Dps Is a Stationary Phase-Specific Protein of Escherichia coli Nucleoid

Abstract

Bacterial genomic DNA is highly organized into one or few compacted bodies known as nucleoid, which is composed of DNA, RNA and several DNA-binding proteins. These DNA-binding proteins require essential alterations in their expression during stationary phase of growth in order to re-spond to stressful environmental conditions. Dps (DNA-binding protein from starved cells) is one of such DNA-binding proteins, which accumulates most when E. coli cells reach to the stationary phase. Here, we have characterized Dps protein under various growth phases. Immunofluorescent microscopic observation reveals that Dps plays a key role in final round of genome compaction during the stationary phase. Similar results are also obtained by Western immunoblot analysis, after quantification of Dps protein from the exponential phase and early stationary phase nucleoid bound fractions, separated by sucrose density gradient centrifugation. Our results support the conclusion that Dps occupies more than half of the stationary phase nucleoid in E. coli.

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Talukder, A. and Ishihama, A. (2014) Dps Is a Stationary Phase-Specific Protein of Escherichia coli Nucleoid. Advances in Microbiology, 4, 1095-1104. doi: 10.4236/aim.2014.415120.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Rouviere-Yaniv, J., Yaniv, M. and Germond, J.E. (1979) E. coli DNA Binding Protein HU Forms Nucleosome Like Structure with Circular Double-Stranded DNA. Cell, 17, 265-274.
http://dx.doi.org/10.1016/0092-8674(79)90152-1
[2] Hecht, R.M., Taggart, R.T. and Pettijohn, D.E. (1975) Size and DNA Content of Purified E. coli Nucleoids Observed by Fluorescence Microscopy. Nature, 253, 60-62.
http://dx.doi.org/10.1038/253060a0
[3] Ishihama, A. (1999) Modulation of the Nucleoid, the Transcription Apparatus and the Translation Machinery for Stationary Phase Survival. Genes to Cells, 4, 135-143.
[4] Stonington, O.G. and Pettijohn, D.E. (1971) The Folded Genome of Escherichia coli Isolated in a Protein-DNA-RNA Complex. Proceedings of Natural Academy of Sciences of the United States of America, 68, 6-9.http://dx.doi.org/10.1073/pnas.68.1.6
[5] Makinoshima, H., Nishimura, A. and Ishihama, A. (2002) Fractionation of Escherichia coli Cell Populations at Different Stages during Growth Transition to Stationary Phase. Molecular Microbiology, 43, 269-279.http://dx.doi.org/10.1046/j.1365-2958.2002.02746.x
[6] Jishage, M. and Ishihama, A. (1997) Variation in RNA Polymerase Sigma Subunit Composition within Different Stocks of Escherichia coli W3110. Journal of Bacteriology, 179, 959-963.
[7] Almiron, M., Link, A.J., Furlong, D. and Kolter, R. (1992) A Novel DNA-Binding Protein with Regulatory and Protective Roles in Starved Escherichia coli. Genes & Development, 6, 2646-2654.
http://dx.doi.org/10.1101/gad.6.12b.2646
[8] Ali Azam, T., Iwata, A., Nishimura, A., Ueda, S. and Ishihama, A. (1999). Growth Phase-Dependent Variation in Protein Composition of the Escherichia coli Nucleoid. Journal of Bacteriology, 181, 6361-6370.
[9] Martinez, A. and Kolter, R. (1997) Protection of DNA during Oxidative Stress by the Nonspecific DNA-Binding Protein Dps. Journal of Bacteriology, 179, 5188-5194.
[10] Talukder, A.A. (2005) Survival and Death in Bacteria. In: Yamada, M., Ed., Structure and Composition of Escherichia coli Nucleoid, Research Signpost, Kerala, Vol. 2, 77-101.
