Reversing resistance: Different routes and common themes across pathogens

Proceedings of the Royal Society B: Biological Sciences

Volumn 284, Issue 1863, 2017, Pages

  Allen, Richard C ^a   Engelstädter, Jan ^b   Bonhoeffer, Sebastian ^a   McDonald, Bruce A ^a   Hall, Alex R ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Antimicrobials; Biocides; Fungicides; Reversing resistance

Indexed keywords

ANTIBIOTICS; ANTIMICROBIAL ACTIVITY; EPIDEMIOLOGY; FITNESS; GENOTYPE; PATHOGEN; PESTICIDE; PESTICIDE RESISTANCE; PREDICTION;

DISINFECTANT AGENT;

ANTIBIOTIC RESISTANCE; GENETICS; GENOTYPE; MOLECULAR EVOLUTION; POPULATION GENETICS; REPRODUCTIVE FITNESS;

DISINFECTANTS; DRUG RESISTANCE, MICROBIAL; EVOLUTION, MOLECULAR; GENETIC FITNESS; GENETICS, POPULATION; GENOTYPE;

EID: 85030709439     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2017.1619     Document Type: Review

References (97)

1. Chung A, Perera R, Brueggemann AB, Elamin AE, Harnden A, Mayon-White R, Smith S, Crook DW, Mant D. 2007 Effect of antibiotic prescribing on antibiotic resistance in individual children in primary care: prospective cohort study. BMJ 335, 429. (doi: 10.1136/bmj.39274.647465.BE)
2. Kublin JG et al. 2003 Reemergence of chloroquinesensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J. Infect. Dis. 187, 1870-1875. (doi: 10.1086/375419)
3. Sun L, Klein EY, Laxminarayan R. 2012 Seasonality and temporal correlation between community antibiotic use and resistance in the United States. Clin. Infect. Dis. 55, 687-694. (doi: 10.1093/cid/cis509)
4. van Leeuwen WJ, Guinee P, Kampelmacher EH, Manten A, van Schothorst M, Voogd CE. 1979 Decrease of drug resistance in Salmonella in the Netherlands. Antimicrob. Agents Chemother. 16, 237-239. (doi: 10.1128/AAC.16.2.237)
5. Aarestrup FM. 2000 Characterization of glycopeptide-resistant Enterococcus faecium (GRE) from broilers and pigs in Denmark: genetic evidence that persistence of GRE in pig herds is associated with coselection by resistance to macrolides. J. Clin. Microbiol. 38, 2774-2777.
6. Enne VI, Livermore DM, Stephens P, Hall LM. 2001 Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 357, 1325-1328. (doi: 10.1016/S0140-6736(00)04519-0)
7. Heuer OE, Pedersen K, Andersen JS, Madsen M. 2002 Vancomycin-resistant enterococci (VRE) in broiler flocks 5 years after the avoparcin ban. Microb. Drug Resist. 8, 133-138. (doi: 10.1089/107662902760190680)
8. Sundqvist M, Geli P, Andersson DI, Sjolund-Karlsson M, Runehagen A, Cars H, Abelson-Storby K, Cars O, Kahlmeter G. 2010 Little evidence for reversibility of trimethoprim resistance after a drastic reduction in trimethoprim use. J. Antimicrob. Chemother. 65, 350-360. (doi: 10.1093/jac/dkp387)
9. Comas I et al. 2012 Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat. Genet. 44, 106-112. (doi: 10.1038/ng.1038)
10. Baym M, Stone LK, Kishony R. 2016 Multidrug evolutionary strategies to reverse antibiotic resistance. Science 351, aad3292. (doi: 10.1126/science.aad3292)
11. Foucault ML, Depardieu F, Courvalin P, Grillot-Courvalin C. 2010 Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci. Proc. Natl Acad. Sci. USA 107, 16964-16969. (doi: 10.1073/pnas.1006855107)
12. Andersson DI, Hughes D. 2010 Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8, 260-271. (doi: 10.1038/nrmicro2319)
