1887

Abstract

The ability to detect regulatory elements within genome sequences is important in understanding how gene expression is controlled in biological systems. In this work, microarray data analysis is combined with genome sequence analysis to predict DNA sequences in the photosynthetic bacterium that bind the regulators PrrA, PpsR and FnrL. These predictions were made by using hierarchical clustering to detect genes that share similar expression patterns. The DNA sequences upstream of these genes were then searched for possible transcription factor recognition motifs that may be involved in their co-regulation. The approach used promises to be widely applicable for the prediction of -acting DNA binding elements. Using this method the authors were independently able to detect and extend the previously described consensus sequences that have been suggested to bind FnrL and PpsR. In addition, sequences that may be recognized by the global regulator PrrA were predicted. The results support the earlier suggestions that the DNA binding sequence of PrrA may have a variable-sized gap between its conserved block elements. Using the predicted DNA binding sequences, a whole-genome-scale analysis was performed to determine the relative importance of the interplay between the three regulators PpsR, FnrL and PrrA. Results of this analysis showed that, compared to the regulation by PpsR and FnrL, a much larger number of genes are candidates to be regulated by PrrA. The study demonstrates by example that integration of multiple data types can be a powerful approach for inferring transcriptional regulatory patterns in microbial systems, and it allowed the detection of photosynthesis-related regulatory patterns in .

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2005-10-01
2019-10-21
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References