[11] Ali Azam, T., Hiraga, S. and Ishihama, A. (2000) Two Types of Localization of the DNA-Binding Proteins within the Escherichia coli Nucleoid. Genes to Cells, 5, 613-626.
http://dx.doi.org/10.1046/j.1365-2443.2000.00350.x
[12] Ali Azam, T. and Ishihama, A. (1999) Twelve Species of the Nucleoid-Associated Protein from Escherichia coli. Sequence Recognition Specificity and DNA Binding Affinity. Journal of Biological Chemistry, 274, 33105-33113.http://dx.doi.org/10.1074/jbc.274.46.33105
[13] Grant, R.A., Filman, D.J., Finkel, S.E., Kolter, R. and Hogle, J.M. (1998) The Crystal Structure of Dps, a Ferritin Homolog That Binds and Protects DNA. Nature Structural Biology, 5, 294-303.
http://dx.doi.org/10.1038/nsb0498-294
[14] Kim, J., Yoshimura, S.H., Hizume, K., Ohniwa, R.L, Ishihama, A. and Takeyasu, K., (2004) Fundamental Structural Units of the Escherichia coli Nucleoid Revealed by Atomic Force Microscopy. Nucleic Acid Research, 32, 1982-1992.http://dx.doi.org/10.1093/nar/gkh512
[15] Kornberg, T., Lockwood, A. and Worcel, A. (1974) Replication of the Escherichia coli Chromosome with a Soluble Enzyme System. Proceedings of the National Academy of Sciences of the United States of America, 71, 3189-3193.http://dx.doi.org/10.1073/pnas.71.8.3189
[16] Murphy, L.D. and Zimmerman, S.B. (1997) Isolation and Characterization of Spermidine Nucleoids from Escherichia coli. Journal of Structural Biology, 199, 336-346.
http://dx.doi.org/10.1006/jsbi.1997.3884
[17] Ball, C.A., Osuna, R., Ferguson, K.C. and Johnson, R.C. (1992) Dramatic Changes in Fis Levels upon Nutrient Upshift in Escherichia coli. Journal of Bacteriology, 174, 8043-8056.
[18] Sato, Y.T., Watanabe, S., Kenmotsu, T., Ichikawa, M., Yoshikawa, Y., Teramoto, J., Imanaka, T., Ishihama, A. and Yoshikawa, K. (2013) Structural Change of DNA Induced by Nucleoid Proteins: Growth Phase-Specific Fis and Stationary Phase-Specific Dps. Biophysics Journal, 105, 1037-1044. http://dx.doi.org/10.1016/j.bpj.2013.07.025
[19] Pettijohn, D.E. (1996) The Nucleoid. In: Neidhardt, F.C., et al., Eds., Escherichia coli and Salmonella, American Society for Microbiology Press, Washington DC, 158-166.
[20] Ghosh, S., Mallick, B. and Nagaraja, V. (2014) Direct Regulation of Topoisomerase Activity by a Nucleoid-Associated Protein. Nucleic Acids Research, 42, 11156-11165.
http://dx.doi.org/10.1093/nar/gku804
[21] Ishihama, A. (2009) The Nucleoid: An Overview. In: Neidhardt, F.C., et al., Eds., Escherichia coli and Salmonella, 2nd Version, American Society for Microbiology Press, Washington DC.
[22] Cournac, A. and Plumbridge, J. (2013) DNA Looping in Prokaryotes: Experimental and Theoretical Approaches. Journal of Bacteriology, 195, 1109-1119. http://dx.doi.org/10.1128/JB.02038-12
[23] Wolf, S.G., Frenkiel, D., Arad, T., Finkel, S.E., Kolter, R. and Minsky, A. (1999) DNA Protection by Stress-Induced Biocrystallization. Nature, 400, 83-85. http://dx.doi.org/10.1038/21918
[24] Meyer, A.S. and Grainger, D.C. (2013) The Escherichia coli Nucleoid in Stationary Phase. Advance in Applied Microbiology, 83, 69-86. http://dx.doi.org/10.1016/B978-0-12-407678-5.00002-7
[25] Ohniwa, R.L., Muchaku, H., Saito, S., Wada, C. and Morioka, K. (2013) Atomic Force Microscopy Analysis of the Role of Major DNA-Binding Proteins in Organization of the Nucleoid in Escherichia coli. PLoS ONE, 8, e72954.http://dx.doi.org/10.1371/journal.pone.0072954

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