Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Positive selection inhibits gene mobilization and transfer in soil bacterial communities

Nature Ecology & Evolution volume 1, pages 1348–1353 (2017)Cite this article

Subjects

Abstract

Horizontal gene transfer (HGT) between bacterial lineages is a fundamental evolutionary process that accelerates adaptation. Sequence analyses show that conjugative plasmids are principal agents of HGT in natural communities. However, we lack understanding of how the ecology of bacterial communities and their environments affect the dynamics of plasmid-mediated gene mobilization and transfer. Here we show, in simple experimental soil bacterial communities containing a conjugative mercury resistance plasmid, the repeated, independent mobilization of transposon-borne genes from chromosome to plasmid, plasmid to chromosome and, in the absence of mercury selection, interspecific gene transfers from the chromosome of one species to the other via the plasmid. By reducing conjugation, positive selection for plasmid-encoded traits, like mercury resistance, can consequently inhibit HGT. Our results suggest that interspecific plasmid-mediated gene mobilization is most likely to occur in environments where plasmids are infectious, parasitic elements rather than those where plasmids are positively selected, beneficial elements.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Evolved clones show extensive within- and between-species gene mobilization.
Fig. 2: Plasmid dynamics are altered under positive selection.
Fig. 3: Spread of chromosomally acquired mercury resistance.

Similar content being viewed by others

References

  1. Halary, S., Leigh, J. W., Cheaib, B., Lopez, P. & Bapteste, E. Network analyses structure genetic diversity in independent genetic worlds. Proc. Natl Acad. Sci. USA 107, 127–132 (2010).

    Article  PubMed  Google Scholar 

  2. Norman, A., Hansen, L. H. & Sorensen, S. J. Conjugative plasmids: vessels of the communal gene pool. Phil. Trans. R. Soc. B 364, 2275–2289 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Frost, L. S., Leplae, R., Summers, A. O. & Toussaint, A. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3, 722–732 (2005).

    Article  PubMed  CAS  Google Scholar 

  4. Conlan, S. et al. Plasmid dynamics in KPC-positive Klebsiella pneumoniae during long-term patient colonization. mBio 7, e00742-16 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Sheppard, A. E. et al. Nested Russian doll-like genetic mobility drives rapid dissemination of the carbapenem resistance gene bla KPC. Antimicrob. Agents Chemother. 60, 3767–3778 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571–582 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Johnson, T. J. & Nolan, L. K. Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol. Mol. Biol. Rev. 73, 750–774 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Stoodley, P., Sauer, K., Davies, D. G. & Costerton, J. W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187–209 (2002).

    Article  PubMed  CAS  Google Scholar 

  9. Lopatkin, A. J. et al. Antibiotics as a selective driver for conjugation dynamics. Nat. Microbiol. 1, 16044 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Stevenson, C., Hall, J. P., Harrison, E., Wood, A. J. & Brockhurst, M. A. Gene mobility promotes the spread of resistance in bacterial populations. ISME J. 63, 1577 (2017).

    Google Scholar 

  11. Jacoby, G. A., Rogers, J. E., Jacob, A. E. & Hedges, R. W. Transposition of Pseudomonas toluene-degrading genes and expression in Escherichia coli. Nature 274, 179–180 (1978).

    Article  PubMed  CAS  Google Scholar 

  12. Hedges, R. W. & Jacob, A. E. In vivo translocation of genes of Pseudomonas aeruginosa onto a promiscuously transmissible plasmid. FEMS Microbiol. Lett. 2, 15–19 (1977).

    Article  CAS  Google Scholar 

  13. Hemme, C. L. et al. Lateral gene transfer in a heavy metal-contaminated-groundwater microbial community. mBio 7, e02234-15 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Xue, H. et al. Eco-evolutionary dynamics of episomes among ecologically cohesive bacterial populations. mBio 6, e00552-15 (2015).

    PubMed  PubMed Central  CAS  Google Scholar 

  15. Gomez, P. & Buckling, A. Bacteria-phage antagonistic coevolution in soil. Science 332, 106–109 (2011).

    Article  PubMed  CAS  Google Scholar 

  16. Hall, J. P. J. et al. Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects. Environ. Microbiol. 17, 5008–5022 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. 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. USA 113, 8260–8265 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Li, P., Feng, X. B., Qiu, G. L., Shang, L. H. & Li, Z. G. Mercury pollution in Asia: a review of the contaminated sites. J. Hazard. Mater. 168, 591–601 (2009).

    Article  PubMed  CAS  Google Scholar 

  19. Williams, D., Paterson, S., Brockhurst, M. A. & Winstanley, C. Refined analyses suggest that recombination is a minor source of genomic diversity in Pseudomonas aeruginosa chronic cystic fibrosis infections. Microb. Genom. 2, e000051 (2016).

  20. Silby, M. W. et al. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 10, R51 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Ravindran, A., Jalan, N., Yuan, J. S., Wang, N. & Gross, D. C. Comparative genomics of Pseudomonas syringae pv. syringae strains B301D and HS191 and insights into intrapathovar traits associated with plant pathogenesis. MicrobiologyOpen 4, 553–573 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Kivistik, P. A., Kivisaar, M. & Horak, R. Target site selection of Pseudomonas putida transposon Tn4652. J. Bacteriol. 189, 3918–3921 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Levin, B. R., Stewart, F. M. & Rice, V. A. The kinetics of conjugative plasmid transmission: fit of a simple mass action model. Plasmid 2, 247–260 (1979).

