The evolution of plasmid stability: Are infectious transmission and compensatory evolution competing evolutionary trajectories?

Plasmid

Volumn 91, Issue , 2017, Pages 90-95

  Hall, James P J ^a   Brockhurst, Michael A ^a   Dytham, Calvin ^b   Harrison, Ellie ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONJUGATION; MODEL; PLASMID; BACTERIAL CHROMOSOME; BACTERIUM; BACTERIUM CONJUGATION; CHEMISTRY; EVOLUTION; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC SELECTION; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; REPRODUCTIVE FITNESS; STATISTICAL MODEL;

BACTERIA; BIOLOGICAL EVOLUTION; CHROMOSOMES, BACTERIAL; CONJUGATION, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENETIC FITNESS; GENETIC LOCI; MODELS, STATISTICAL; MUTAGENESIS, INSERTIONAL; PLASMIDS; SELECTION, GENETIC;

EID: 85019042566     PISSN: 0147619X     EISSN: 10959890     Source Type: Journal    
DOI: 10.1016/j.plasmid.2017.04.003     Document Type: Article

References (44)

1. Allen, G.E., Dytham, C., An efficient method for stochastic simulation of biological populations in continuous time. Biosystems 98 (2009), 37–42.
2. Bahl, M.I., Hansen, L.H., Sørensen, S.J., Impact of conjugal transfer on the stability of IncP-1 plasmid pKJK5 in bacterial populations. FEMS Microbiol. Lett. 266 (2007), 250–256.
3. Bañuelos-Vazquez, L.A., Tejerizo, G.T., Brom, S., Regulation of conjugative transfer of plasmids and integrative conjugative elements. Plasmid, 2017, 10.1016/j.plasmid.2017.04.002.
4. Beaber, J.W., Hochhut, B., Waldor, M.K., SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427 (2003), 72–74.
5. Bergstrom, C.T., Lipsitch, M., Levin, B.R., Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155 (2000), 1505–1519.
6. Bidlack, J.E., Silverman, P.M., An active type IV secretion system encoded by the F plasmid sensitizes Escherichia coli to bile salts. J. Bacteriol. 186 (2004), 5202–5209.
7. Carattoli, A., Plasmids and the spread of resistance. Int. J. Med. Microbiol. 303 (2013), 298–304.
8. Dahlberg, C., Chao, L., Amelioration of the cost of conjugative plasmid carriage in Escherichia coli K12. Genetics 165 (2003), 1641–1649.
9. De Gelder, L., Ponciano, J.M., Joyce, P., Top, E.M., Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 153 (2007), 452–463.
10. De Gelder, L., Williams, J.J., Ponciano, J.M., Sota, M., Top, E.M., Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid. Genetics 178 (2008), 2179–2190.
11. Dionisio, F., Conceicao, I.C., Marques, A.C.R., Fernandes, L., Gordo, I., The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol. Lett., 1, 2005.
12. Dunny, G.M., Johnson, C.M., Regulatory circuits controlling enterococcal conjugation: lessons for functional genomics. Curr. Opin. Microbiol. 14 (2011), 174–180.
13. Ellis, R.J., Lilley, A.K., Lacey, S.J., Murrell, D., Godfray, H.C.J., Frequency-dependent advantages of plasmid carriage by Pseudomonas in homogeneous and spatially structured environments. ISME J. 1 (2007), 92–95.
14. Fernandez-Lopez, R., del Campo, I., Revilla, C., Cuevas, A., de la Cruz, F., Negative feedback and transcriptional overshooting in a regulatory network for horizontal gene transfer. PLoS Genet., 10, 2014, 15.
15. Fox, R.E., Zhong, X., Krone, S.M., Top, E.M., Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations. ISME J. 2 (2008), 1024–1039.
16. Frost, L.S., Leplae, R., Summers, A.O., Toussaint, A., Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3 (2005), 722–732.
17. Gullberg, E., Albrecht, L.M., Karlsson, C., Sandegren, L., Andersson, D.I., Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. MBio, 5, 2014.
18. Hall, J.P.J., Harrison, E., Lilley, A.K., Paterson, S., Spiers, A.J., Brockhurst, M.A., Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects. Environ. Microbiol. 17 (2015), 5008–5022.
19. Hall, J.P.J., Wood, A.J., Harrison, E., Brockhurst, M.A., Source-sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 8260–8265.
20. Harrison, E., Brockhurst, M.A., Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol. 20 (2012), 262–267.
21. Harrison, E., Guymer, D., Spiers, A.J., Paterson, S., Brockhurst, M.A., Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Curr. Biol., 2015.
22. Harrison, E., Wood, A.J., Dytham, C., Pitchford, J.W., Truman, J., Spiers, A.J. et al., Bacteriophages limit the existence conditions for conjugative plasmids. mBio, 2015.
