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Spatial organization of the flow of genetic information in bacteria


Eukaryotic cells spatially organize mRNA processes such as translation and mRNA decay. Much less is clear in bacterial cells where the spatial distribution of mature mRNA remains ambiguous. Using a sensitive method based on quantitative fluorescence in situ hybridization, we show here that in Caulobacter crescentus and Escherichia coli, chromosomally expressed mRNAs largely display limited dispersion from their site of transcription during their lifetime. We estimate apparent diffusion coefficients at least two orders of magnitude lower than expected for freely diffusing mRNA, and provide evidence in C. crescentus that this mRNA localization restricts ribosomal mobility. Furthermore, C. crescentus RNase E appears associated with the DNA independently of its mRNA substrates. Collectively, our findings show that bacteria can spatially organize translation and, potentially, mRNA decay by using the chromosome layout as a template. This chromosome-centric organization has important implications for cellular physiology and for our understanding of gene expression in bacteria.

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Figure 1: groESL mRNAs remain confined within subcellular regions.
Figure 2: groESL and creS mRNAs largely remain at the site of birth for their entire lifespan.
Figure 3: Endogenous LacZ-encoding mRNAs display diffraction-limited dispersion from sites of transcription in E. coli.
Figure 4: Dispersion of groESL–lacO 120 mRNA.
Figure 5: mRNA limits diffusion of translating ribosomes.
Figure 6: RNase E colocalizes with the DNA in C. crescentus.


  1. Passalacqua, K. D. et al. Structure and complexity of a bacterial transcriptome. J. Bacteriol. 191, 3203–3211 (2009)

    Article  CAS  Google Scholar 

  2. Epshtein, V. & Nudler, E. Cooperation between RNA polymerase molecules in transcription elongation. Science 300, 801–805 (2003)

    Article  ADS  CAS  Google Scholar 

  3. Vogel, U. & Jensen, K. F. The RNA chain elongation rate in Escherichia coli depends on the growth rate. J. Bacteriol. 176, 2807–2813 (1994)

    Article  CAS  Google Scholar 

  4. Bernstein, J. A., Khodursky, A. B., Lin, P. H., Lin-Chao, S. & Cohen, S. N. Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc. Natl Acad. Sci. USA 99, 9697–9702 (2002)

    Article  ADS  CAS  Google Scholar 

  5. Miller, O. L. Jr, Hamkalo, B. A. & Thomas, C. A. Jr. Visualization of bacterial genes in action. Science 169, 392–395 (1970)

    Article  ADS  Google Scholar 

  6. Guet, C. C. et al. Minimally invasive determination of mRNA concentration in single living bacteria. Nucleic Acids Res. 36, e73 (2008)

    Article  Google Scholar 

  7. Golding, I. & Cox, E. C. RNA dynamics in live Escherichia coli cells. Proc. Natl Acad. Sci. USA 101, 11310–11315 (2004)

    Article  ADS  CAS  Google Scholar 

  8. Maamar, H., Raj, A. & Dubnau, D. Noise in gene expression determines cell fate in Bacillus subtilis. Science 317, 526–529 (2007)

    Article  ADS  CAS  Google Scholar 

  9. Golding, I., Paulsson, J., Zawilski, S. M. & Cox, E. C. Real-time kinetics of gene activity in individual bacteria. Cell 123, 1025–1036 (2005)

    Article  CAS  Google Scholar 

  10. Valencia-Burton, M., McCullough, R. M., Cantor, C. R. & Broude, N. E. RNA visualization in live bacterial cells using fluorescent protein complementation. Nature Methods 4, 421–427 (2007)

    Article  CAS  Google Scholar 

  11. Pilhofer, M., Pavlekovic, M., Lee, N. M., Ludwig, W. & Schleifer, K. H. Fluorescence in situ hybridization for intracellular localization of nifH mRNA. Syst. Appl. Microbiol. 32, 186–192 (2009)

    Article  CAS  Google Scholar 

  12. Valencia-Burton, M. et al. Spatiotemporal patterns and transcription kinetics of induced RNA in single bacterial cells. Proc. Natl Acad. Sci. USA 106, 16399–16404 (2009)

    Article  ADS  CAS  Google Scholar 

  13. Avedissian, M. & Lopes Gomes, S. Expression of the groESL operon is cell-cycle controlled in Caulobacter crescentus. Mol. Microbiol. 19, 79–89 (1996)

    Article  CAS  Google Scholar 

  14. Lim, F. & Peabody, D. S. Mutations that increase the affinity of a translational repressor for RNA. Nucleic Acids Res. 22, 3748–3752 (1994)

    Article  CAS  Google Scholar 

  15. Lau, I. F. et al. Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol. Microbiol. 49, 731–743 (2003)

    Article  CAS  Google Scholar 

  16. Deana, A. & Belasco, J. G. Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev. 19, 2526–2533 (2005)

    Article  CAS  Google Scholar 

  17. Viollier, P. H. & Shapiro, L. Spatial complexity of mechanisms controlling a bacterial cell cycle. Curr. Opin. Microbiol. 7, 572–578 (2004)

