Chapter 4 : Fitness Costs of Plasmids: A Limit to Plasmid Transmission

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Fitness Costs of Plasmids: A Limit to Plasmid Transmission, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819743/9781555819736_Chap04-1.gif /docserver/preview/fulltext/10.1128/9781555819743/9781555819736_Chap04-2.gif


Horizontal gene transfer (HGT) is a key source of genetic diversity in bacteria ( ), and plasmids are one of the main vehicles driving this process ( ). Plasmids are widely distributed across prokaryotes, and help bacteria adapt to a myriad of different environments, conditions, and stresses ( ), playing a key role in bacterial ecology and evolution ( ). The most vivid testimony to the power of plasmids as catalysts for bacterial adaptation is their role in the spread of antibiotic resistance among clinical pathogens ( ), which has emerged as a major health problem over the past decades ( ).

Citation: San Millan A, MacLean R. 2019. Fitness Costs of Plasmids: A Limit to Plasmid Transmission, p 65-79. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0016-2017
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Fitness costs produced by plasmids. Potential fitness effects produced by plasmids during their life cycle in the bacterial host.

Citation: San Millan A, MacLean R. 2019. Fitness Costs of Plasmids: A Limit to Plasmid Transmission, p 65-79. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0016-2017
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Wiedenbeck J,, Cohan FM . 2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35 : 957 976.[CrossRef][PubMed]
2. Summers DK . 1996. The Biology of Plasmids. Blackwell Science Ltd, Oxford, United Kingdom.[CrossRef]
3. Smillie C,, Garcillán-Barcia MP,, Francia MV,, Rocha EP,, de la Cruz F . 2010. Mobility of plasmids. Microbiol Mol Biol Rev 74 : 434 452.[CrossRef][PubMed]
4. Smalla K,, Jechalke S,, Top EM . 2015. Plasmid detection, characterization, and ecology. Microbiol Spectr 3 : PLAS-0038-2014.[CrossRef][PubMed]
5. Ochman H,, Lawrence JG,, Groisman EA . 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405 : 299 304.[CrossRef][PubMed]
6. Gogarten JP,, Townsend JP . 2005. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3 : 679 687.[CrossRef][PubMed]
7. San Millan A,, Escudero JA,, Gifford DR,, Mazel D,, MacLean RC . 2016. Multicopy plasmids potentiate the evolution of antibiotic resistance in bacteria. Nat Ecol Evol 1 : 10.[CrossRef][PubMed]
8. Carattoli A . 2013. Plasmids and the spread of resistance. Int J Med Microbiol 303 : 298 304.[CrossRef][PubMed]
9. Review on Antimicrobial Resistance . 2016. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. Review on Antimicrobial Resistance, London, United Kingdom. https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf. Accessed date 12/01/2017.
10. Baltrus DA . 2013. Exploring the costs of horizontal gene transfer. Trends Ecol Evol 28 : 489 495.[CrossRef][PubMed]
11. Vogwill T,, MacLean RC . 2015. The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach. Evol Appl 8 : 284 295.[CrossRef][PubMed]
12. Hall JP,, Wood AJ,, Harrison E,, Brockhurst MA . 2016. Source-sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities. Proc Natl Acad Sci U S A 113 : 8260 8265.[CrossRef][PubMed]
13. 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.[PubMed]
14. Levin BR,, Stewart FM . 1980. The population biology of bacterial plasmids: a priori conditions for the existence of mobilizable nonconjugative factors. Genetics 94 : 425 443.[PubMed]
15. Simonsen L . 1991. The existence conditions for bacterial plasmids: theory and reality. Microb Ecol 22 : 187 205.[CrossRef][PubMed]
