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DNA Condensation in Bacteria

  • ON THE 100th ANNIVERSARY OF THE BIRTH OF ACADEMICIAN V.I. GOLDANSKY
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Russian Journal of Physical Chemistry B Aims and scope Submit manuscript

Abstract

Deoxyribonucleic acid (DNA) is organized hierarchically in the nucleoid of an actively growing cell, with three levels of DNA compaction. The lower level (small scale ≥1 kb base pairs (bps)) is provided by the interaction with DNA-bound proteins. Actively growing cells maintain a dynamic, far from equilibrium order through metabolism. When cells enter a dormant state (almost complete absence of metabolism), the usual biochemical methods of protecting DNA cease to work, and the cells, adapting to the new conditions, are forced to use the physical mechanisms of DNA protection. The structure of DNA in the nucleoid of dormant cells formed during starvation stress is studied using synchrotron radiation diffraction and transmission electron microscopy (TEM). The experimental results make it possible to visualize the structures of the lower hierarchical level of DNA compaction in the nucleoid of dormant cells. A series of diffraction experiments conducted for the first time indicate the presence of a periodic ordered organization of DNA in all the studied bacteria. The TEM method made it possible to extract fine visual information about the type of DNA condensation in the nucleoid of the bacterium Escherichia coli (E. coli). Intracellular nanocrystalline, as well as liquid-crystalline and folded nucleosome-like, structures of DNA are found. The folded nucleosome-like structure was observed for the first time and is the result of the multiple folding of long DNA molecules around the DNA-binding protein (Dps) of starved cells and its associates. The different types of condensed state of DNA found by us in the studied dormant E. coli cells (DNA condensation heterogeneity) provide additional arguments in favor of the concept that considers a microbial population as a multicellular organism. The study of changes in the DNA architecture under the effect of the chemical analog of the autoinducer of anabiosis 4-hexylresorcinol (4-HR) is studied. An increase in the 4-HR concentration induces the transition of a part of the cells of the population to anabiotic dormant state, and then to a mummified state. The studies of the structure of DNA in the anabiotic and mummified states show the spectroscopic identity of the DNA structure in the dormant anabiotic state and in the dormant state formed during starvation stress. Studies of the structure of DNA in the mummified state show a strong difference from the structure of DNA in the anabiotic state.

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ACKNOWLEDGMENTS

The authors thank the ESRF staff for the opportunity to conduct experiments. The analytical electron microscopy and biaxial tomography were performed at the User Center “Electron microscopy in life sciences,” Moscow State University. The calculations were carried out on a high-performance MVS-10P computer system at the Interdepartmental Supercomputer Center of the Russian Academy of Sciences.

Funding

The authors thank the Russian Ministry of Science and Higher Education for financially supporting this study, which was carried out as part of a state task of the Russian Ministry of Education and Science (subject nos. 122040400089-6 and 122040800164-6).

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Authors and Affiliations

  1. Semyonov Federal Research Center for Chemical Physic, Russian Academy of Sciences, Moscow, Russia

    Yu. F. Krupyanskii, A. A. Generalova, V. V. Kovalenko, N. G. Loiko, E. V. Tereshkin, A. V. Moiseenko & K. B. Tereshkina

  2. Federal Research Center “Fundamentals of Biotechnology” Russian Academy of Sciences, Moscow, Russia

    N. G. Loiko

  3. Moscow State University, Moscow, Russia

    A. V. Moiseenko & O. S. Sokolova

  4. European Synchrotron Radiation Facility, 38043, Grenoble, France

    A. N. Popov

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  1. Yu. F. Krupyanskii
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  2. A. A. Generalova
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  3. V. V. Kovalenko
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  4. N. G. Loiko
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  6. A. V. Moiseenko
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  7. K. B. Tereshkina
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  8. O. S. Sokolova
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  9. A. N. Popov
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Correspondence to Yu. F. Krupyanskii.

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Krupyanskii, Y.F., Generalova, A.A., Kovalenko, V.V. et al. DNA Condensation in Bacteria. Russ. J. Phys. Chem. B 17, 517–532 (2023). https://doi.org/10.1134/S1990793123030211

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  • DOI: https://doi.org/10.1134/S1990793123030211

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