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From water and ions to crowded biomacromolecules: in vivo structuring of a prokaryotic cell - PubMed

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Review

. 2011 Sep;75(3):491-506, second page of table of contents.

doi: 10.1128/MMBR.00010-11.

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Review

From water and ions to crowded biomacromolecules: in vivo structuring of a prokaryotic cell

Jan Spitzer. Microbiol Mol Biol Rev. 2011 Sep.

Abstract

The interactions and processes which structure prokaryotic cytoplasm (water, ions, metabolites, and biomacromolecules) and ensure the fidelity of the cell cycle are reviewed from a physicochemical perspective. Recent spectroscopic and biological evidence shows that water has no active structuring role in the cytoplasm, an unnecessary notion still entertained in the literature; water acts only as a normal solvent and biochemical reactant. Subcellular structuring arises from localizations and interactions of biomacromolecules and from the growth and modifications of their surfaces by catalytic reactions. Biomacromolecular crowding is a fundamental physicochemical characteristic of cells in vivo. Though some biochemical and physiological effects of crowding (excluded volume effect) have been documented, crowding assays with polyglycols, dextrans, etc., do not properly mimic the compositional variety of biomacromolecules in vivo. In vitro crowding assays are now being designed with proteins, which better reflect biomacromolecular environments in vivo, allowing for hydrophobic bonding and screened electrostatic interactions. I elaborate further the concept of complex vectorial biochemistry, where crowded biomacromolecules structure the cytosol into electrolyte pathways and nanopools that electrochemically "wire" the cell. Noncovalent attractions between biomacromolecules transiently supercrowd biomacromolecules into vectorial, semiconducting multiplexes with a high (35 to 95%)-volume fraction of biomacromolecules; consequently, reservoirs of less crowded cytosol appear in order to maintain the experimental average crowding of ∼25% volume fraction. This nonuniform crowding model allows for fast diffusion of biomacromolecules in the uncrowded cytosolic reservoirs, while the supercrowded vectorial multiplexes conserve the remarkable repeatability of the cell cycle by preventing confusing cross talk of concurrent biochemical reactions.

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Figures

Fig. 1.
Fig. 1.

(a) General origin of complementarity of electrolyte pathways to crowded charged particles at a 25% volume fraction (over 50% with Debye lengths added). There is no bulk concentration of solutes dissolved in water. The small circles emphasize that ionic distributions are nonuniform everywhere throughout the volume of crowded spheres. (b) Hydrophobic and screened electrostatic attractions bring about complex structures with a very-high-volume fraction of particles (multiplexes), with semiconducting pathways and nanopools and larger reservoirs with quasi-bulk concentrations of ions and low-molecular-weight dissolved compounds.

Fig. 2.
Fig. 2.

Cartoon of an electrolyte pathway that is permeable to cations only, with an active electrochemical gradient between the ionic pools. Surface potential reaches over −25.7 mV in the pathway at 25°C.

Fig. 3.
Fig. 3.

System of supercrowded spatiotemporal semiconductors “spot welded” by attractive noncovalent forces (screened electrostatic and hydrophobic forces), giving a multiplex of electrolyte nanopools and electrolyte pathways fed from larger electrolyte reservoirs, such as the ATP/ADP reservoir.

Fig. 4.
Fig. 4.

Model of unequal biomacromolecular crowding in vivo at a larger scale. A supercrowded multiplex with electrolyte nanopools and semiconducting pathways and uncrowded reservoirs of cytosolic electrolyte (quasi-bulk concentrations) with a low content of biomacromolecules is shown.

Fig. 5.
Fig. 5.

Physicochemical model of a cell, characterized by electrostatic and pressure differences across the cell envelope and between the cytosolic reservoirs and the nucleoid (not shown). The membrane is red, with attached supercrowded multiplexes and nucleoid excrescences on the inside and the cell wall and extracellular layers on the outside. Ribosomes (blue circles) are distributed mostly along the periphery of the nucleoid, which is connected spatiotemporally to the cell envelope. Signaling receptors are shown to span the cell envelope (bottom and left); they convert extracellular physicochemical signals into cytoplasmic signals that are transmitted vectorially to specific cytoplasmic “addresses” during the cell cycle.

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