16. Bergstrom CT,, Lipsitch M,, Levin BR . 2000. Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155 : 1505 1519.[PubMed]
17. Lili LN,, Britton NF,, Feil EJ . 2007. The persistence of parasitic plasmids. Genetics 177 : 399 405.[CrossRef][PubMed]
18. Krone SM,, Lu R,, Fox R,, Suzuki H,, Top EM . 2007. Modelling the spatial dynamics of plasmid transfer and persistence. Microbiology 153 : 2803 2816.[CrossRef][PubMed]
19. Harrison E,, Brockhurst MA . 2012. Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol 20 : 262 267.[CrossRef][PubMed]
20. Bouma JE,, Lenski RE . 1988. Evolution of a bacteria/plasmid association. Nature 335 : 351 352.[CrossRef][PubMed]
21. 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.[CrossRef][PubMed]
22. 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.[CrossRef][PubMed]
23. 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.[CrossRef][PubMed]
24. Peña-Miller R,, Rodríguez-González R,, MacLean RC,, San Millan A . 2015. Evaluating the effect of horizontal transmission on the stability of plasmids under different selection regimes. Mob Genet Elements 5 : 1 5.[CrossRef]
25. 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.[CrossRef][PubMed]
26. Loftie-Eaton W,, Yano H,, Burleigh S,, Simmons RS,, Hughes JM,, Rogers LM,, Hunter SS,, Settles ML,, Forney LJ,, Ponciano JM,, Top EM . 2016. Evolutionary paths that expand plasmid host-range: implications for spread of antibiotic resistance. Mol Biol Evol 33 : 885 897.[CrossRef][PubMed]
27. Yano H,, Wegrzyn K,, Loftie-Eaton W,, Johnson J,, Deckert GE,, Rogers LM,, Konieczny I,, Top EM . 2016. Evolved plasmid-host interactions reduce plasmid interference cost. Mol Microbiol 101 : 743 756.[CrossRef][PubMed]
28. Porse A,, Schønning K,, Munck C,, Sommer MO . 2016. Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts. Mol Biol Evol 33 : 2860 2873.[CrossRef][PubMed]
29. Lorenz MG,, Wackernagel W . 1994. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58 : 563 602.[PubMed]
30. Matsumoto A,, Sekoguchi A,, Imai J,, Kondo K,, Shibata Y,, Maeda S . 2016. Natural Escherichia coli strains undergo cell-to-cell plasmid transformation. Biochem Biophys Res Commun 481 : 59 62.[CrossRef][PubMed]
31. Quiles-Puchalt N,, Martínez-Rubio R,, Ram G,, Lasa I,, Penadés JR . 2014. Unravelling bacteriophage Φ11 requirements for packaging and transfer of mobile genetic elements in Staphylococcus aureus. Mol Microbiol 91 : 423 437.[CrossRef][PubMed]
32. Vielmetter W,, Bonhoeffer F,, Schütte A . 1968. Genetic evidence for transfer of a single DNA strand during bacterial conjugation. J Mol Biol 37 : 81 86.[CrossRef][PubMed]
33. Baharoglu Z,, Bikard D,, Mazel D . 2010. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet 6 : e1001165.[CrossRef][PubMed]
34. Baharoglu Z,, Mazel D . 2014. SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 38 : 1126 1145.[CrossRef][PubMed]
35. Jones C,, Holland IB . 1985. Role of the SulB (FtsZ) protein in division inhibition during the SOS response in Escherichia coli: FtsZ stabilizes the inhibitor SulA in maxicells. Proc Natl Acad Sci U S A 82 : 6045 6049.[CrossRef][PubMed]
36. Petrova V,, Chitteni-Pattu S,, Drees JC,, Inman RB,, Cox MM . 2009. An SOS inhibitor that binds to free RecA protein: the PsiB protein. Mol Cell 36 : 121 130.[CrossRef][PubMed]
37. Jones AL,, Barth PT,, Wilkins BM . 1992. Zygotic induction of plasmid ssb and psiB genes following conjugative transfer of Incl1 plasmid Collb-P9. Mol Microbiol 6 : 605 613.[CrossRef][PubMed]
