Order for Free: Molecular Diversity and Complexity Promote Self‐Organisation

45 In his book aAt Home in the Universeo, Stuart Kauffman describes a living organism as a system of chemicals that has the capacity to catalyse its own reproduction. In his view, achieving autocatalytic closure among a collection of molecular species becomes the root property of life. Alone, each molecular species is adeado; jointly, the collective system of molecules is aaliveo. The Kauffman thesis is very compelling for the chemical biologist since catalysis is no longer relegated to being a sustainer of life but instead becomes a key originator of life. However, catalysis alone cannot be enough to originate life. All living systems aeato; they take in matter and energy in order to sustain and reproduce themselves. Therefore, living systems must be the equivalent of closed autocatalytic but open (nonequilibrium) thermodynamic systems. But even supposing that life can originate from autocatalytic closure among a collection of molecular species, how does this view of life account for the fearsome order that characterises living systems and seems so much at variance with the second law of thermodynamics? In Kauffman's view, molecular diversity and complexity in an open thermodynamic system themselves give order, aorder for freeo or self-organisation that arises naturally. In other words, order (selforganisation) is a direct consequence of molecular diversity and complexity. Compartmentalisation is a key part of the self-organisation process, if for nothing else than to sustain spatial integrity and prevent dilution of the reacting molecules that comprise each open thermodynamic, closed autocatalytic living system. The ability of lipids to self-assemble into lipid bilayers and more complex mesophases is well established, and has long been accepted to form a key part of compartmentalisation in biology. However, living cells also possess an intricate cytoskeleton involving proteins such as globular monomeric actin (G-actin) and the filamentous actin (F-actin). In this context, a recent publication by Wong et al. is interesting. They described the spontaneous hierarchical self-assembly of F-actin filaments and cationic lipid membranes into tubules (approximately 0.25 100 mm) consisting of stacks of composite membranes composed of three layers, a lipid bilayer sandwiched between two layers of actin; a structural organisation highly reminiscent of multilayered bacterial cell walls that exist far from closed equilibrium (Figures 1 and 2). Wong et al. suggested that these tubules with their composite membrane architecture could be considered as spontaneously assembled aartificialo bacteria. If we accept this conclusion then this publication should be regarded as important for providing evidence of molecular diversity and complexity leading to lifelike aorder for freeo. Amongst biologists, discussions about the origins of life have been focussed by arguments of natural selection. There has been an apparent tendency to ignore selforganisation. Most likely this is because there is a fundamental difficulty in recognising how living systems may be governed simultaneously by two sources of order, self-organisation born of molecular diversity and complexity, and the aforceso of natural selection. However if we are to understand properly the origin of life, a final theory of biology must allow for the commingling of self-organisation and selection processes as an expression of an even deeper order. Surely, as Kauffman argues, self-organisation precedes natural selection. Stable, low-energy, self-organised states (arobust systemso) such as lipid bilayers and mesophases, the structures described by Wong et al. , the DNA Order for Free: Molecular Diversity and Complexity Promote Self-Organisation Andrew D. Miller*