23. Harrison, E., Dytham, C., Hall, J.P.J., Guymer, D., Spiers, A.J., Paterson, S. et al., Rapid compensatory evolution promotes the survival of conjugative plasmids. Mob. Genet. Elements, 6, 2016, e1179074.
24. Heuer, H., Fox, R.E., Top, E.M., Frequent conjugative transfer accelerates adaptation of a broad-host-range plasmid to an unfavorable Pseudomonas putida host. FEMS Microbiol. Ecol., 59, 2007.
25. Jalasvuori, M., Friman, V.P., Nieminen, A., Bamford, J.K.H., Buckling, A., Bacteriophage selection against a plasmid-encoded sex apparatus leads to the loss of antibiotic-resistance plasmids. Biol. Lett. 7 (2011), 902–905.
26. Koraimann, G., Wagner, M.A., Social behavior and decision making in bacterial conjugation. Front. Cell. Infect. Microbiol., 4, 2014.
27. Kottara, A., Hall, J.P.J., Harrison, E., Brockhurst, M.A., Multi-host environments select for host-generalist conjugative plasmids. BMC Evol. Biol., 16, 2016, 70.
28. Lilley, A.K., Bailey, M.J., The acquisition of indigenous plasmids by a genetically marked pseudomonad population colonizing the sugar beet phytosphere is related to local environmental conditions. Appl. Environ. Microbiol. 63 (1997), 1577–1583.
29. Loftie-Eaton, W., Yano, H., Burleigh, S., Simmons, R.S., Hughes, J.M., Rogers, L.M. et al., Evolutionary paths that expand plasmid host-range: implications for spread of antibiotic resistance. Mol. Biol. Evol. 33 (2016), 885–897.
30. McAnulla, C., Edwards, A., Sanchez-Contreras, M., Sawers, R.G., Downie, J.A., Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar viciae. Microbiology 153 (2007), 2074–2082.
31. McNally, A., Oren, Y., Kelly, D., Pascoe, B., Dunn, S., Sreecharan, T. et al., Combined analysis of variation in core, accessory and regulatory genome regions provides a super-resolution view into the evolution of bacterial populations. PLoS Genet., 12, 2016, e1006280.
32. Porse, A., Schønning, K., Munck, C., Sommer, M.O.A., Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts. Mol. Biol. Evol. 33 (2016), 2860–2873.
33. Rankin, D.J., Rocha, E.P.C., Brown, S.P., What traits are carried on mobile genetic elements, and why?. Heredity 106 (2011), 1–10.
34. San Millan, A., Toll-Riera, M., Qi, Q., MacLean, R.C., Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa. Nat. Commun., 6, 2015, 6845.
35. Sengupta, M., Austin, S., Prevalence and significance of plasmid maintenance functions in the virulence plasmids of pathogenic bacteria. Infect. Immun. 79 (2011), 2502–2509.
36. Sheppard, A.E., Stoesser, N., Wilson, D.J., Sebra, R., Kasarskis, A., Anson, L.W. et al., Nested Russian doll-like genetic mobility drives rapid dissemination of the Carbapenem resistance gene bla(KPC). Antimicrob. Agents Chemother. 60 (2016), 3767–3778.
37. Singh, P.K., Ramachandran, G., Ramos-Ruiz, R., Peiró-Pastor, R., Abia, D., Wu, L.J., Meijer, W.J.J., Mobility of the native Bacillus subtilis conjugative plasmid pLS20 is regulated by intercellular signaling. PLoS Genet., 9, 2013, e1003892.
38. Smillie, C., Garcillan-Barcia, M.P., Francia, M.V., Rocha, E.P.C., de la Cruz, F., Mobility of plasmids. Microbiol. Mol. Biol. Rev., 74, 2010 434–+.
39. Sota, M., Yano, H., Hughes, J.M., Daughdrill, G.W., Abdo, Z., Forney, L.J. et al., Shifts in the host range of a promiscuous plasmid through parallel evolution of its replication initiation protein. ISME J. 4 (2010), 1568–1580.
40. Turner, P.E., Cooper, V.S., Lenski, R.E., Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52 (1998), 315–329.
41. White, J.W., Rassweiler, A., Samhouri, J.F., Stier, A.C., White, C., Ecologists should not use statistical significance tests to interpret simulation model results. Oikos 123 (2014), 385–388.
42. Zahrl, D., Wagner, M., Bischof, K., Koraimann, G., Expression and assembly of a functional type IV secretion system elicit extracytoplasmic and cytoplasmic stress responses in Escherichia coli. J. Bacteriol. 188 (2006), 6611–6621.
43. Zaleski, P., Wawrzyniak, P., Sobolewska, A., Lukasiewicz, N., Baran, P., Romanczuk, K. et al., pIGWZ12—a cryptic plasmid with a modular structure. Plasmid 79 (2015), 37–47.
44. Zhong, X., Droesch, J., Fox, R., Top, E.M., Krone, S.M., On the meaning and estimation of plasmid transfer rates for surface-associated and well-mixed bacterial populations. J. Theor. Biol. 294 (2012), 144–152.