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Biochemical, Molecular Genetic, and Structural Analyses of the Staphylococcal Nucleoid

Published online by Cambridge University Press:  18 January 2007

Kazuya Morikawa ,
Ryosuke L. Ohniwa ,
Joongbaek Kim ,
Sayaka L. Takeshita ,
Atsushi Maruyama ,
Yumiko Inose ,
Kunio Takeyasu  and
Toshiko Ohta
Kazuya Morikawa
Affiliation:
Institute of Basic Medical Sciences, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennoh-dai, Tsukuba 305-8575, Japan
Ryosuke L. Ohniwa
Affiliation:
Laboratory of Plasma Membrane and Nuclear Signaling, Kyoto University Graduate School of Biostudies, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto 606-8502, Japan
Joongbaek Kim
Affiliation:
Laboratory of Plasma Membrane and Nuclear Signaling, Kyoto University Graduate School of Biostudies, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto 606-8502, Japan
Sayaka L. Takeshita
Affiliation:
Institute of Basic Medical Sciences, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennoh-dai, Tsukuba 305-8575, Japan
Atsushi Maruyama
Affiliation:
Institute of Basic Medical Sciences, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennoh-dai, Tsukuba 305-8575, Japan
Yumiko Inose
Affiliation:
Institute of Basic Medical Sciences, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennoh-dai, Tsukuba 305-8575, Japan
Kunio Takeyasu
Affiliation:
Laboratory of Plasma Membrane and Nuclear Signaling, Kyoto University Graduate School of Biostudies, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto 606-8502, Japan
Toshiko Ohta
Affiliation:
Institute of Basic Medical Sciences, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennoh-dai, Tsukuba 305-8575, Japan
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Abstract

The nucleoid structure of an important human pathogen, Staphylococcus aureus, was dissected by atomic force microscopy (AFM). The nucleoids dispersed on a cover glass consisted of fibrous units with two different widths of 40 and 80 nm, a feature shared with those of Escherichia coli. On the other hand, cells exposed to an oxidative stress exhibited clogged nucleoids. A knock-out of mrgA (metallo regulated genes A) encoding a staphylococcal homolog of the nucleoid compaction factor (E. coli Dps) eliminated the compaction response to the oxidative stress and reduced the susceptibilities to H2O2 and UV irradiation. We also observed that the negative supercoiling of plasmids is increased by the oxidative stress. A possible interrelation between the helical density and the nucleoid compaction is discussed in relation to the oxidative stress response.

Keywords

AFMnucleoidoxidative-stressStaphylococcus aureusMrgAsuperhelicity
Type
Research Article
Information
Microscopy and Microanalysis , Volume 13 , Issue 1: Special Issue: Environmental, Industrial, and AppliedMicrobiology , February 2007 , pp. 30 - 35
Copyright
2007 Microscopy Society of America

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References

REFERENCES

Alice, A.F. & Sanchez-Rivas, C. (1997). DNA supercoiling and osmoresistance in Bacillus subtilis 168. Curr Microbiol 35, 309–315.Google Scholar
Altuvia, S., Almiron, M., Huisman, G., Kolter, R. & Storz, G. (1994). The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol 13, 265–272.Google Scholar
Becerra, M.C. & Albesa, I. (2002). Oxidative stress induced by ciprofloxacin in Staphylococcus aureus. Biochem Biophys Res Commun 297, 1003–1007.Google Scholar
Dame, R.T. (2005). The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol Microbiol 56, 858–870.Google Scholar
Fournier, B. & Klier, A. (2004). Protein A gene expression is regulated by DNA supercoiling which is modified by the ArlS-ArlR two-component system of Staphylococcus aureus. Microbiology 150, 3807–3819.Google Scholar
Hansma, H.G. & Hoh, J.H. (1994). Biomolecular imaging with the atomic force microscope. Annu Rev Biophys Biomol Struct 23, 115–139.Google Scholar
Kim, J., Yoshimura, S.H., Hizume, K., Ohniwa, R.L., Ishihama, A. & Takeyasu, K. (2004). Fundamental structural units of the Escherichia coli nucleoid revealed by atomic force microscopy. Nucleic Acids Res 32, 1982–1992.Google Scholar
Kuwahara-Arai, K., Kondo, N., Hori, S., Tateda-Suzuki, E. & Hiramatsu, K. (1996). Suppression of methicillin resistance in a mecA-containing pre-methicillin-resistant Staphylococcus aureus strain is caused by the mecI-mediated repression of PBP 2′ production. Antimicrob Agents Chemother 40, 2680–2685.Google Scholar
Martinez, A. & Kolter, R. (1997). Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179, 5188–5194.Google Scholar
Morikawa, K., Inose, Y., Okamura, H., Maruyama, A., Hayashi, H., Takeyasu, K. & Ohta, T. (2003). A new staphylococcal sigma factor in the conserved gene cassette: Functional significance and implication for the evolutionary processes. Genes Cells 8, 699–712.Google Scholar
Morikawa, K., Maruyama, A., Inose, Y., Higashide, M., Hayashi, H. & Ohta, T. (2001). Overexpression of sigma factor, sB, urges Staphylococcus aureus to thicken the cell wall and to resist b-lactams. Biochem Biophys Res Commun 288, 385–389.Google Scholar
Morikawa, K., Ohniwa, R.L., Kim, J., Maruyama, A., Ohta, T. & Takeyasu, K. (2006). Bacterial nucleoid dynamics: Oxidative stress response in Straphylococcus aureus. Genes Cells 11, 409–423.Google Scholar
Muskhelishvili, G. & Travers, A. (2003). Transcription factor as a topological homeostat. Front Biosci 8, d279–285.Google Scholar
Nair, S. & Finkel, S.E. (2004). Dps protects cells against multiple stresses during stationary phase. J Bacteriol 186, 4192–4198.Google Scholar
Ren, B., Tibbelin, G., Kajino, T., Asami, O. & Ladenstein, R. (2003). The multi-layered structure of Dps with a novel di-nuclear ferroxidase center. J Mol Biol 329, 467–477.Google Scholar
Schneider, S.W., Larmer, J., Henderson, R.M. & Oberleithner, H. (1998). Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pflugers Arch 435, 362–367.Google Scholar
Sheridan, S.D., Opel, M.L. & Hatfield, G.W. (2001). Activation and repression of transcription initiation by a distant DNA structural transition. Mol Microbiol 40, 684–690.Google Scholar
Takeyasu, K., Kim, J., Ohniwa, R.L., Kobori, T., Inose, Y., Morikawa, K., Ohta, T., Ishihama, A. & Yoshimura, S.H. (2004). Genome architecture studied by nanoscale imaging: Analyses among bacterial phyla and their implication to eukaryotic genome folding. Cytogenet Genome Res 107, 38–48.Google Scholar
Talukder, A.A., Iwata, A., Nishimura, A., Ueda, S. & Ishihama, A. (1999). Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181, 6361–6370.Google Scholar
Tseng, C.P. (1997). Regulation of fumarase (fumB) gene expression in Escherichia coli in response to oxygen, iron and heme availability: Role of the arcA, fur, and hemA gene products. FEMS Microbiol Lett 157, 67–72.Google Scholar
Weinstein-Fischer, D., Elgrably-Weiss, M. & Altuvia, S. (2000). Escherichia coli response to hydrogen peroxide: A role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35, 1413–1420.Google Scholar