13. Levin BR, Baquero F, Johnsen PJ. 2014 A modelguided analysis and perspective on the evolution and epidemiology of antibiotic resistance and its future. Curr. Opin. Microbiol. 19, 83-89. (doi: 10.1016/j.mib.2014.06.004)
14. World Health Organization. 2012 Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae.
15. Jansen G et al. 2016 Association between clinical antibiotic resistance and susceptibility of Pseudomonas in the cystic fibrosis lung. Evol. Med. Public Health 2016, 182-194. (doi: 10.1093/emph/eow016)
16. Linde CC, Zhan J, McDonald BA. 2002 Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92, 946-955. (doi: 10.1094/PHYTO.2002.92.9.946)
17. Zhan J, Stefanato FL, McDonald BA. 2006 Selection for increased cyproconazole tolerance in Mycosphaerella graminicola through local adaptation and in response to host resistance. Mol. Plant Pathol. 7, 259-268. (doi: 10.1111/j.1364-3703.2006.00336.x)
18. Pereira DA, McDonald BA, Brunner PC. 2017 Mutations in the CYP51 gene reduce DMI sensitivity in Parastagonospora nodorum populations in Europe and China. Pest Manag. Sci. 73, 1503-1510. (doi: 10.1002/ps.4486)
19. Mohd-Assaad N, McDonald BA, Croll D. 2016 Multilocus resistance evolution to azole fungicides in fungal plant pathogen populations. Mol. Ecol. 25, 6124-6142. (doi: 10.1111/mec.13916)
20. Gifford DR, MacLean RC. 2013 Evolutionary reversals of antibiotic resistance in experimental populations of Pseudomonas aeruginosa. Evolution 67, 2973-2981. (doi: 10.1111/evo.12158)
21. Yang WL et al. 2015 Persistence of transmitted HIV-1 drug resistance mutations associated with fitness costs and viral genetic backgrounds. PLoS Pathog. 11, e1004722. (doi: 10.1371/journal.ppat.1004722)
22. Medaney F, Dimitriu T, Ellis RJ, Raymond B. 2016 Live to cheat another day: bacterial dormancy facilitates the social exploitation of beta-lactamases. ISME J. 10, 778-787. (doi: 10.1038/ismej.2015.154)
23. Pader V. 2016 Staphylococcus aureus inactivates daptomycin by releasing membrane phospholipids. Nat. Microbiol. 2, 16194. (doi: 10.1038/nmicrobiol.2016.194)
24. Paterson PJ, Seaton S, Prentice HG, Kibbler CC. 2003 Treatment failure in invasive aspergillosis: susceptibility of deep tissue isolates following treatment with amphotericin B. J. Antimicrob. Chemother. 52, 873-876. (doi: 10.1093/jac/dkg434)
25. Vincent BM, Lancaster AK, Scherz-Shouval R, Whitesell L, Lindquist S, Mitchell AP. 2013 Fitness trade-offs restrict the evolution of resistance to amphotericin B. PLoS Biol. 11, e1001692. (doi: 10.1371/journal.pbio.1001692)
26. Laufer MK, Takala-Harrison S, Dzinjalamala FK, Stine OC, Taylor TE, Plowe CV. 2010 Return of chloroquine-susceptible falciparum malaria in Malawi was a reexpansion of diverse susceptible parasites. J. Infect. Dis. 202, 801-808. (doi: 10.1086/655659)
27. Suzuki F, Yamaguchi J, Koba A, Nakajima T, Arai M. 2010 Changes in fungicide resistance frequency and population structure of Pyricularia oryzae after discontinuance of MBI-D fungicides. Plant Dis. 94, 329-334. (doi: 10.1094/PDIS-94-3-0329)
28. Suzuki F, Arai M, Yamaguchi J. 2007 Genetic analysis of Pyricularia grisea population by rep-PCR during development of resistance to scytalone dehydratase inhibitors of melanin biosynthesis. Plant Dis. 91, 176-184. (doi: 10.1094/PDIS-91-2-0176)
29. Secor GA, Rivera VV, Khan MFR, Gudmestad NC. 2010 Monitoring fungicide sensitivity of Cercospora beticola of sugar beet for disease management decisions. Plant Dis. 94, 1272-1282. (doi: 10.1094/PDIS-07-09-0471)
30. Nagaev I, Björkman J, Andersson DI, Hughes D. 2001 Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol. Microbiol. 40, 433-439. (doi: 10.1046/j.1365-2958.2001.02389.x)
31. Castro H et al. 2013 Persistence of HIV-1 transmitted drug resistance mutations. J. Infect. Dis. 208, 1459-1463. (doi: 10.1093/infdis/jit345)
32. Levin BR, Perrot V, Walker N. 2000 Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154, 985-997.
33. Lindgren PK, Marcusson LL, Sandvang D, Frimodt-Moller N, Hughes D. 2005 Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections. Antimicrob. Agents Chemother. 49, 2343-2351. (doi: 10.1128/AAC.49.6.2343-2351.2005)
34. Brandis G, Wrande M, Liljas L, Hughes D. 2012 Fitness-compensatory mutations in rifampicinresistant RNA polymerase. Mol. Microbiol. 85, 142-151. (doi: 10.1111/j.1365-2958.2012.08099.x)
35. Björkman J et al. 2000 Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287, 1479-1482. (doi: 10.1126/science.287.5457.1479)
36. Schulzzur Wiesch PS, Engelstädter J, Bonhoeffer S. 2010 Compensation of fitness costs and reversibility of antibiotic resistance. Antimicrob. Agents Chemother. 54, 2085-2095. (doi: 10.1128/AAC.01460-09)
37. Moura de Sousa J, Balbontín R, Durão P, Gordo I. 2017 Multidrug-resistant bacteria compensate for the epistasis between resistances. PLoS Biol. 15, e2001741. (doi: 10.1371/journal.pbio.2001741)
38. Borrell S, Teo Y, Giardina F, Streicher EM, Klopper M, Feldmann J, Müller B, Victor TC, Gagneux S. 2013 Epistasis between antibiotic resistance mutations drives the evolution of extensively drug-resistant tuberculosis. Evol. Med. Public Health 1, 65-74. (doi: 10.1093/emph/eot003)
39. Trindade S, Sousa A, Gordo I. 2012 Antibiotic resistance and stress in the light of Fisher’s model. Evolution 66, 3815-3824. (doi: 10.1111/j.1558-5646.2012.01722.x)
40. Cuevas JM, Geller R, Garijo R, López-Aldeguer J, Sanjuán R, Rowland-Jones SL. 2015 Extremely high mutation rate of HIV-1 in vivo. PLoS Biol. 13, e1002251. (doi: 10.1371/journal.pbio.1002251)
41. Dykes C, Demeter LM. 2007 Clinical significance of human immunodeficiency virus type 1 replication fitness. Clin. Microbiol. Rev. 20, 550-578. (doi: 10.1128/CMR.00017-07)
42. Pingen M, Nijhuis M, de Bruijn JA, Boucher CAB, Wensing AMJ. 2011 Evolutionary pathways of transmitted drug-resistant HIV-1. J. Antimicrob. Chemother. 66, 1467-1480. (doi: 10.1093/jac/dkr157)
43. 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. (doi: 10.1099/mic.0.2006/001784-0)
44. Subbiah M, Top EM, Shah DH, Call DR. 2011 Selection pressure required for long-term persistence of blaCMY-2-positive IncA/C plasmids. Appl. Environ. Microbiol. 77, 4486-4493. (doi: 10.1128/AEM.02788-10)
45. Vogwill T, MacLean RC. 2015 The genetic basis of the fitness costs of antimicrobial resistance: a metaanalysis approach. Evol. Appl. 8, 284-295. (doi: 10.1111/eva.12202)
46. Dahlberg C, Chao L. 2003 Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165, 1641-1649.
47. Stewart FM, Levin BR. 1977 The population biology of bacterial plasmids: a priori conditions for the existence of conjugationally transmitted factors. Genetics 87, 209-228.
