931. http://dx.doi.org/10.1128/AAC.49.5.1927-1931.2005.
22. de Toro M, Rodríguez I, Rojo-Bezares B, Helmuth R, Torres C, Guerra B, Sáenz Y. 2013. pMdT1, a small ColE1-like plasmid mobilizing a new variant of the aac(6=)-Ib-cr gene in Salmonella enterica serovar Typhimurium. J Antimicrob Chemother 68:1277-80. http://dx.doi.org/10.1093/jac/dkt001.
23. Clinical and Laboratory Standards Institute. 2009. Performance standards for antimicrobial susceptibility testing; 19th ed. Approved standard M100-S19. CLSI, Wayne, PA.
24. Björkman J, Andersson DI. 2000. The cost of antibiotic resistance from a bacterial perspective. Drug Resist Updat 3:237-245. http://dx.doi.org/10.1054/drup.2000.0147.
25. Lenski RE. 1991. Quantifying fitness and gene stability in microorganisms, p 173-192. In Ginzburg LR (ed), Assessing ecological risks of biotecnology. Butterworth-Heinemann, Boston, MA.
26. San Millan A, Heilbron K, MacLean RC. 2014. Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations. ISME J 8:601-612. http://dx.doi.org/10.1038/ismej.2013.182.
27. Providenti MA, O'Brien JM, Ewing RJ, Paterson ES, Smith ML. 2006. The copy-number of plasmids and other genetic elements can be determined by SYBR-Green-based quantitative real-time PCR. J Microbiol Methods 65:476-487. http://dx.doi.org/10.1016/j.mimet.2005.09.007.
28. Pinheiro JC, Bates DM. 2000. Mixed-effects models in S and S-PLUS. Springer Science & Business Media, Berlin, Germany.
29. Meyers BR, Wilkinson P, Mendelson MH, Walsh S, Bournazos C, Hirschman SZ. 1991. Pharmacokinetics of ampicillin-sulbactam in healthy elderly and young volunteers. Antimicrob Agents Chemother 35: 2098-2101. http://dx.doi.org/10.1128/AAC.35.10.2098.
30. Lacy MK, Lu W, Xu X, Tessier PR, Nicolau DP, Quintiliani R, Nightingale CH. 1999. Pharmacodynamic comparisons of levofloxacin, ciprofloxacin, and ampicillin against Streptococcus pneumoniae in an in vitro model of infection. Antimicrob Agents Chemother 43:672-677.
31. Uhlin BE, Nordström K. 1977. R plasmid gene dosage effects in Escherichia coli K-12: copy mutants of the R plasmic R1drd-19. Plasmid 1:1-7. http://dx.doi.org/10.1016/0147-619X(77)90003-8.
32. Lüthje P, von Köckritz-Blickwede M, Schwarz S. 2007. Identification and characterization of nine novel types of small staphylococcal plasmids carrying the lincosamide nucleotidyltransferase gene lnu(A). J Antimicrob Chemother 59:600-606. http://dx.doi.org/10.1093/jac/dkm008.
33. Patnaik PR. 2000. An evaluation of models for the effect of plasmid copy number on bacterial growth rate. Biotechnol Lett 22:1719-1725. http://dx.doi.org/10.1023/A:1005696401254.
34. Harrison E, Koufopanou V, Burt A, Maclean RC. 2012. The cost of copy number in a selfish genetic element: the 2-μm plasmid of Saccharomyces cerevisiae. J Evol Biol 25:2348-2356. http://dx.doi.org/10.1111/j.1420-9101.2012.02610.x.
35. Albarracín Orio AG, Piñas GE, Cortes PR, Cian MB, Echenique J. 2011. Compensatory evolution of pbp mutations restores the fitness cost imposed by β-lactam resistance in Streptococcus pneumoniae. PLoS Pathog 7:e1002000. http://dx.doi.org/10.1371/journal.ppat.1002000.
36. Marcusson LL, Frimodt-Møller N, Hughes D. 2009. Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 5:e1000541. http://dx.doi.org/10.1371/journal.ppat.1000541.