The metabolism paradigm

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The sudden appearance on Earth of a system capable of both metabolism and replication is too unlikely to be taken seriously. All reasonable theories on the origin of life assume therefore that chemical evolution started from systems that could perform only one of those functions. Hence the great schism between metabolismfirst theories (Oparin's paradigm) and replication-first scenarios

(Haldane's paradigm).

In favour of the metabolism paradigm there are, first of all, the results of the simulation experiments, and in particular the fact that the abiotic production of amino acids is so much easier than that of nucleic acids. Chemistry tells us that the primitive Earth could indeed generate enormous amounts of organic molecules that were potentially capable of having some type of metabolism, and of producing structures as complex as Oparin's coacervates, Fox's microspheres, or Wachtershauser's vesicles.

The problem, of course, is to evaluate the evolutionary potential of these structures. It is true that Fox's microspheres, for example, can grow and divide by budding or fission, but they lack any form of heredity, and the simulation experiments are too brief to inform us about their long-term potential. The only way of obtaining this kind of information is by using mathematical or chemical models, and such a solution, however imperfect, does have a certain degree of plausibility.

The first model of a system that is capable of growing by metabolism and of dividing by fission was proposed - with the name of chemoton - by Ganti (1975). Such a system receives metabolites from the environment, expels waste products, and performs a metabolic cycle that begins with one molecule and ends by making two of them. The system is therefore autocatalytic, but it is not using enzymes, and this leaves us in the dark about its biological potential.

In order to have a metabolic and enzymatic system, it would be necessary to have proteinaceous enzymes which can catalyse the synthesis of other enzymes, and for this they should be capable of making peptide bonds. Such systems have not been found in nature, so far, but according to Stuart Kauffman (1986) they could have existed in the past, and in primitive compartments could have produced autocatalytic networks which had the potential to "jump" from chaos to order. Even if we admit that those enzymes existed, however, we still have the problem of accounting for the origin of the complex autocatalytic networks that housed them.

An elegant solution to this problem has been proposed by Freeman Dyson (1985) with the model of a generalised metabolic system, whose behaviour is totally random and whose chemical composition is not specified in advance. In order to describe the evolution of such a system, Dyson used Kimura's equations of genetic drift, and found that, in certain conditions, a system of inert molecules does have a finite chance of jumping from a state of inertia to a state of metabolic activity. Dyson's model is interesting because it has at least three important implications:

(1) A primitive metabolic system had to have a certain initial complexity to start with: it cannot contain fewer than 10 000 monomers for its molecules, and the monomers must be of at least ten different types (which means that amino acids are in but nucleic acids are out).

(2) The system is very tolerant of errors, and can therefore survive and leave descendants even without mechanisms of exact replication.

(3) The system can tolerate, within very wide limits, the presence of molecules which are either inert or parasitic, and therefore do not contribute to metabolism.

This last property is particularly important, because it allows Dyson to make a hypothesis on the origin of nucleic acids. The assumption is that primitive metabolic systems learned to use ATP molecules as energy sources, thus transforming them into AMP molecules that were accumulated as waste products. These packed deposits, in turn, created the conditions for the polymerisation of nucleotides, thus leading to the origin of the first RNAs. At the beginning, the RNA molecules were useless and even potentially dangerous compounds, but the system could tolerate them, and eventually the RNAs became perfectly integrated into their hosts.

Up until the origin of RNA molecules, Dyson describes the logical consequences of the initial hypotheses, and his scheme is therefore a coherent theory of chemical evolution. But the mathematical model does not say anything about the subsequent integration of RNAs and hosts, and on this point Dyson resorts to a supplementary conjecture. He proposes that primitive RNAs invaded their metabolic hosts, and used them for their own replication, like viruses do, which is exactly Haldane's hypothesis. Dyson concludes therefore that, after Oparin's metabolism stage, came Haldane's replication stage, and his final scheme becomes: "metabolism first, replication second". That RNAs could replicate themselves within precellular systems, as viruses do, is highly unlikely, but this point has nothing to do with Dyson's mathematical model, and can be regarded as an unnecessary addition. If we stick only to the intrinsic characteristics of Dyson's model, we have something very useful in our hands, because the scheme does give a valid answer to the main problem of chemical evolution: the problem of explaining how primitive systems made of proteins could be able to produce RNAs.

A somewhat parallel solution to the same problem has also been given by Wächtershäuser, with the description of an hypothetical, but plausible, sequence of chemical reactions that lead to the same final result. We have therefore both mathematical and chemical models that are capable, in principle, of explaining chemical evolution. This is only the first part of precellular evolution, and there still is a long way to go before the origin of the cell, but at least the metabolism paradigm does give us a good starting point.

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