38. Althorpe NJ,, Chilley PM,, Thomas AT,, Brammar WJ,, Wilkins BM . 1999. Transient transcriptional activation of the Incl1 plasmid anti-restriction gene ( ardA) and SOS inhibition gene ( psiB) early in conjugating recipient bacteria. Mol Microbiol 31 : 133 142.[CrossRef][PubMed]
39. Baharoglu Z,, Krin E,, Mazel D . 2012. Connecting environment and genome plasticity in the characterization of transformation-induced SOS regulation and carbon catabolite control of the Vibrio cholerae integron integrase. J Bacteriol 194 : 1659 1667.[CrossRef][PubMed]
40. Campoy S,, Hervàs A,, Busquets N,, Erill I,, Teixidó L,, Barbé J . 2006. Induction of the SOS response by bacteriophage lytic development in Salmonella enterica. Virology 351 : 360 367.[CrossRef][PubMed]
41. 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 : e1004171.[CrossRef][PubMed]
42. Fernandez-Lopez R,, de la Cruz F . 2015. Rebooting the genome: the role of negative feedback in horizontal gene transfer. Mob Genet Elements 4 : 1 6.[CrossRef][PubMed]
43. Johnson CM,, Grossman AD . 2015. Integrative and conjugative elements (ICEs): what they do and how they work. Annu Rev Genet 49 : 577 601.[CrossRef][PubMed]
44. León-Sampedro R,, Novais C,, Peixe L,, Baquero F,, Coque TM . 2016. Diversity and evolution of the Tn 5801- tet(M)-like integrative and conjugative elements among Enterococcus, Streptococcus, and Staphylococcus. Antimicrob Agents Chemother 60 : 1736 1746.[CrossRef][PubMed]
45. Dimopoulou ID,, Russell JE,, Mohd-Zain Z,, Herbert R,, Crook DW . 2002. Site-specific recombination with the chromosomal tRNA Leu gene by the large conjugative Haemophilus resistance plasmid. Antimicrob Agents Chemother 46 : 1602 1603.[CrossRef][PubMed]
46. Cheng Q,, Paszkiet BJ,, Shoemaker NB,, Gardner JF,, Salyers AA . 2000. Integration and excision of a Bacteroides conjugative transposon, CTnDOT. J Bacteriol 182 : 4035 4043.[CrossRef][PubMed]
47. Roberts AP,, Mullany P . 2009. A modular master on the move: the Tn 916 family of mobile genetic elements. Trends Microbiol 17 : 251 258.[CrossRef][PubMed]
48. Rocha EP,, Danchin A . 2002. Base composition bias might result from competition for metabolic resources. Trends Genet 18 : 291 294.[CrossRef][PubMed]
49. Nishida H . 2012. Comparative analyses of base compositions, DNA sizes, and dinucleotide frequency profiles in archaeal and bacterial chromosomes and plasmids. Int J Evol Biol 2012 : 342482.[CrossRef][PubMed]
50. Wernegreen JJ . 2015. Endosymbiont evolution: predictions from theory and surprises from genomes. Ann N Y Acad Sci 1360 : 16 35.[CrossRef][PubMed]
51. Raghavan R,, Kelkar YD,, Ochman H . 2012. A selective force favoring increased G+C content in bacterial genes. Proc Natl Acad Sci U S A 109 : 14504 14507.[CrossRef][PubMed]
52. Hershberg R,, Petrov DA . 2010. Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6 : e1001115.[CrossRef][PubMed]
53. Hildebrand F,, Meyer A,, Eyre-Walker A . 2010. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 6 : e1001107.[CrossRef][PubMed]
54. Fang FC,, Rimsky S . 2008. New insights into transcriptional regulation by H-NS. Curr Opin Microbiol 11 : 113 120.[CrossRef][PubMed]
55. Ingmer H,, Miller C,, Cohen SN . 2001. The RepA protein of plasmid pSC101 controls Escherichia coli cell division through the SOS response. Mol Microbiol 42 : 519 526.[CrossRef][PubMed]
56. del Solar G,, Espinosa M . 2000. Plasmid copy number control: an ever-growing story. Mol Microbiol 37 : 492 500.[CrossRef][PubMed]
57. Lederberg J,, Tatum EL . 1953. Sex in bacteria; genetic studies, 1945–1952. Science 118 : 169 175.[CrossRef][PubMed]
58. Ilangovan A,, Connery S,, Waksman G . 2015. Structural biology of the Gram-negative bacterial conjugation systems. Trends Microbiol 23 : 301 310.[CrossRef][PubMed]