48. 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. (doi: 10.1111/j.1574-6941.2006.00223.x)
49. Smith HW. 1975 Persistence of tetracycline resistance in pig E. coli. Nature 258, 628-630. (doi: 10.1038/258628a0)
50. Van Melderen L, Saavedra De Bast M. 2009 Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet. 5, e1000437. (doi: 10.1371/journal.pgen.1000437)
51. Lee HJ, Jin HM, Park MS, Park W, Madsen EL, Jeon CO. 2015 Recovery of plasmid pEMB1, whose toxinantitoxin system stabilizes an ampicillin resistanceconferring beta-lactamase gene in Escherichia coli, from natural environments. Appl. Environ. Microbiol. 81, 40-47. (doi: 10.1128/AEM.02691-14)
52. Johnsen PJ, Osterhus JI, Sletvold H, Sorum M, Kruse H, Nielsen K, Simonsen GS, Sundsfjord A. 2005 Persistence of animal and human glycopeptideresistant enterococci on two Norwegian poultry farms formerly exposed to avoparcin is associated with a widespread plasmid-mediated vanA element within a polyclonal Enterococcus faecium population. Appl. Environ. Microbiol. 71, 159-168. (doi: 10.1128/AEM.71.1.159-168.2005)
53. D’Costa VM, McGrann KM, Hughes DW, Wright GD. 2006 Sampling the antibiotic resistome. Science 311, 374-377. (doi: 10.1126/science.1120800)
54. Leaves NI et al. 2000 Epidemiological studies of large resistance plasmids in Haemophilus. J. Antimicrob. Chemother. 45, 599-604. (doi: 10.1093/jac/45.5.599)
55. Selmecki A, Forche A, Berman J. 2006 Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313, 367-370. (doi: 10.1126/science.1128242)
56. Pelleau S et al. 2015 Adaptive evolution of malaria parasites in French Guiana: reversal of chloroquine resistance by acquisition of a mutation in pfcrt. Proc. Natl Acad. Sci. USA 112, 11672-11677. (doi: 10.1073/pnas.1507142112)
57. Brunner PC, Stefanato FL, McDonald BA. 2008 Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Mol. Plant Pathol. 9, 305-316. (doi: 10.1111/j.1364-3703.2007.00464.x)
58. Cools HJ, Fraaije BA. 2013 Update on mechanisms of azole resistance in Mycosphaerella graminicola and implications for future control. Pest Manag. Sci. 69, 150-155. (doi: 10.1002/ps.3348)
59. Paulander W, Maisnier-Patin S, Andersson DI. 2007 Multiple mechanisms to ameliorate the fitness burden of mupirocin resistance in Salmonella typhimurium. Mol. Microbiol. 64, 1038-1048. (doi: 10.1111/j.1365-2958.2007.05713.x)
60. Hurdle JG, O’Neill AJ, Ingham E, Fishwick C, Chopra I. 2004 Analysis of mupirocin resistance and fitness in Staphylococcus aureus by molecular genetic and structural modeling techniques. Antimicrob. Agents Chemother. 48, 4366-4376. (doi: 10.1128/AAC.48.11.4366-4376.2004)
61. Vilhelmsson SE, Tomasz A, Kristinsson KG. 2000 Molecular evolution in a multidrug-resistant lineage of Streptococcus pneumoniae: emergence of strains belonging to the serotype 6B Icelandic clone that lost antibiotic resistance traits. J. Clin. Microbiol. 38, 1375-1381.
62. De Gelder L et al. 2004 Combining mathematical models and statistical methods to understand and predict the dynamics of antibiotic-sensitive mutants in a population of resistant bacteria during experimental evolution. Genetics 168, 1131-1144. (doi: 10.1534/genetics.104.033431)
