Chapter 2. The evolution of membranes

M. Bloom
Canadian Institute for Advanced Research & Department of Physics, University of British Columbia,
6224 Agricultural Road, Vancouver, B.C., Canada V6T 1Z1

O.G. Mouritsen
Canadian Institute for Advanced Research & Department of Physical Chemistry,
The Technical University of Denmark, DK-2800, Lyngby, Denmark

1. Introduction: optimization of physical properties via evolutionary processes

Membranes play a crucial physical role in cells, defining as they do the boundary between the inside and outside of cells or organelles of cells. For this reason it is obviously appropriate to examine the evolution of membranes in relation to the
evolution of cells. Still, although the study of cellular evolution is currently an extremely active and rapidly moving field, very little consideration has been given to the evolution of membranes. As an example, the word evolution does not appear in the index of a recent, comprehensive textbook on biomembranes [1]. In a symmetrical manner, the word membrane is not be found in an authoritative treatment of evolution in a textbook on biophysics [1a]. This is not really surprising in view
of the fact that the systematic treatment of the evolution of physical properties of biological materials is a non-existent field.

Modern biology, and especially evolutionary biology, is dominated by 'molecular biology', the study at the molecular level of the transfer of genetic information. Aside from structural proteins and relevant physical properties of proteins in general,
the physical properties of biological materials are not programmed directly by the genes. The genetic code controls the synthesis of proteins, some of which act as enzymes for the synthesis or modification of other molecules. The physical properties are governed by the structures formed when these molecules aggregate in a manner dictated by the normal laws of physics and physical chemistry. Although the feedback leading to genetic control can be one or more stages removed from protein synthesis that is controlled directly by nucleic acid sequences, we assume that evolutionary processes still lead to optimization of the physical properties of biological materials because of the almost unimaginably long time scale available.

This assumption is the motivation for our examination of membrane evolution in this chapter. The assumption of optimization of physical properties via evolutionary processes cannot be proven for cell membranes at this time. A schematic illustration of the essential features of the plasma membranes of eucaryotic cells is shown in fig. 1. The lipid bilayer core of biological membranes is fluid and leads to their characteristic, ultra-soft mechanical properties [2]. Because physical scientists have had little direct experience with such soft materials, we are still at an early stage in the characterization of their physical properties at the present time. We propose that information from evolutionary considerations be used to improve our perception and understanding of 'Nature's design' in order to focus on potentially useful experimental and theoretical questions.

In view of our relative lack of experience in dealing with the physical properties of soft, natural materials, it is useful to provide some clear-cut examples of optimization of physical properties of other types of biological materials via evolutionary processes.  This is possible because biological systems also make hard, crystalline materials whose physical properties are extremely well understood and characterized using conventional condensed matter methods. Whenever such materials, made by cells, are carefully examined, they invariably prove to have been optimized via evolutionary processes. An illustrative example is given in section 2.

Fig. 1. Schematic illustration of a biological membrane showing the geometrical relationship between the lipid bilayer and other membrane features (courtesy of Mr. Broo Sorensen of the Technical University of Denmark). The membrane depicted here is representative of the plasma membranes of eucaryotic cells. The rubber-like 'cytoskeleton' attached to the cytoplasmic (inner) surface of the bilayer exerts a strong influence on the mechanical properties of such a composite membrane. The glycocalyx carbohydrate network on the outside surface is generally believed to be responsible for cell-cell recognition and adhesion to other cells. The black objects extending from one side of the lipid bilayer to the other represent integral membrane proteins.

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