59. Costa TR,, Ilangovan A,, Ukleja M,, Redzej A,, Santini JM,, Smith TK,, Egelman EH,, Waksman G . 2016. Structure of the bacterial sex F pilus reveals an assembly of a stoichiometric protein-phospholipid complex. Cell 166 : 1436 1444.e10.[CrossRef][PubMed]
60. Turner PE,, Cooper VS,, Lenski RE . 1998. Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52 : 315 329.[CrossRef][PubMed]
61. Kozlowicz BK,, Shi K,, Gu ZY,, Ohlendorf DH,, Earhart CA,, Dunny GM . 2006. Molecular basis for control of conjugation by bacterial pheromone and inhibitor peptides. Mol Microbiol 62 : 958 969.[CrossRef][PubMed]
62. McAnulla C,, Edwards A,, Sanchez-Contreras M,, Sawers RG,, Downie JA . 2007. Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar viciae. Microbiology 153 : 2074 2082.[CrossRef][PubMed]
63. Koraimann G,, Wagner MA . 2014. Social behavior and decision making in bacterial conjugation. Front Cell Infect Microbiol 4 : 54.[CrossRef][PubMed]
64. Dahlberg C,, Chao L . 2003. Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165 : 1641 1649.[PubMed]
65. Zahrl D,, Wagner M,, Bischof K,, Koraimann G . 2006. Expression and assembly of a functional type IV secretion system elicit extracytoplasmic and cytoplasmic stress responses in Escherichia coli. J Bacteriol 188 : 6611 6621.[CrossRef][PubMed]
66. Caro LG,, Schnös M . 1966. The attachment of the male-specific bacteriophage F1 to sensitive strains of Escherichia coli. Proc Natl Acad Sci U S A 56 : 126 132.[CrossRef][PubMed]
67. Novotny C,, Knight WS,, Brinton CC Jr . 1968. Inhibition of bacterial conjugation by ribonucleic acid and deoxyribonucleic acid male-specific bacteriophages. J Bacteriol 95 : 314 326.[PubMed]
68. Jalasvuori M,, Friman VP,, Nieminen A,, Bamford JK,, Buckling A . 2011. Bacteriophage selection against a plasmid-encoded sex apparatus leads to the loss of antibiotic-resistance plasmids. Biol Lett 7 : 902 905.[CrossRef][PubMed]
69. Ojala V,, Laitalainen J,, Jalasvuori M . 2013. Fight evolution with evolution: plasmid-dependent phages with a wide host range prevent the spread of antibiotic resistance. Evol Appl 6 : 925 932.[CrossRef][PubMed]
70. Park C,, Zhang J . 2012. High expression hampers horizontal gene transfer. Genome Biol Evol 4 : 523 532.[CrossRef][PubMed]
71. Sorek R,, Zhu Y,, Creevey CJ,, Francino MP,, Bork P,, Rubin EM . 2007. Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318 : 1449 1452.[CrossRef][PubMed]
72. Lamberte LE,, Baniulyte G,, Singh SS,, Stringer AM,, Bonocora RP,, Stracy M,, Kapanidis AN,, Wade JT,, Grainger DC . 2017. Horizontally acquired AT-rich genes in Escherichia coli cause toxicity by sequestering RNA polymerase. Nat Microbiol 2 : 16249.[CrossRef][PubMed]
73. Plotkin JB,, Kudla G . 2011. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12 : 32 42.[CrossRef][PubMed]
74. Tuller T,, Girshovich Y,, Sella Y,, Kreimer A,, Freilich S,, Kupiec M,, Gophna U,, Ruppin E . 2011. Association between translation efficiency and horizontal gene transfer within microbial communities. Nucleic Acids Res 39 : 4743 4755.[CrossRef][PubMed]
75. Medrano-Soto A,, Moreno-Hagelsieb G,, Vinuesa P,, Christen JA,, Collado-Vides J . 2004. Successful lateral transfer requires codon usage compatibility between foreign genes and recipient genomes. Mol Biol Evol 21 : 1884 1894.[CrossRef][PubMed]
76. Komar AA,, Lesnik T,, Reiss C . 1999. Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation. FEBS Lett 462 : 387 391.[CrossRef]
77. Kudla G,, Murray AW,, Tollervey D,, Plotkin JB . 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324 : 255 258.[CrossRef][PubMed]