  1. Bailey, T. L. & Elkan, C. ( 1994; ). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings of the International Conference on Intelligent Systems for Molecular Biology, ISMB 2, 28–36.
    [Google Scholar]
  2. Bailey, T. L. & Gribskov, M. ( 1998; ). Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14, 48–54.[CrossRef]
    [Google Scholar]
  3. Braatsch, S., Gomelsky, M., Kuphal, S. & Klug, G. ( 2002; ). A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol Microbiol 45, 827–836.[CrossRef]
    [Google Scholar]
  4. Choudhary, M. & Kaplan, S. ( 2000; ). DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res 28, 862–867.[CrossRef]
    [Google Scholar]
  5. Comolli, J. C., Carl, A. J., Hall, C. & Donohue, T. ( 2002; ). Transcriptional activation of the Rhodobacter sphaeroides cytochrome c 2 gene P2 promoter by the response regulator PrrA. J Bacteriol 184, 390–399.[CrossRef]
    [Google Scholar]
  6. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. ( 2004; ). weblogo: a sequence logo generator. Genome Research 14, 1188–1190.[CrossRef]
    [Google Scholar]
  7. Du, S. & Bauer, C. E. ( 1999; ). DNA binding characteristics of RegA. A constitutively active anaerobic activator of photosynthesis gene expression in Rhodobacter capsulatus. J Biol Chem 274, 16343–16348.[CrossRef]
    [Google Scholar]
  8. Dubbs, J. M. & Tabita, F. R. ( 2003; ). Interactions of the cbb II promoter-operator region with CbbR and RegA (PrrA) regulators indicate distinct mechanisms to control expression of the two cbb operons of Rhodobacter sphaeroides. J Biol Chem 278, 16443–16450.[CrossRef]
    [Google Scholar]
  9. Dubbs, J. M., Bird, T. H., Bauer, C. E. & Tabita, F. R. ( 2000; ). Interaction of CbbR and RegA* transcription regulators with the Rhodobacter sphaeroides cbb I promoter-operator region. J Biol Chem 275, 19224–19230.[CrossRef]
    [Google Scholar]
  10. Eisen, M. B., Spellman, P. T., Brown, P. O. & Botstein, D. ( 1998; ). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95, 14863–14868.[CrossRef]
    [Google Scholar]
  11. Elsen, S., Swem, L. R., Swem, D. L. & Bauer, C. E. ( 2004; ). RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbiology and Molecular Biology Reviews 68, 263–279.[CrossRef]
    [Google Scholar]
  12. Emmerich, R., Strehler, P., Hennecke, H. & Fischer, H. M. ( 2000; ). An imperfect inverted repeat is critical for DNA binding of the response regulator RegR of Bradyrhizobium japonicum. Nucleic Acids Res 28, 4166–4171.[CrossRef]
    [Google Scholar]
  13. Eraso, J. M. & Kaplan, S. ( 1994; ). prrA, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacteriol 176, 32–43.
    [Google Scholar]
  14. Eraso, J. M. & Kaplan, S. ( 1997; ). Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides: a mutant histidine kinase. J Bacteriol 177, 2695–2706.
    [Google Scholar]
  15. Gomelsky, M. & Kaplan, S. ( 1997; ). Molecular genetic analysis suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 179, 128–134.
    [Google Scholar]
  16. Gomelsky, M., Horne, I. M., Lee, H. J., Pemberton, J. M., McEwan, A. G. & Kaplan, S. ( 2000; ). Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J Bacteriol 182, 2253–2261.[CrossRef]
    [Google Scholar]
  17. Jaubert, M., Zappa, S., Fardoux, J. & 7 other authors ( 2004; ). Light and redox control of photosynthesis gene expression in Bradyrhizobium. Dual roles of two PpsR*. J Biol Chem 279, 44407–44416.[CrossRef]
    [Google Scholar]
  18. Joshi, H. M. & Tabita, F. R. ( 1996; ). A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc Natl Acad Sci U S A 93, 14515–14520.[CrossRef]
    [Google Scholar]
  19. Kammler, M., Schon, C. & Hantke, K. ( 1993; ). Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175, 6212–6219.
    [Google Scholar]
  20. Kang, Y., Weber, K. D., Qiu, Y., Kiley, P. J. & Blattner, F. R. ( 2005; ). Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J Bacteriol 187, 1135–1160.[CrossRef]
    [Google Scholar]
  21. Karls, R. K., Wolf, J. R. & Donohue, T. J. ( 1999; ). Activation of the cycA P2 promoter for the Rhodobacter sphaeroides cytochrome c 2 gene by the photosynthesis response regulator. Mol Microbiol 34, 822–835.[CrossRef]
    [Google Scholar]
  22. Laguri, C., Phillips-Jones, M. K. & Williamson, M. P. ( 2003; ). Solution structure and DNA binding of the effector domain from the global regulator PrrA (RegA) from Rhodobacter sphaeroides: insights into DNA binding specificity. Nucleic Acids Res 31, 6778–6787.[CrossRef]
    [Google Scholar]
  23. Lee, J. K. & Kaplan, S. ( 1992; ). cis-acting regulatory elements involved in oxygen and light control of puc operon transcription in Rhodobacter sphaeroides. J Bacteriol 174, 1158–1171.
    [Google Scholar]
