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Stress, order and survival

Nature Reviews Molecular Cell Biology volume 3, pages 50–60 (2002)Cite this article

Key Points

  • Order in the inanimate world is displayed by equilibrium structures such as crystals and liquid crystals, as well as by dynamic phenomena exemplified by whirlwinds and oscillatory processes. By contrast, the chemistry and structure of living systems seem to be biased towards dynamic order, which requires energy consumption.

  • Starved bacteria protect their DNA by producing large amounts of Dps, a DNA-binding protein whose interaction with DNA results in the formation of Dps–DNA co-crystals, within which DNA molecules are physically sequestered.

  • Sporal DNA is protected by its packaging into extremely condensed and presumably ordered structures, which attenuate DNA accessibility to detrimental agents and environmental assaults.

  • Bacteria that are exposed to agents that cause double-strand DNA breaks form a highly ordered DNA–RecA co-crystal that initially promotes repair activities and subsequently allows for DNA protection through physical sequestration.

  • S-layers are crystalline arrays that cover the surface of unicellular organisms — such as bacteria and archaea — that are regularly exposed to harsh environments. These ordered structures are presumed to promote endurance of such organisms.

  • The induction of many bacteriophages and viruses is effected by environmental stress. The highly ordered crystalline-like organization of mature viruses enhances their ability to withstand environmental assaults.

  • Ordered ribosomal arrays are formed in living systems that are subjected to hypothermia or anoxia, as well as in nerve cells undergoing programmed cell death. It is proposed that ribosomal crystallization derives from stress-related attenuation of energy-dependent ribosomal transport.

  • When the cellular energy balance is severely perturbed and dynamic processes can no longer be sustained, survival can be supported by biocrystallization — the capacity of intracellular assemblies to assume an equilibrium order in the form of crystalline or liquid-crystalline structures. In these structures, vital components are protected through physical sequestration that is independent of energy consumption.

Abstract

Much of the sophisticated chemistry of life is accomplished by multicomponent complexes, which act as molecular machines. Intrinsic to their accuracy and efficiency is the energy that is supplied by hydrolysis of nucleoside triphosphates. Conditions that deplete energy sources should therefore cause decay and death. But studies on organisms that are exposed to prolonged stress indicate that this fate could be circumvented through the formation of highly ordered intracellular assemblies. In these thermodynamically stable structures, vital components are protected by a physical sequestration that is independent of energy consumption.

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Figure 1: DNA supercoiling.
Figure 2: DNA–Dps co-crystals.
Figure 3: Liquid-crystalline DNA phases.
Figure 4: DNA–RecA crystals.
Figure 5: Dps–ferritin homology18.
Figure 6: S-layers.
Figure 7: Order in dsRNA bluetongue virus.
Figure 8: Order in T7 bacteriophage.
Figure 9: Intracellular ribosome crystals.

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Acknowledgements

This article is dedicated to the memory of Shneior Lifson, a friend and mentor who, at the age of 87, passed away very young. We are indebted to D. Fass, A. Horovitz, S. Safran, Z. Reich and E. J. Wachtel from the Weizmann Institute of Science, and P. Higgins from the University of Alabama at Birmingham for helpful discussions. We thank R. A. Grant, J. M. Hogle, U. B. Sleytr, D. I. Stuart, J. F. Conway, A. C. Steven, M. Barbieri and A. McPherson for kindly providing figures

Author information

Authors and Affiliations

  1. Department of Organic Chemistry, The Weizmann Institute of Science, Rehovot, 76100, Israel

    Abraham Minsky, Eyal Shimoni & Daphna Frenkiel-Krispin

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  1. Abraham Minsky
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Correspondence to Abraham Minsky.

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DATABASES

OMIM:

Alzheimer's disease

Creutzfeldt–Jacob disease

Pick's disease

 Swiss-Prot:

Dps

HO

Rad52

Glossary

LIQUID CRYSTALS

The crystalline state is characterized by a long-range periodic order in both the position and orientation of its constituent atoms or molecules, whereas the liquid state has no long-range order. The liquid-crystalline phase is an intermediate state; a fluid whose constituents show a partial degree of orientational order.

THE BELOUSOV–ZHABOTINSKII REACTION

An example of chemical processes that are maintained far from equilibrium by autocatalysis; one of the reaction products acts to increase the reaction rate. In these processes, the concentrations of reactants and products vary periodically in space and time, which leads to the emergence of ordered, regular patterns.

HELICASE

An enzyme that unwinds the two strands of the DNA duplex to allow processes such as DNA replication, recombination, repair and transcription.

PHAGOSOMES19

When relatively large particles such as bacteria bind to the cell surface, the cell membrane engulfs the particle and internalizes it within a dynamic structure called the phagosome. After internalization, the phagosome fuses with endocytic organelles to form a mature phagolysosome, in which the particle is degraded.

PhoPQ VIRULENCE SYSTEM

This two-component regulatory system controls the pathogenic properties of the bacterium Salmonella typhimurium. PhoQ is the sensor. On sensing a drop in the concentration of Mg2+ ions outside the cell, it activates PhoP, which regulates the expression of many virulence-related genes.

CHOLESTERIC PHASE

A liquid-crystalline organization, which is composed of chiral molecules that are partially aligned in successive layers. These stacked layers continuously rotate with respect to each other to form a helical arrangement (Fig. 3c), which is characterized by unique optical properties.

INSECTICIDAL PROTEINS

During sporulation, several strains of the bacterium Bacillus thuringiensis produce a crystalline inclusion, which consists of proteins with highly toxic activity against the larvae of various insects. B. thuringiensis strains are widely used to protect crops against insect damage.

EXONUCLEASE

An enzyme that digests polynucleotide chains. It can begin at either the 3′ (3′ exonuclease) or 5′ (5′ exonuclease) termini.

HOLLIDAY JUNCTION

A four-stranded cruciform DNA structure that creates a physical link between DNA duplexes.

BRANCH MIGRATION

The process of exchange of base-pairing partners at a helical junction formed from homologous sequences.

RESOLUTION

Cleavage of the Holliday junction to generate two DNA duplexes.

THE FENTON REACTION

A chemical process in which highly reactive ·OH radicals are produced when Fe2+ ions are oxidized in aqueous solutions to Fe3+ ions.

BACTERIOPHAGES

Viruses that infect bacteria.

ICOSAHEDRAL SYMMETRY

An icosahedron is composed of 20 facets, each an equilateral triangle, and 12 vertices. The structure is referred to as having a 5:3:2 symmetry, because it shows six five-fold axes, which pass through the vertices; ten three-fold axes, which extend through each face; and fifteen two-fold axes, which pass through the edges.

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Minsky, A., Shimoni, E. & Frenkiel-Krispin, D. Stress, order and survival. Nat Rev Mol Cell Biol 3, 50–60 (2002). https://doi.org/10.1038/nrm700

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