78. Cortazzo P,, Cerveñansky C,, Marín M,, Reiss C,, Ehrlich R,, Deana A . 2002. Silent mutations affect in vivo protein folding in Escherichia coli. Biochem Biophys Res Commun 293 : 537 541.[CrossRef]
79. Drummond DA,, Wilke CO . 2008. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134 : 341 352.[CrossRef][PubMed]
80. Ling J,, O’Donoghue P,, Söll D . 2015. Genetic code flexibility in microorganisms: novel mechanisms and impact on physiology. Nat Rev Microbiol 13 : 707 721.[CrossRef][PubMed]
81. Bonomo J,, Gill RT . 2005. Amino acid content of recombinant proteins influences the metabolic burden response. Biotechnol Bioeng 90 : 116 126.[CrossRef][PubMed]
82. Shachrai I,, Zaslaver A,, Alon U,, Dekel E . 2010. Cost of unneeded proteins in E. coli is reduced after several generations in exponential growth. Mol Cell 38 : 758 767.[CrossRef][PubMed]
83. Dittmar KA,, Sørensen MA,, Elf J,, Ehrenberg M,, Pan T . 2005. Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep 6 : 151 157.[CrossRef][PubMed]
84. Elf J,, Nilsson D,, Tenson T,, Ehrenberg M . 2003. Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 300 : 1718 1722.[CrossRef][PubMed]
85. Hernández-Arriaga AM,, Chan WT,, Espinosa M,, Díaz-Orejas R . 2014. Conditional activation of toxin-antitoxin systems: postsegregational killing and beyond. Microbiol Spectr 2 : 2.[CrossRef][PubMed]
86. San Millan JL,, Hernandez-Chico C,, Pereda P,, Moreno F . 1985. Cloning and mapping of the genetic determinants for microcin B17 production and immunity. J Bacteriol 163 : 275 281.[PubMed]
87. Jain R,, Rivera MC,, Lake JA . 1999. Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96 : 3801 3806.[CrossRef][PubMed]
88. Cohen O,, Gophna U,, Pupko T . 2011. The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol Biol Evol 28 : 1481 1489.[CrossRef][PubMed]
89. Pál C,, Papp B,, Lercher MJ . 2005. Horizontal gene transfer depends on gene content of the host. Bioinformatics 21( Suppl 2) : ii222 ii223.[CrossRef][PubMed]
90. 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. ISME J 4 : 1568 1580.[CrossRef][PubMed]
91. del Solar G,, Giraldo R,, Ruiz-Echevarría MJ,, Espinosa M,, Díaz-Orejas R . 1998. Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev 62 : 434 464.[PubMed]
92. Silva RF,, Mendonça SC,, Carvalho LM,, Reis AM,, Gordo I,, Trindade S,, Dionisio F . 2011. Pervasive sign epistasis between conjugative plasmids and drug-resistance chromosomal mutations. PLoS Genet 7 : e1002181.[CrossRef][PubMed]
93. Morton ER,, Platt TG,, Fuqua C,, Bever JD . 2014. Non-additive costs and interactions alter the competitive dynamics of co-occurring ecologically distinct plasmids. Proc Biol Sci 281 : 20132173.[CrossRef][PubMed]
94. Fornelos N,, Browning DF,, Butala M . 2016. The use and abuse of LexA by mobile genetic elements. Trends Microbiol 24 : 391 401.[CrossRef][PubMed]
95. Penadés JR,, Christie GE . 2015. The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu Rev Virol 2 : 181 201.[CrossRef][PubMed]
96. Miyakoshi M,, Shintani M,, Inoue K,, Terabayashi T,, Sai F,, Ohkuma M,, Nojiri H,, Nagata Y,, Tsuda M . 2012. ParI, an orphan ParA family protein from Pseudomonas putida KT2440-specific genomic island, interferes with the partition system of IncP-7 plasmids. Environ Microbiol 14 : 2946 2959.[CrossRef][PubMed]
97. Shintani M,, Suzuki-Minakuchi C,, Nojiri H . 2015. Nucleoid-associated proteins encoded on plasmids: occurrence and mode of function. Plasmid 80 : 32 44.[CrossRef][PubMed]
98. Baños RC,, Vivero A,, Aznar S,, García J,, Pons M,, Madrid C,, Juárez A . 2009. Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet 5 : e1000513.[CrossRef][PubMed]
