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General properties of transcriptional time series in Escherichia coli

Nature Genetics volume 43, pages 554–560 (2011)Cite this article

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Abstract

Gene activity is described by the time series of discrete, stochastic mRNA production events. This transcriptional time series shows intermittent, bursty behavior. One consequence of this temporal intricacy is that gene expression can be tuned by varying different features of the time series. Here we quantify copy-number statistics of mRNA from 20 Escherichia coli promoters using single-molecule fluorescence in situ hybridization in order to characterize the general properties of these transcriptional time series. We find that the degree of burstiness is correlated with gene expression level but is largely independent of other parameters of gene regulation. The observed behavior can be explained by the underlying variation in the duration of bursting events. Using Shannon's mutual information function, we estimate the mutual information transmitted between an outside stimulus, such as the extracellular concentration of inducer molecules, and intracellular levels of mRNA. This suggests that the outside stimulus transmits information reflected in the properties of transcriptional time series.

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Figure 1: Different features of the transcriptional time series can be modulated to vary gene expression level.
Figure 2: Single-molecule FISH (smFISH) used to characterize mRNA copy-number statistics.
Figure 3: Gene expression level in E. coli is varied by changing the gene off rate.
Figure 4: The transcriptional time series optimizes information representation by the cell.

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Acknowledgements

We are grateful to S. Adhya, W. Boos, M. Cashel, V. Chakravartty, L. Chubiz, D. Court, J. Cronan, M. Dreyfus, M. Elowitz, Y. Feng, H. Garcia, T. Hwa, J. Imlay, S. Jang, T. Kuhlman, J. Little, A. van Oudenaarden, A. Raj, C. Rao, R. Milo, V. Shahrezaei, A. Sokac and P. Swain for advice and for providing reagents. We thank members of the Golding laboratory for providing help with experiments. We thank H. Garcia, J. Kondev, R. Phillips, A. Raj, Á. Sánchez, S. Sawai and G. Tkacˇik for commenting on earlier versions of the manuscript. Work in the Golding laboratory was supported by grants from US National Institutes of Health (R01GM082837) and the National Science Foundation (082265, PFC: Center for the Physics of Living Cells). Work in the Segev and Golding laboratories was supported by a joint grant from the Human Frontier Science Program (RGY 70/2008).

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Authors and Affiliations

  1. Verna and Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, Texas, USA

    Lok-hang So, Leonardo A Sepúlveda & Ido Golding

  2. Department of Physics, University of Illinois, Urbana, Illinois, USA

    Lok-hang So, Chenghang Zong & Ido Golding

  3. Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel

    Anandamohan Ghosh & Ronen Segev

  4. Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel

    Anandamohan Ghosh & Ronen Segev

  5. Center for Biophysics and Computational Biology, University of Illinois, Urbana, Illinois, USA

    Leonardo A Sepúlveda & Ido Golding

  6. Center for the Physics of Living Cells, University of Illinois, Illinois, Urbana, USA

    Ido Golding

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  1. Lok-hang So
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  2. Anandamohan Ghosh
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Contributions

I.G., L.-h.S. and R.S. designed the project. L.-h.S. performed the majority of experiments and the theoretical analysis of gene activity. L.A.S. and C.Z. performed additional experiments and developed analysis tools for gene activity. R.S. and A.G. performed the information theory analysis. I.G., L.-h.S., L.A.S., R.S. and A.G. wrote the paper.

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Correspondence to Ido Golding.

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So, Lh., Ghosh, A., Zong, C. et al. General properties of transcriptional time series in Escherichia coli. Nat Genet 43, 554–560 (2011). https://doi.org/10.1038/ng.821

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