1887

Abstract

The acquisition of plasmids is often accompanied by fitness costs such that compensatory evolution is required to allow plasmid survival, but it is unclear whether compensatory evolution can be extensive or rapid enough to maintain plasmids when they are very costly. The mercury-resistance plasmid pQBR55 drastically reduced the growth of its host, SBW25, immediately after acquisition, causing a small colony phenotype. However, within 48 h of growth on agar plates we observed restoration of the ancestral large colony morphology, suggesting that compensatory mutations had occurred. Relative fitness of these evolved strains, in lab media and in soil microcosms, varied between replicates, indicating different mutational mechanisms. Using genome sequencing we identified that restoration was associated with chromosomal mutations in either a hypothetical DNA-binding protein PFLU4242, RNA polymerase or the GacA/S two-component system. Targeted deletions in , or recapitulated the ameliorated phenotype upon plasmid acquisition, indicating three distinct mutational pathways to compensation. Our data shows that plasmid compensatory evolution is fast enough to allow survival of a plasmid despite it imposing very high fitness costs upon its host, and indeed may regularly occur during the process of isolating and selecting individual plasmid-containing clones.

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2019-10-15
2019-11-18
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References

  1. Norman A, Hansen LH, Sørensen SJ. Conjugative plasmids: vessels of the communal gene pool. Philos Trans R Soc Lond B Biol Sci 2009;364: 2275– 2289 [CrossRef]
    [Google Scholar]
  2. San Millan A, MacLean RC. Fitness costs of plasmids: a limit to plasmid transmission. Microbiol Spectr 2017;5: [CrossRef]
    [Google Scholar]
  3. Kottara A, Hall JPJ, Harrison E, Brockhurst MA. Variable plasmid fitness effects and mobile genetic element dynamics across Pseudomonas species. FEMS Microbiol Ecol 2018;94: [CrossRef]
    [Google Scholar]
  4. Hall JPJ, Wood AJ, Harrison E, Brockhurst MA. Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities. Proc Natl Acad Sci USA 2016;113: 8260– 8265 [CrossRef]
    [Google Scholar]
  5. Harrison E, Guymer D, Spiers AJ, Paterson S, Brockhurst MA. Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Curr Biol 2015;25: 2034– 2039 [CrossRef]
    [Google Scholar]
  6. Loftie-Eaton W, Bashford K, Quinn H, Dong K, Millstein J et al. Compensatory mutations improve general permissiveness to antibiotic resistance plasmids. Nat Ecol Evol 2017;1: 1354– 1363 [CrossRef]
    [Google Scholar]
  7. San Millan A, Toll-Riera M, Qi Q, MacLean RC. Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa. Nat Commun 2015;6: 6845 [CrossRef]
    [Google Scholar]
  8. Harrison E, Dytham C, Hall JPJ, Guymer D, Spiers AJ et al. Rapid compensatory evolution promotes the survival of conjugative plasmids. Mob Genet Elements 2016;6: e1179074 [CrossRef]
    [Google Scholar]
  9. Stalder T, Rogers LM, Renfrow C, Yano H, Smith Z et al. Emerging patterns of plasmid-host coevolution that stabilize antibiotic resistance. Sci Rep 2017;7: 4853 [CrossRef]
    [Google Scholar]
  10. Sota M, Yano H, Hughes JM, Daughdrill GW, Abdo Z et al. Shifts in the host range of a promiscuous plasmid through parallel evolution of its replication initiation protein. ISME J 2010;4: 1568– 1580 [CrossRef]
    [Google Scholar]
  11. De Gelder L, Williams JJ, Ponciano JM, Sota M, Top EM. Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid. Genetics 2008;178: 2179– 2190 [CrossRef]
    [Google Scholar]
  12. Turner PE, Williams ESCP, Okeke C, Cooper VS, Duffy S et al. Antibiotic resistance correlates with transmission in plasmid evolution. Evolution 2014;68: 3368– 3380 [CrossRef]
    [Google Scholar]
  13. Porse A, Schønning K, Munck C, Sommer MOA. Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts. Mol Biol Evol 2016;33: 2860– 2873 [CrossRef]
    [Google Scholar]
  14. Lilley AK, Bailey MJ. 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 1997;63: 1577– 1583
    [Google Scholar]
  15. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014;58: 3895– 3903 [CrossRef]
    [Google Scholar]
  16. Xiong J, Alexander DC, Ma JH, Déraspe M, Low DE et al. Complete sequence of pOZ176, a 500-kilobase IncP-2 plasmid encoding IMP-9-mediated carbapenem resistance, from outbreak isolate Pseudomonas aeruginosa 96. Antimicrob Agents Chemother 2013;57: 3775– 3782 [CrossRef]