99. Navarre WW,, Porwollik S,, Wang Y,, McClelland M,, Rosen H,, Libby SJ,, Fang FC . 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313 : 236 238.[CrossRef][PubMed]
100. Ali SS,, Soo J,, Rao C,, Leung AS,, Ngai DH,, Ensminger AW,, Navarre WW . 2014. Silencing by H-NS potentiated the evolution of Salmonella. PLoS Pathog 10 : e1004500.[CrossRef][PubMed]
101. Gordon BR,, Li Y,, Cote A,, Weirauch MT,, Ding P,, Hughes TR,, Navarre WW,, Xia B,, Liu J . 2011. Structural basis for recognition of AT-rich DNA by unrelated xenogeneic silencing proteins. Proc Natl Acad Sci U S A 108 : 10690 10695.[CrossRef][PubMed]
102. Yamada H,, Yoshida T,, Tanaka K,, Sasakawa C,, Mizuno T . 1991. Molecular analysis of the Escherichia coli hns gene encoding a DNA-binding protein, which preferentially recognizes curved DNA sequences. Mol Gen Genet 230 : 332 336.[CrossRef][PubMed]
103. Jáuregui R,, Abreu-Goodger C,, Moreno-Hagelsieb G,, Collado-Vides J,, Merino E . 2003. Conservation of DNA curvature signals in regulatory regions of prokaryotic genes. Nucleic Acids Res 31 : 6770 6777.[CrossRef][PubMed]
104. Takeda T,, Yun CS,, Shintani M,, Yamane H,, Nojiri H . 2011. Distribution of genes encoding nucleoid-associated protein homologs in plasmids. Int J Evol Biol 2011 : 685015.[CrossRef][PubMed]
105. 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.[CrossRef][PubMed]
106. Lang KS,, Johnson TJ . 2016. Characterization of Acr2, an H-NS-like protein encoded on A/C2-type plasmids. Plasmid 87-88 : 17 27.[CrossRef][PubMed]
107. Friedman SA,, Austin SJ . 1988. The P1 plasmid-partition system synthesizes two essential proteins from an autoregulated operon. Plasmid 19 : 103 112.[CrossRef]
108. Bingle LE,, Thomas CM . 2001. Regulatory circuits for plasmid survival. Curr Opin Microbiol 4 : 194 200.[CrossRef][PubMed]
109. Escudero JA,, Loot C,, Nivina A,, Mazel D . 2015. The integron: adaptation on demand. Microbiol Spectr 3 : MDNA3-0019-2014.[CrossRef][PubMed]
110. Collis CM,, Hall RM . 1995. Expression of antibiotic resistance genes in the integrated cassettes of integrons. Antimicrob Agents Chemother 39 : 155 162.[CrossRef]
111. Bennett PM . 2008. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153( Suppl 1) : S347 S357.[CrossRef][PubMed]
112. Lang KS,, Johnson TJ . 2015. Transcriptome modulations due to A/C2 plasmid acquisition. Plasmid 80 : 83 89.[CrossRef][PubMed]
113. Lang KS,, Danzeisen JL,, Xu W,, Johnson TJ . 2012. Transcriptome mapping of pAR060302, a bla CMY-2-positive broad-host-range IncA/C plasmid. Appl Environ Microbiol 78 : 3379 3386.[CrossRef][PubMed]
114. Lacotte Y,, Ploy MC,, Raherison S . 2017. Class 1 integrons are low-cost structures in Escherichia coli. ISME J 11 : 1535 1544.[CrossRef][PubMed]
115. Dougherty K,, Smith BA,, Moore AF,, Maitland S,, Fanger C,, Murillo R,, Baltrus DA . 2014. Multiple phenotypic changes associated with large-scale horizontal gene transfer. PLoS One 9 : e102170.[CrossRef][PubMed]
116. Brusselaers N,, Vogelaers D,, Blot S . 2011. The rising problem of antimicrobial resistance in the intensive care unit. Ann Intensive Care 1 : 47.[CrossRef][PubMed]
117. Boucher HW,, Talbot GH,, Bradley JS,, Edwards JE,, Gilbert D,, Rice LB,, Scheld M,, Spellberg B,, Bartlett J . 2009. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48 : 1 12.[CrossRef][PubMed]
118. European Centre for Disease Prevention and Control . 2015. Antimicrobial Resistance Surveillance in Europe 2014. European Centre for Disease Prevention and Control, Stockholm, Sweden. http://ecdc.europa.eu/en/publications/Publications/antimicrobial-resistance-europe-2014.pdf. Accessed date 17/12/2016.