    Article  PubMed  CAS  Google Scholar 

  24. Hausner, M. & Wuertz, S. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 65, 3710–3713 (1999).

    PubMed  PubMed Central  CAS  Google Scholar 

  25. Bergstrom, C. T., Lipsitch, M. & Levin, B. R. Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155, 1505–1519 (2000).

    PubMed  PubMed Central  CAS  Google Scholar 

  26. Harrison, E. et al. Rapid compensatory evolution promotes the survival of conjugative plasmids. Mob. Genet. Elements 6, e1179074 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Baltrus, D. A. Exploring the costs of horizontal gene transfer. Trends Ecol. Evol. 28, 489–495 (2013).

    Article  PubMed  Google Scholar 

  28. McCarthy, A. J. et al. Extensive horizontal gene transfer during Staphylococcus aureus co-colonization in vivo. Genome Biol. Evol. 6, 2697–2708 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Shapiro, B. J. How clonal are bacteria over time? Curr. Opin. Microbiol. 31, 116–123 (2016).

    Article  PubMed  Google Scholar 

  30. Polz, M. F., Alm, E. J. & Hanage, W. P. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29, 170–175 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Sousa, A., Bourgard, C., Wahl, L. M. & Gordo, I. Rates of transposition in Escherichia coli. Biol. Lett. 9, 20130838 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Dennis, J. J. The evolution of IncP catabolic plasmids. Curr. Opin. Biotechnol. 16, 291–298 (2005).

    Article  CAS  Google Scholar 

  33. Revilla, C. et al. Different pathways to acquiring resistance genes illustrated by the recent evolution of IncW plasmids. Antimicrob. Agents Chemother. 52, 1472–1480 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Carraro, N., Rivard, N., Burrus, V. & Ceccarelli, D. Mobilizable genomic islands, different strategies for the dissemination of multidrug resistance and other adaptive traits. Mob. Genet. Elements 7, 1–6 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Condit, R., Stewart, F. M. & Levin, B. R. The population biology of bacterial transposons: a priori conditions for maintenance as parasitic DNA. Am. Nat. 132, 129–147 (1988).

    Article  Google Scholar 

  36. Twiss, E., Coros, A. M., Tavakoli, N. P. & Derbyshire, K. M. Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol. Microbiol. 57, 1593–1607 (2005).

    Article  PubMed  CAS  Google Scholar 

  37. Baharoglu, Z., Bikard, D. & Mazel, D. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet. 6, e1001165 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Christie-Oleza, J. A., Lanfranconi, M. P., Nogales, B., Lalucat, J. & Bosch, R. Conjugative interaction induces transposition of ISPst9 in Pseudomonas stutzeri AN10. J. Bacteriol. 191, 1239–1247 (2009).

    Article  PubMed  CAS  Google Scholar 

  39. He, S. et al. Mechanisms of evolution in high-consequence drug resistance plasmids. mBio 7, e01987-16 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  40. O’Neill, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations (Wellcome Trust & HM Government, London, 2016).

    Google Scholar 

  41. Cho, J. C. & Tiedje, J. M. Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl. Environ. Microbiol. 66, 5448–5456 (2000).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. 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, 2179–2190 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Harrison, E., Guymer, D., Spiers, A. J., Paterson, S. & Brockhurst, M. A. Parallel compensatory evolution stabilizes plasmids across the parasitism–mutualism continuum. Curr. Biol. 25, 2034–2039 (2015).

    Article  PubMed  CAS  Google Scholar 

  44. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Chen, K. et al. BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat. Methods 6, 677–681 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Lilley, A. K., Bailey, M. J., Day, M. J. & Fry, J. C. Diversity of mercury resistance plasmids obtained by exogenous isolation from the bacteria of sugar beet in three successive years. FEMS Microbiol. Ecol. 20, 211–227 (1996).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank P. Koldkjaer and others at the Liverpool Centre for Genomic Research for assistance with sample preparation and sequencing. This work was supported by ERC Grant Agreement no. 311490-COEVOCON to M.A.B. and a Philip Leverhulme Prize from Leverhulme Trust to M.A.B.

Author information

Authors and Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK

    James P. J. Hall, Ellie Harrison & Michael A. Brockhurst

  2. Department of Biology, University of York, York, YO10 5DD, UK

    James P. J. Hall

  3. Institute of Integrative Biology, University of Liverpool, Biosciences Building, Liverpool, L69 7ZB, UK

    David Williams & Steve Paterson

Authors
  1. James P. J. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Steve Paterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ellie Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael A. Brockhurst
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.P.J.H., E.H. and M.A.B. designed the study; J.P.J.H. collected data; J.P.J.H., D.W. and S.P. analysed the data. J.P.J.H. and M.A.B. drafted the manuscript. All authors discussed results and commented on the manuscript.

Corresponding authors

Correspondence to James P. J. Hall or Michael A. Brockhurst.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary Information

Supplementary Tables 1–4

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hall, J.P.J., Williams, D., Paterson, S. et al. Positive selection inhibits gene mobilization and transfer in soil bacterial communities. Nat Ecol Evol 1, 1348–1353 (2017). https://doi.org/10.1038/s41559-017-0250-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0250-3

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology