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.

  • Letter
  • Published:

Caulobacter crescentus intrinsic dimorphism provides a prompt bimodal response to copper stress

Nature Microbiology volume 1, Article number: 16098 (2016) Cite this article

Subjects

Abstract

Stress response to fluctuating environments often implies a time-consuming reprogramming of gene expression. In bacteria, the so-called bet hedging strategy, which promotes phenotypic stochasticity within a cell population, is the only fast stress response described so far1. Here, we show that Caulobacter crescentus asymmetrical cell division allows an immediate bimodal response to a toxic metals-rich environment by allocating specific defence strategies to morphologically and functionally distinct siblings. In this context, a motile swarmer cell favours negative chemotaxis to flee from a copper source, whereas a sessile stalked sibling engages a ready-to-use PcoAB copper homeostasis system, providing evidence of a prompt stress response through intrinsic bacterial dimorphism.

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

Figure 1: Cu detoxification response in Cu-treated ST cells.
Figure 2: Respective roles of PcoA and PcoB during the Cu detoxification response.
Figure 3: Cu-treated SW cells escape.
Figure 4: Model of the C. crescentus bimodal response.

Similar content being viewed by others

References

  1. Veening, J. W., Smits, W. K. & Kuipers, O. P. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62, 193–210 (2008).

    Article  Google Scholar 

  2. Cannon, W. B. Bodily Changes in Pain Hunger Fear and Rage (D. Appleton & Co., 1920).

    Google Scholar 

  3. Osman, D. & Cavet, J. S. Copper homeostasis in bacteria. Adv. Appl. Microbiol. 65, 217–247 (2008).

    Article  Google Scholar 

  4. Bagwell, C. E., Milliken, C. E., Ghoshroy, S. & Blom, D. A. Intracellular copper accumulation enhances the growth of Kineococcus radiotolerans during chronic irradiation. Appl. Environ. Microbiol. 74, 1376–1384 (2008).

    Article  Google Scholar 

  5. Palumaa, P. Copper chaperones. The concept of conformational control in the metabolism of copper. FEBS Lett. 587, 1902–1910 (2013).

    Article  Google Scholar 

  6. Ma, Z., Jacobsen, F. E. & Giedroc, D. P. Metal transporters and metal sensors: how coordination chemistry controls bacterial metal homeostasis. Chem. Rev. 109, 4644–4681 (2009).

    Article  Google Scholar 

  7. Rensing, C. & Grass, G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 27, 197–213 (2003).

    Article  Google Scholar 

  8. Outten, F. W., Outten, C. E., Hale, J. & O'Halloran, T. V. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR. J. Biol. Chem. 275, 31024–31029 (2000).

    Article  Google Scholar 

  9. Outten, F. W., Huffman, D. L., Hale, J. A. & O'Halloran, T. V. The independent Cue and Cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 276, 30670–30677 (2001).

    Article  Google Scholar 

  10. Stoyanov, J. V., Hobman, J. L. & Brown, N. L. CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol. Microbiol. 39, 502–511 (2001).

    Article  Google Scholar 

  11. Fang, G. et al. Transcriptomic and phylogenetic analysis of a bacterial cell cycle reveals strong associations between gene co-expression and evolution. BMC Genomics 14, 450 (2013).

    Article  Google Scholar 

  12. Skerker, J. M. & Laub, M. T. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nature Rev. Microbiol. 2, 325–337 (2004).

    Article  Google Scholar 

  13. Lee, S. M. et al. The Pco proteins are involved in periplasmic copper handling in Escherichia coli. Biochem. Biophys. Res. Commun. 295, 616–620 (2002).

    Article  Google Scholar 

  14. Jacobs, C., Hung, D. & Shapiro, L. Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc. Natl Acad. Sci. USA 98, 4095–4100 (2001).

    Article  Google Scholar 

  15. Jacobs, C., Ausmees, N., Cordwell, S. J., Shapiro, L. & Laub, M. T. Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol. Microbiol. 47, 1279–1290 (2003).

    Article  Google Scholar 

  16. Reichelt, M., von Specht, B. U. & Hahn, H. P. The Caulobacter crescentus outer membrane protein Omp58 (RsaF) is not required for paracrystalline S-layer secretion. FEMS Microbiol. Lett. 201, 277–283 (2001).

    Google Scholar 

  17. Huffman, D. L. et al. Spectroscopy of Cu(ii)-PcoC and the multicopper oxidase function of PcoA, two essential components of Escherichia coli Pco copper resistance operon. Biochemistry (Moscow) 41, 10046–10055 (2002).

    Article  Google Scholar 

  18. Fernandez-Fernandez, C., Grosse, K., Sourjik, V. & Collier, J. The β-sliding clamp directs the localization of HdaA to the replisome in Caulobacter crescentus. Microbiol. Read. Engl. 159, 2237–2248 (2013).