119. Stoesser N,, Sheppard AE,, Pankhurst L,, De Maio N,, Moore CE,, Sebra R,, Turner P,, Anson LW,, Kasarskis A,, Batty EM,, Kos V,, Wilson DJ,, Phetsouvanh R,, Wyllie D,, Sokurenko E,, Manges AR,, Johnson TJ,, Price LB,, Peto TE,, Johnson JR,, Didelot X,, Walker AS,, Crook DW, Modernizing Medical Microbiology Informatics Group (MMMIG) . 2016. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. mBio 7 : e02162.[CrossRef][PubMed]
120. Dimou V,, Dhanji H,, Pike R,, Livermore DM,, Woodford N . 2012. Characterization of Enterobacteriaceae producing OXA-48-like carbapenemases in the UK. J Antimicrob Chemother 67 : 1660 1665.[CrossRef][PubMed]
121. Toll-Riera M,, San Millan A,, Wagner A,, MacLean RC . 2016. The genomic basis of evolutionary innovation in Pseudomonas aeruginosa. PLoS Genet 12 : e1006005.[CrossRef][PubMed]
122. Gifford DR,, Moss E,, MacLean RC . 2016. Environmental variation alters the fitness effects of rifampicin resistance mutations in Pseudomonas aeruginosa. Evolution 70 : 725 730.[CrossRef][PubMed]
123. Turner KH,, Wessel AK,, Palmer GC,, Murray JL,, Whiteley M . 2015. Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum. Proc Natl Acad Sci U S A 112 : 4110 4115.[CrossRef][PubMed]
124. Harrison F,, Diggle SP . 2016. An ex vivo lung model to study bronchioles infected with Pseudomonas aeruginosa biofilms. Microbiology 162 : 1755 1760.[CrossRef][PubMed]
125. Paulander W,, Pennhag A,, Andersson DI,, Maisnier-Patin S . 2007. Caenorhabditis elegans as a model to determine fitness of antibiotic-resistant Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother 51 : 766 769.[CrossRef][PubMed]
126. Ramarao N,, Nielsen-Leroux C,, Lereclus D . 2012. The insect Galleria mellonella as a powerful infection model to investigate bacterial pathogenesis. J Vis Exp (70) : e4392.[CrossRef][PubMed]
127. Ubeda C,, Bucci V,, Caballero S,, Djukovic A,, Toussaint NC,, Equinda M,, Lipuma L,, Ling L,, Gobourne A,, No D,, Taur Y,, Jenq RR,, van den Brink MR,, Xavier JB,, Pamer EG . 2013. Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization. Infect Immun 81 : 965 973.[CrossRef][PubMed]
128. Græsbøll K,, Nielsen SS,, Toft N,, Christiansen LE . 2014. How fitness reduced, antimicrobial resistant bacteria survive and spread: a multiple pig-multiple bacterial strain model. PLoS One 9 : e100458.[CrossRef][PubMed]
129. Harrison E,, Truman J,, Wright R,, Spiers AJ,, Paterson S,, Brockhurst MA . 2015. Plasmid carriage can limit bacteria-phage coevolution. Biol Lett 11 : 11.[CrossRef][PubMed]
130. Medaney F,, Ellis RJ,, Raymond B . 2016. Ecological and genetic determinants of plasmid distribution in Escherichia coli. Environ Microbiol 18 : 4230 4239.[CrossRef][PubMed]
131. Shintani M,, Takahashi Y,, Tokumaru H,, Kadota K,, Hara H,, Miyakoshi M,, Naito K,, Yamane H,, Nishida H,, Nojiri H . 2010. Response of the Pseudomonas host chromosomal transcriptome to carriage of the IncP-7 plasmid pCAR1. Environ Microbiol 12 : 1413 1426.[CrossRef][PubMed]
132. Getino M,, de la Cruz F . 2017. Natural and artificial strategies to control the conjugative transmission of plasmids. Microbiol Spectr In press.
133. Lacotte Y,, Ploy MC,, Raherison S . 2017. Class 1 integrons are low-cost structures in Escherichia coli. ISME J 11 : 1535 1544.[CrossRef][PubMed]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error