Natural conjugative plasmids induce bacterial biofilm development (original) (raw)

Nature volume 412, pages 442–445 (2001)Cite this article

Abstract

Horizontal gene transfer is a principal source of evolution leading to change in the ecological character of bacterial species1. Bacterial conjugation2, which promotes the horizontal transfer of genetic material between donor and recipient cells by physical contact, is a phenomenon of fundamental evolutionary consequence3. Although conjugation has been studied primarily in liquid, most natural bacterial populations are found associated with environmental surfaces in complex multispecies communities called biofilms4. Biofilms are ideally suited to the exchange of genetic material of various origins, and it has been shown that bacterial conjugation occurs within biofilms5,6. Here I investigate the direct contribution of conjugative plasmids themselves to the capacity of the bacterial host to form a biofilm. Natural conjugative plasmids expressed factors that induced planktonic bacteria to form or enter biofilm communities, which favour the infectious transfer of the plasmid. This general connection between conjugation and biofilms suggests that medically relevant plasmid-bearing strains are more likely to form a biofilm. This may influence both the chances of biofilm-related infection risks and of conjugational spread of virulence factors.

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

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

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

Additional access options:

Similar content being viewed by others

References

  1. de la Cruz, I. & Davies, I. Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol. 8, 128–133 (2000).
    Article CAS Google Scholar
  2. Lederberg, J. & Tatum, E. L. Gene recombination in Escherichia coli. Nature 158, 558 (1946)..
    Article ADS CAS Google Scholar
  3. Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304 (2000).
    Article ADS CAS Google Scholar
  4. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. & Lappin-Scott, H. M. Microbial biofilms. Annu. Rev. Microbiol. 49, 711–745 (1995).
    Article CAS Google Scholar
  5. 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).
    Article ADS CAS Google Scholar
  6. Christensen, B. B. et al. Establishment of new genetic traits in a microbial biofilm community. Appl. Environ. Microbiol. 64, 2247–2255 (1998).
    Article ADS CAS Google Scholar
  7. O'Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295–304 (1998).
    Article CAS Google Scholar
  8. Pratt, L. A. & Kolter, R. Genetic analyses of bacterial biofilm formation. Curr. Opin. Microbiol. 2, 598–603 (1999).
    Article CAS Google Scholar
  9. Frost, L. S., Ippen-Ihler, K. & Skurray, R. A. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 58, 162–210 (1994).
    Article CAS Google Scholar
  10. Ried, G. & Henning, U. A unique amino acid substitution in the outer membrane protein OmpA causes conjugation deficiency in Escherichia coli K-12. FEBS Lett. 223, 387–390 (1987).
    Article CAS Google Scholar
  11. Lundquist, P. D. & Levin, B. R. Transitory derepression and the maintenance of conjugative plasmids. Genetics 113, 483–497 (1986).
    Article CAS Google Scholar
  12. Watnick, P. & Kolter, R. Biofilm, city of microbes. J. Bacteriol. 182, 2675–2679 (2000).
    Article CAS Google Scholar
  13. Bergstrom, C. T., Lipsitch, M. & Levin, B. R. Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155, 1505–1519 (2000).
    Article CAS Google Scholar
  14. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322 (1999).
    Article ADS CAS Google Scholar
  15. Chaveroche, M. K., Ghigo, J. M. & d’Enfert, C. A rapid method for efficient gene replacement in the filamentous fungus aspergillus nidulans. Nucleic Acids Res. 28, E97 (2000).
    Article CAS Google Scholar
  16. Couturier, M., Bex, F., Bergquist, P. L. & Maas, W. K. Identification and classification of bacterial plasmids. Microbiol. Rev. 52, 375–395 (1988).
    Article CAS Google Scholar
  17. Bukhari, A. I., Shapiro, J. A. & Adhya, S. L. (eds) DNA Insertion Elements, Plasmids and Episomes 601–656 (Cold Spring Harbor Laboratory, Cold Spring Harbor, 1977).
    Google Scholar
  18. Bradley, D. E., Taylor, D. E. & Cohen, D. R. Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J. Bacteriol. 143, 1466–1460 (1980).
    Article CAS Google Scholar
  19. Frost, L. S. in Bacterial conjugation (ed. Clewel, D. B.) 189–221 (Plenum, New York, 1993).
    Book Google Scholar

Download references

Acknowledgements

I am grateful to C. Wandersman for support and constant interest during the course of this work. I also thank D. Mazel, G. Gerbaud and P. Courvalin for providing the plasmids and strains used in this study; A. Idja and P. Roux for technical assistance; R. Longin for providing facilities of the Pasteur Institute Laboratory of Fermentations; and D. Mazel, E. Stewart, D. A. Rowe-Magnus and P. Delepelaire for helpful discussions and critical reading of the manuscript. This work was supported by grants from the Programme de Recherche Fondamentale en Microbiologie et Maladie Infectieuses, réseau Infections Nosocomiales (MENRT) and the Pasteur Institute.

Author information

Authors and Affiliations

  1. Unité des Membranes Bactériennes Institut Pasteur (CNRS URA 2172), 25 rue du Dr Roux, Paris, 75724, Cedex 15, France
    Jean-Marc Ghigo

Authors

  1. Jean-Marc Ghigo
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toJean-Marc Ghigo.

Supplementary information

Figure 4

(JPG 27.1 KB)

Supplemental data: A Kinetics of biofilm formation of strain TG1 carrying a GFP-expressing plasmid pGFPmn2. (Top): biofilm at different times after inoculation. Size bars: 10 µM (Bottom) Epifluorescence photomicrographs of the corresponding Pyrex slides. B Scanning laser confocal photomicrographs of TG1 (pGFPmn2). (Top) Schematic indicating the observation point. (Bottom) Z-axis.

Figure 5

(JPG 48.2 KB)

Supplemental data: Kinetics of surface adhesion in the F- and F+ E. coli strains. Compared cell density of strain MG1655 Ftet and MG1655 after 5; 10 and 24 hours of culture in microfermenters. Transmitted light microscopy of the Pyrex slide stained with crystal violet. Size bars: 10 µm

Figure 6

(JPG 28.5 KB)

Supplemental data: Natural conjugative plasmids promote biofilm formation. Representative examples of the biofilm promoting ability of natural conjugative plasmids. (Left) Plasmid-free E. coli F- strain BM21. Incompatibility groups of the presented plasmids are indicated.

Figure 7

(JPG 47.9 KB)

Derepression of conjugation ability of natural conjugative plasmids. Comparison of biofilm formation ability of strain E. coli BM21 carrying natural conjugative plasmids inoculated alone (left) or co-inoculated 24H after the initial inoculation of strain E. coli MG1655. Conjugative plasmids are described in Table 1. 16

Rights and permissions

About this article

Cite this article

Ghigo, JM. Natural conjugative plasmids induce bacterial biofilm development.Nature 412, 442–445 (2001). https://doi.org/10.1038/35086581

Download citation