    Article  Google Scholar 

  19. Oakley, A. J. et al. Flexibility revealed by the 1.85 A crystal structure of the beta sliding-clamp subunit of Escherichia coli DNA polymerase III. Acta Crystallogr. D 59, 1192–1199 (2003).

    Article  Google Scholar 

  20. Hiniker, A., Collet, J.-F. & Bardwell, J. C. A. Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC. J. Biol. Chem. 280, 33785–33791 (2005).

    Article  Google Scholar 

  21. Macomber, L. & Imlay, J. A. The iron–sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl Acad. Sci. USA 106, 8344–8349 (2009).

    Article  Google Scholar 

  22. Py, B., Moreau, P. L. & Barras, F. Fe–S clusters, fragile sentinels of the cell. Curr. Opin. Microbiol. 14, 218–223 (2011).

    Article  Google Scholar 

  23. Hallez, R., Bellefontaine, A.-F., Letesson, J.-J. & De Bolle, X. Morphological and functional asymmetry in α-proteobacteria. Trends Microbiol. 12, 361–365 (2004).

    Article  Google Scholar 

  24. Deghelt, M. et al. G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus. Nature Commun. 5, 4366 (2014).

    Article  Google Scholar 

  25. Poindexter, J. S. Selection for nonbuoyant morphological mutants of Caulobacter crescentus. J. Bacteriol. 135, 1141–1145 (1978).

    Google Scholar 

  26. Ely, B. in Methods in Enzymology Vol. 204 (ed. Miller, J. H. ) 372–384 (Academic, 1991).

    Google Scholar 

  27. Evinger, M. & Agabian, N. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J. Bacteriol. 132, 294–301 (1977).

    Google Scholar 

  28. Winzeler, E. & Shapiro, L. Use of flow cytometry to identify a Caulobacter 4.5 S RNA temperature-sensitive mutant defective in the cell cycle. J. Mol. Biol. 251, 346–365 (1995).

    Article  Google Scholar 

  29. Levi, A. & Jenal, U. Holdfast formation in motile swarmer cells optimizes surface attachment during Caulobacter crescentus development. J. Bacteriol. 188, 5315–5318 (2006).

    Article  Google Scholar 

  30. Le Blastier, S. et al. Phosphate starvation triggers production and secretion of an extracellular lipoprotein in Caulobacter crescentus. PLoS ONE 5, e14198 (2010).

    Article  Google Scholar 

  31. Achard, M. E. S. et al. The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect. Immun. 78, 2312–2319 (2010).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank C. Jacobs-Wagner, J. Collier, L. Shapiro, P. Viollier and J. Smit for providing strains and antibodies. The authors acknowledge the microscopy platform of the De Duve Institute (UCL) for allowing access to the Zen Observer Z.1 inverted microscope, and thank C. Staudt (URPhym, UNamur) for technical support regarding the oxygraph and R. Stephan from the GIGA Flow Cytometry Facility (ULg) for technical support with FACS cell counting. Finally, the authors thank C. Jacobs-Wagner, J.-F. Collet, G. Cornelis and X. De Bolle for critical reading of the manuscript and the URBM members for discussions. This work was supported by the University of Namur. E.L. and S.G. were supported by the Belgian Fund for Industrial and Agricultural Research Associate (FRIA).

Author information

Authors and Affiliations

  1. Unité de Recherche en Biologie des Micro-organismes, University of Namur, 61 Rue de Bruxelles, 5000 Namur, Belgium

    Emeline Lawarée, Sébastien Gillet, Gwennaëlle Louis, Françoise Tilquin, Sophie Le Blastier & Jean-Yves Matroule

  2. Unité de Recherche en Biologie Végétale, University of Namur, 61 Rue de Bruxelles, 5000 Namur, Belgium

    Pierre Cambier

Authors
  1. Emeline Lawarée
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sébastien Gillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gwennaëlle Louis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Françoise Tilquin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sophie Le Blastier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pierre Cambier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jean-Yves Matroule
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.L., S.G., G.L., F.T., S.L.B. and P.C. performed the experiments. E.L., S.G. and G.L. analysed the data. E.L. and J.-Y.M. initiated and designed the research. E.L., S.G. and J.-Y.M. wrote the manuscript.

Corresponding author

Correspondence to Jean-Yves Matroule.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1-15, Supplementary Text, Supplementary Tables 1 and 2, Supplementary References (PDF 27626 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lawarée, E., Gillet, S., Louis, G. et al. Caulobacter crescentus intrinsic dimorphism provides a prompt bimodal response to copper stress. Nat Microbiol 1, 16098 (2016). https://doi.org/10.1038/nmicrobiol.2016.98

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nmicrobiol.2016.98

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