    [Google Scholar]
  17. Botelho J, Grosso F, Quinteira S, Mabrouk A, Peixe L. The complete nucleotide sequence of an IncP-2 megaplasmid unveils a mosaic architecture comprising a putative novel blaVIM-2-harbouring transposon in Pseudomonas aeruginosa. J Antimicrob Chemother 2017;72: 2225– 2229 [CrossRef]
    [Google Scholar]
  18. Zhang XX, Rainey PB. Construction and validation of a neutrally-marked strain of Pseudomonas fluorescens SBW25. J Microbiol Methods 2007;71: 78– 81 [CrossRef]
    [Google Scholar]
  19. Turner SL, Lilley AK, Bailey MJ. Two dnaB genes are associated with the origin of replication of pQBR55, an exogenously isolated plasmid from the rhizosphere of sugar beet. FEMS Microbiol Ecol 2002;42: 209– 215 [CrossRef]
    [Google Scholar]
  20. Cheng X, de Bruijn I, van der Voort M, Loper JE, Raaijmakers JM. The Gac regulon of Pseudomonas fluorescens SBW25. Environ Microbiol Rep 2013;5: 608– 619 [CrossRef]
    [Google Scholar]
  21. Hall JPJ, Harrison E, Lilley AK, Paterson S, Spiers AJ et al. Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects. Environ Microbiol 2015;17: 5008– 5022 [CrossRef]
    [Google Scholar]
  22. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory; 1989
    [Google Scholar]
  23. Gómez P, Buckling A. Bacteria-Phage antagonistic coevolution in soil. Science 2011;332: 106– 109 [CrossRef]
    [Google Scholar]
  24. Lenski RE, Rose MR, Simpson SC, Tadler SC. Long-Term experimental evolution in Escherichia coli. I. adaptation and divergence during 2,000 generations. Am Nat 1991;138: 1315– 1341 [CrossRef]
    [Google Scholar]
  25. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25: 1754– 1760 [CrossRef]
    [Google Scholar]
  26. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010;20: 1297– 1303 [CrossRef]
    [Google Scholar]
  27. Deatherage DE, Barrick JE. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 2014;1151: 165– 188 [CrossRef]
    [Google Scholar]
  28. Hall JPJ, Williams D, Paterson S, Harrison E, Brockhurst MA. Positive selection inhibits gene mobilisation and transfer in soil bacterial communities. Nat Ecol Evol 2017;1: 1348– 1353 [CrossRef]
    [Google Scholar]
  29. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013;14: 178– 192 [CrossRef]
    [Google Scholar]
  30. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P et al. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 2006;4: 295– 305 [CrossRef]
    [Google Scholar]
  31. Malone JG. Role of small colony variants in persistence of Pseudomonas aeruginosa infections in cystic fibrosis lungs. Infect Drug Resist 2015;8: 237– 247 [CrossRef]
    [Google Scholar]
  32. Hughes JM, Lohman BK, Deckert GE, Nichols EP, Settles M et al. The role of clonal interference in the evolutionary dynamics of plasmid-host adaptation. mbio 2012;3: e00077– 12 [CrossRef]
    [Google Scholar]
  33. Lapouge K, Schubert M, Allain FHT, Haas D. Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 2008;67: 241– 253 [CrossRef]
    [Google Scholar]
  34. Jousset A, Scheu S, Bonkowski M. Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of Indigenous bacteria. Funct Ecol 2008;22: 714– 719 [CrossRef]
    [Google Scholar]
  35. Madsen JS, Hylling O, Jacquiod S, Pécastaings S, Hansen LH et al. An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer. ISME J 2018
    [Google Scholar]
  36. Qi Q, Preston GM, MacLean RC. Linking system-wide impacts of RNA polymerase mutations to the fitness cost of rifampin resistance in Pseudomonas aeruginosa. mBio 2014;5: e01562 [CrossRef]
    [Google Scholar]
  37. Rodríguez-Verdugo A, Tenaillon O, Gaut BS. First-Step mutations during adaptation restore the expression of hundreds of genes. Mol Biol Evol 2016;33: 25– 39 [CrossRef]
    [Google Scholar]
  38. Park C, Zhang J. High expression hampers horizontal gene transfer. Genome Biol Evol 2012;4: 523– 532 [CrossRef]
    [Google Scholar]
  39. Machnicka MA, Kaminska KH, Dunin-Horkawicz S, Bujnicki JM. Phylogenomics and sequence-structure-function relationships in the GmrSD family of type IV restriction enzymes. BMC Bioinformatics 2015;16: 336 [CrossRef]
    [Google Scholar]
  40. Hall JPJ, Harrison E, Brockhurst MA. Competitive species interactions constrain abiotic adaptation in a bacterial soil community. Evol Lett 2018;2: 580– 589 [CrossRef]
    [Google Scholar]
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