  24. Li, C. & Hung Wong, W. ( 2001; ). Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biology 2, 1–11.
    [Google Scholar]
  25. Li, C. & Wong, W. H. ( 2001; ). Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98, 31–36.[CrossRef]
    [Google Scholar]
  26. Liu, X., Brutlag, D. L. & Liu, J. S. ( 2001; ). BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. In Pacific Symposium on Biocomputing, pp. 127–138.
  27. Masuda, S. & Bauer, C. E. ( 2002; ). AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110, 613–623.[CrossRef]
    [Google Scholar]
  28. Masuda, S., Matsumoto, Y., Nagashima, K. V., Shimada, K., Inoue, K., Bauer, C. E. & Matsuura, K. ( 1999; ). Structural and functional analyses of photosynthetic regulatory genes regA and regB from Rhodovulum sulfidophilum, Roseobacter denitrificans, and Rhodobacter capsulatus. J Bacteriol 181, 4205–4215.
    [Google Scholar]
  29. Moskvin, O. V., Gomelsky, L. & Gomelsky, M. ( 2005; ). Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development. J Bacteriol 187, 2148–2156.[CrossRef]
    [Google Scholar]
  30. Oh, J. I. & Kaplan, S. ( 1999; ). The cbb 3 terminal oxidase of Rhodobacter sphaeroides 2.4.1: structural and functional implications for the regulation of spectral complex formation. Biochemistry 38, 2688–2696.[CrossRef]
    [Google Scholar]
  31. Oh, J. I. & Kaplan, S. ( 2001; ). Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39, 1116–1123.[CrossRef]
    [Google Scholar]
  32. Oh, J. I. & Kaplan, S. ( 2002; ). Oxygen adaptation. The role of the CcoQ subunit of the cbb 3 cytochrome c oxidase of Rhodobacter sphaeroides 2.4.1. J Biol Chem 277, 16220–16228.[CrossRef]
    [Google Scholar]
  33. Oh, J. I., Eraso, J. M. & Kaplan, S. ( 2000; ). Interacting regulatory circuits involved in orderly control of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 182, 3081–3087.[CrossRef]
    [Google Scholar]
  34. Pappas, C. T., Sram, J., Moskvin, O. V. & 7 other authors ( 2004; ). Construction and validation of the Rhodobacter sphaeroides 2.4.1 DNA microarray: transcriptome flexibility at diverse growth modes. J Bacteriol 186, 4748–4758.[CrossRef]
    [Google Scholar]
  35. Penfold, R. J. & Pemberton, J. M. ( 1994; ). Sequencing, chromosomal inactivation, and functional expression in Escherichia coli of ppsR, a gene which represses carotenoid and bacteriochlorophyll synthesis in Rhodobacter sphaeroides. J Bacteriol 176, 2869–2876.
    [Google Scholar]
  36. Qian, Y. & Tabita, F. R. ( 1996; ). A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter sphaeroides. J Bacteriol 178, 12–18.
    [Google Scholar]
  37. Roh, J. H. & Kaplan, S. ( 2002; ). Interdependent expression of the ccoNOQP-rdxBHIS loci in Rhodobacter sphaeroides 2.4.1. J Bacteriol 184, 5330–5338.[CrossRef]
    [Google Scholar]
  38. Roh, J. H., Smith, W. E. & Kaplan, S. ( 2004; ). Effects of oxygen and light intensity on transcriptome expression in Rhodobacter sphaeroides 2.4.1. Redox active gene expression profile. J Biol Chem 279, 9146–9155.[CrossRef]
    [Google Scholar]
  39. Sistrom, W. R. ( 1962; ). The kinetics of the synthesis of photopigments in Rhodopseudomonas sphaeroides. J Gen Microbiol 28, 607–616.[CrossRef]
    [Google Scholar]
  40. Swem, L. R., Elsen, S., Bird, T. H., Swem, D. L., Koch, H. G., Myllykallio, H., Daldal, F. & Bauer, C. E. ( 2001; ). The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. J Mol Biol 309, 121–138.[CrossRef]
    [Google Scholar]
  41. Zeilstra-Ryalls, J. H. & Kaplan, S. ( 1995; ). Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: the role of the fnrL gene. J Bacteriol 177, 6422–6431.
    [Google Scholar]
  42. Zeilstra-Ryalls, J. H. & Kaplan, S. ( 1998; ). Role of the fnrL gene in photosystem gene expression and photosynthetic growth of Rhodobacter sphaeroides 2.4.1. J Bacteriol 180, 1496–1503.
    [Google Scholar]
  43. Zeilstra-Ryalls, J. H., Gabbert, K., Mouncey, N. J., Kaplan, S. & Kranz, R. G. ( 1997; ). Analysis of the fnrL gene and its function in Rhodobacter capsulatus. J Bacteriol 179, 7264–7273.
    [Google Scholar]
  44. Zeilstra-Ryalls, J., Gomelsky, M., Eraso, J. M., Yeliseev, A., O'Gara, J. & Kaplan, S. ( 1998; ). Control of photosystem formation in Rhodobacter sphaeroides. J Bacteriol 180, 2801–2809.
    [Google Scholar]
  45. Zeng, X., Choudhary, M. & Kaplan, S. ( 2003; ). A second and unusual pucBA operon of Rhodobacter sphaeroides 2.4.1: genetics and function of the encoded polypeptides. J Bacteriol 185, 6171–6184.[CrossRef]
    [Google Scholar]
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vol. , part 10, pp. 3197–3213

Supplementary Tables S1–S8, Supplementary Figs S1–S4 and references [PDF file](460 KB)



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