    Article  CAS  Google Scholar 

  18. Wheeler, R. T. & Shapiro, L. Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol. Cell 4, 683–694 (1999)

    Article  CAS  Google Scholar 

  19. Mangan, E. K. et al. FlbT couples flagellum assembly to gene expression in Caulobacter crescentus. J. Bacteriol. 181, 6160–6170 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Yarchuk, O., Jacques, N., Guillerez, J. & Dreyfus, M. Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J. Mol. Biol. 226, 581–596 (1992)

    Article  CAS  Google Scholar 

  21. Derman, A. I., Lim-Fong, G. & Pogliano, J. Intracellular mobility of plasmid DNA is limited by the ParA family of partitioning systems. Mol. Microbiol. 67, 935–946 (2008)

    Article  CAS  Google Scholar 

  22. Elowitz, M. B., Surette, M. G., Wolf, P. E., Stock, J. B. & Leibler, S. Protein mobility in the cytoplasm of Escherichia coli. J. Bacteriol. 181, 197–203 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Viollier, P. H. et al. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc. Natl Acad. Sci. USA 101, 9257–9262 (2004)

    Article  ADS  CAS  Google Scholar 

  24. Briegel, A. et al. Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography. Mol. Microbiol. 62, 5–14 (2006)

    Article  CAS  Google Scholar 

  25. Forchhammer, J. & Lindahl, L. Growth rate of polypeptide chains as a function of the cell growth rate in a mutant of Escherichia coli 15. J. Mol. Biol. 55, 563–568 (1971)

    Article  CAS  Google Scholar 

  26. Lewis, P. J., Thaker, S. D. & Errington, J. Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J. 19, 710–718 (2000)

    Article  CAS  Google Scholar 

  27. Mascarenhas, J., Weber, M. H. & Graumann, P. L. Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription. EMBO Rep. 2, 685–689 (2001)

    Article  CAS  Google Scholar 

  28. Carpousis, A. J., Luisi, B. F. & McDowall, K. J. Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog Mol Biol Transl Sci 85, 91–135 (2009)

    Article  CAS  Google Scholar 

  29. Taghbalout, A. & Rothfield, L. RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton. Proc. Natl Acad. Sci. USA 104, 1667–1672 (2007)

    Article  ADS  CAS  Google Scholar 

  30. Khemici, V., Poljak, L., Luisi, B. F. & Carpousis, A. J. The RNase E of Escherichia coli is a membrane-binding protein. Mol. Microbiol. 70, 799–813 (2008)

    CAS  PubMed  Google Scholar 

  31. Ward, D. & Newton, A. Requirement of topoisomerase IV parC and parE genes for cell cycle progression and developmental regulation in Caulobacter crescentus. Mol. Microbiol. 26, 897–910 (1997)

    Article  CAS  Google Scholar 

  32. Neidhart, F. C. & Umbarger, H. E. in Escherichia coli and Salmonella: cellular and molecular biology 2nd edition, Vol. 1 (ed. Neidhardt, F. C.) Ch. 3, 13–16 (ASM Press, 1996)

    Google Scholar 

  33. Tamames, J. Evolution of gene order conservation in prokaryotes. Genome Biol. 2, research0020.1–research0020.11 (2001)

    Article  Google Scholar 

  34. Fang, G., Rocha, E. P. & Danchin, A. Persistence drives gene clustering in bacterial genomes. BMC Genomics 9, 4 (2008)

    Article  Google Scholar 

  35. Ely, B. Genetics of Caulobacter crescentus. Methods Enzymol. 204, 372–384 (1991)

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Jensen, R. B. & Shapiro, L. The Caulobacter crescentus smc gene is required for cell cycle progression and chromosome segregation. Proc. Natl Acad. Sci. USA 96, 10661–10666 (1999)

    Article  ADS  CAS  Google Scholar 

  38. Domian, I. J., Quon, K. C. & Shapiro, L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90, 415–424 (1997)

    Article  CAS  Google Scholar 

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We thank P. Angelastro, N. Ausmees, T. Cox, I. Golding, H. Lam, D. S. Peabody, D Leach, D. J. Sherratt and P. Viollier for strains and constructs, M. Cabeen for editorial help, and S. R. Kushner, J. Belasco, K. C. Huang, the Lambda lunch group at NIH, and the Jacobs-Wagner laboratory for valuable discussions. This work was funded in part by a Howard Hughes Medical Institute Predoctoral Fellowship (to A.F.J.), the National Institutes of Health (GM065835 to C.J.-W.) and the Howard Hughes Medical Institute.

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Authors and Affiliations



C.J.-W., P.M.L. and A.F.J. designed experiments. P.M.L. performed the FISH, ribosome and RNaseE experiments, and analysed FISH and FRAP data. A.F.J. carried out the MS2 experiments and analysed the data. P.M.L. and J.H. performed the real-time PCR measurements. O.S. developed the tools for image and data analysis. I.S. described and implemented the mathematical model for the analysis of mRNA diffusion. T.E. provided conceptual and data analysis advice. C.J.-W., P.M.L. and A.F.J. wrote the paper.

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Correspondence to Christine Jacobs-Wagner.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-8 with legends, Supplementary Information comprising Supplementary Text, Image and data analysis, Mathematical modelling, Supplementary Tables S1-S2, Construction of plasmids and strains, FISH probes sequences and References. (PDF 1199 kb)

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Montero Llopis, P., Jackson, A., Sliusarenko, O. et al. Spatial organization of the flow of genetic information in bacteria. Nature 466, 77–81 (2010).

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