63. Enne VI, Delsol AA, Roe JM, Bennett PM. 2006 Evidence of antibiotic resistance gene silencing in Escherichia coli. Antimicrob. Agents Chemother. 50, 3003-3010. (doi: 10.1128/AAC.00137-06)
64. Sivertsen A, Pedersen T, Larssen KW, Bergh K, Rønning TG, Radtke A, Hegstad K. 2016 A silenced vanA gene cluster on a transferable plasmid caused an outbreak of vancomycin-variable enterococci. Antimicrob. Agents Chemother. 60, 4119-4127. (doi: 10.1128/AAC.00286-16)
65. Escudero JA, Loot C, Nivina A, Mazel D. 2015 The integron: adaptation on demand. Microbiol. Spectr. 3, MDNA3-0019-2014. (doi: 10.1128/microbiolspec.MDNA3-0019-2014)
66. Gillings MR. 2014 Integrons: past, present, and future. Microbiol. Mol. Biol. Rev. 78, 257-277. (doi: 10.1128/MMBR.00056-13)
67. Lacotte Y, Ploy MC, Raherison S. 2017 Class 1 integrons are low-cost structures in Escherichia coli. ISME J. 11, 1535-1544. (doi: 10.1038/ismej.2017.38)
68. Collis CM, Hall RM. 1995 Expression of antibiotic resistance genes in the integrated cassettes of integrons. Antimicrob. Agents Chemother. 39, 155-162. (doi: 10.1128/AAC.39.1.155)
69. Barraud O, Ploy M-C. 2015 Diversity of class 1 integron gene cassette rearrangements selected under antibiotic pressure. J. Bacteriol. 197, 2171-2178. (doi: 10.1128/JB.02455-14)
70. Guerin E et al. 2009 The SOS response controls integron recombination. Science 324, 1034. (doi: 10.1126/science.1172914)
71. Druilhe P, Daubersies P, Patarapotikul J, Gentil C, Chene L, Chongsuphajaisiddhi T, Mellouk S, Langsley G. 1998 A primary malarial infection is composed of a very wide range of genetically diverse but related parasites. J. Clin. Invest. 101, 2008-2016. (doi: 10.1172/JCI119890)
72. Horn DL et al. 1998 Why have group A streptococci remained susceptible to penicillin? Report on a symposium. Clin. Infect. Dis. 26, 1341-1345. (doi: 10.1086/516375)
73. Skurnik D et al. 2016 Emergence of antimicrobialresistant Escherichia coli of animal origin spreading in humans. Mol. Biol. Evol. 33, 898-914. (doi: 10.1093/molbev/msv280)
74. Costelloe C, Metcalfe C, Lovering A, Mant D, Hay AD. 2010 Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. BMJ 340, c2096. (doi: 10.1136/bmj.c2096)
75. Marvig RL, Sommer LM, Molin S, Johansen HK. 2015 Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat. Genet. 47, 57-64. (doi: 10.1038/ng.3148)
76. Luciani F. 2009 The epidemiological fitness cost of drug resistance in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 106, 14711-14715. (doi: 10.1073/pnas.0902437106)
77. Schneider P, Bell AS, Sim DG, O’Donnell AJ, Blanford S, Paaijmans KP, Read AF, Reece SE. 2012 Virulence, drug sensitivity and transmission success in the rodent malaria, Plasmodium chabaudi. Proc. R. Soc. B 279, 4677-4685. (doi: 10.1098/rspb.2012.1792)
78. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. 2006 Co-selection of antibiotic and metal resistance. Trends Microbiol. 14, 176-182. (doi: 10.1016/j.tim.2006.02.006)
79. Nikaido H, Pagès JM. 2012 Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol. Rev. 36, 340-363. (doi: 10.1111/j.1574-6976.2011.00290.x)
80. Gaze WH, Abdouslam N, Hawkey PM, Wellington EM. 2005 Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob. Agents Chemother. 49, 1802-1807. (doi: 10.1128/AAC.49.5.1802-1807.2005)
81. Imamovic L, Sommer MO. 2013 Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Sci. Transl. Med. 5, 204ra132. (doi: 10.1126/scitranslmed.3006609)
