DNA Condensation in Bacteria

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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.

About the authors

Yu. F. Krupyanskii

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science

Email: yufk@chph.ras.ru
Moscow, Russia

A. A. Generalova

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science

Email: yufk@chph.ras.ru
Moscow, Russia

V. V. Kovalenko

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science

Email: yufk@chph.ras.ru
Moscow, Russia

N. G. Loiko

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science;
Federal Research Center “Fundamentals of Biotechnology” Russian Academy of Sciences

Email: yufk@chph.ras.ru
Moscow, Russia; Moscow, Russia

E. V. Tereshkin

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science

Email: yufk@chph.ras.ru
Moscow, Russia

A. V. Moiseenko

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science; Moscow State University

Email: yufk@chph.ras.ru
Moscow, Russia; Moscow, Russia

K. B. Tereshkina

Semyonov Federal Research Center for Chemical Physic, Russian Academy of Science

Email: yufk@chph.ras.ru
Moscow, Russia

O. S. Sokolova

Moscow State University

Email: yufk@chph.ras.ru
Moscow, Russia

A. N. Popov

European Synchrotron Radiation Facility

Author for correspondence.
Email: yufk@chph.ras.ru
38043, Grenoble, France

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Copyright (c) 2023 Ю.Ф. Крупянский, А.А. Генералова, В.В. Коваленко, Н.Г. Лойко, Э.В. Терешкин, А.В. Моисеенко, К.Б. Терешкина, О.С. Соколова, А.Н. Попов