82. Lázár V et al. 2013 Bacterial evolution of antibiotic hypersensitivity. Mol. Syst. Biol. 9, 700. (doi: 10.1038/msb.2013.57)
83. Larder BA, Kemp SD, Harrigan PR. 1995 Potential mechanism for sustained antiretroviral efficacy of AZT-3TC combination therapy. Science 269, 696-699. (doi: 10.1126/science.7542804)
84. Diallo K, Oliveira M, Moisi D, Brenner B, Wainberg MA, Gotte M. 2002 Pressure of zidovudine accelerates the reversion of lamivudine resistanceconferring M184 V mutation in the reverse transcriptase of human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 46, 2254-2256. (doi: 10.1128/AAC.46.7.2254-2256.2002)
85. Murry JP, Higgins J, Matthews TB, Huang VY, Van Rompay KKA, Pedersen NC, North TW. 2003 Reversion of the M184 V mutation in simian immunodeficiency virus reverse transcriptase is selected by tenofovir, even in the presence of lamivudine. J. Virol. 77, 1120-1130. (doi: 10.1128/JVI.77.2.1120-1130.2003)
86. World Health Organization. 2015 19th WHO Model List of Essential Medicines.
87. Russell PE. 1995 Fungicide resistance-occurrence and management. J. Agric. Sci. 124, 317-323. (doi: 10.1017/S0021859600073275)
88. Yarden O, Katan T. 1993 Mutations leading to substitutions at amino-acids 198 and 200 of betatubulin that correlate with benomyl-resistance phenotypes of field strains of Botrytis cinerea. Phytopathology 83, 1478-1483. (doi: 10.1094/Phyto-83-1478)
89. Hahn M. 2014 The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J. Chem. Biol. 7, 133-141. (doi: 10.1007/s12154-014-0113-1)
90. Leroux P, Fritz R Debieu D, Albertini C, Lanen C, Bach J, Gredt M, Chapeland F. 2002 Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag. Sci. 58, 876-888. (doi: 10.1002/ps.566)
91. Fungicide Resistance Action Committee CropLife International. 2016 www.frac.info.
92. Dagan R, Melamed R, Muallem M, Piglansky L, Greenberg D, Abramson O, Mendelman PM, Bohidar N, Yagupsky P. 1996 Reduction of nasopharyngeal carriage of pneumococci during the second year of life by a heptavalent conjugate pneumococcal vaccine. J. Infect. Dis. 174, 1271-1278. (doi: 10.1093/infdis/174.6.1271)
93. Lehtinen S, Blanquart F, Croucher NJ, Turner P, Lipsitch M, Fraser C. 2017 Evolution of antibiotic resistance is linked to any genetic mechanism affecting bacterial duration of carriage. Proc. Natl Acad. Sci. USA 114, 1075-1080. (doi: 10.1073/pnas.1617849114)
94. Rudkin JK et al. 2012 Methicillin resistance reduces the virulence of healthcare-associated methicillin-resistant Staphylococcus aureus by interfering with the agr quorum sensing system. J. Infect. Dis. 205, 798-806. (doi: 10.1093/infdis/jir845)
95. Lendenmann MH, Croll D, McDonald BA. 2015 QTL mapping of fungicide sensitivity reveals novel genes and pleiotropy with melanization in the pathogen Zymoseptoria tritici. Fungal Genet. Biol. 80, 53-67. (doi: 10.1016/j.fgb.2015.05.001)
96. MacLean RC, Vogwill T. 2014 Limits to compensatory adaptation and the persistence of antibiotic resistance in pathogenic bacteria. Evol. Med. Public Health 2015, 4-12. (doi: 10.1093/emph/eou032)
97. Munk P et al. 2017 A sampling and metagenomic sequencing-based methodology for monitoring antimicrobial resistance in swine herds. J. Antimicrob. Chemother. 72, 385-392. (doi: 10.1093/jac/dkw415)