The first biochemical systems were centered on RNA
Polymerization of the building blocks into biomolecules might have occurred in the oceans or could have been promoted by the repeated condensation and drying of droplets of water in clouds (Woese, 1979). Alternatively, polymerization might have taken place on solid surfaces, perhaps making use of monomers immobilized on clay particles (Wächtershäuser, 1988), or in hydrothermal vents (Wächtershäuser, 1992). The precise mechanism need not concern us; what is important is that it is possible to envisage purely geochemical processes that could lead to synthesis of polymeric biomolecules similar to the ones found in living systems. It is the next steps that we must worry about. We have to go from a random collection of biomolecules to an ordered assemblage that displays at least some of the biochemical properties that we associate with life. These steps have never been reproduced experimentally and our ideas are therefore based mainly on speculation tempered by a certain amount of computer simulation. One problem is that the speculations are unconstrained because the global ocean could have contained as many as 1010 biomolecules per liter and we can allow a billion years for the necessary events to take place. This means that even the most improbable scenarios cannot be dismissed out of hand and a way through the resulting maze has been difficult to find.
Progress was initially stalled by the apparent requirement that polynucleotides and polypeptides must work in harness in order to produce a self-reproducing biochemical system. This is because proteins are required to catalyze biochemical reactions but cannot carry out their own self-replication. Polynucleotides can specify the synthesis of proteins and self-replicate, but it was thought that they could do neither without the aid of proteins. It appeared that the biochemical system would have to spring fully formed from the random collection of biomolecules because any intermediate stage could not be perpetuated. The major breakthrough came in the mid-1980s when it was discovered that RNA can have catalytic activity. Those ribozymes that are known today carry out three types of biochemical reaction:
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In the test tube, synthetic RNA molecules have been shown to carry out other biologically relevant reactions such as synthesis of ribonucleotides (Unrau and Bartel, 1998), synthesis and copying of RNA molecules (Ekland and Bartel, 1996; Johnston et al., 2001) and transfer of an RNA-bound amino acid to a second amino acid forming a dipeptide, in a manner analogous to the role of tRNA in protein synthesis (Section 11.1; Lohse and Szostak, 1996). The discovery of these catalytic properties solved the polynucleotide-polypeptide dilemma by showing that the first biochemical systems could have been centered entirely on RNA (Bartel and Unrau, 1999).
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Ideas about the RNA world have taken shape in recent years (Robertson and Ellington, 1998). We now envisage that RNA molecules initially replicated in a slow and haphazard fashion simply by acting as templates for binding of complementary nucleotides which polymerized spontaneously (Figure 15.2). This process would have been very inaccurate so a variety of RNA sequences would have been generated, eventually leading to one or more with nascent ribozyme properties that were able to direct their own, more accurate self-replication. It is possible that a form of natural selection operated so that the most efficient replicating systems began to predominate, as has been shown to occur in experimental systems. A greater accuracy in replication would have enabled RNAs to increase in length without losing their sequence specificity, providing the potential for more sophisticated catalytic properties, possibly culminating in structures as complex as present-day Group I introns (see Figure 10.26) and ribosomal RNAs (see Figure 11.11).
To call these RNAs ‘genomes’ is a little fanciful, but the term protogenome has attractions as a descriptor for molecules that are self-replicating and able to direct simple biochemical reactions. These reactions might have included energy metabolism, based, as today, on the release of free energy by hydrolysis of the phosphate-phosphate bonds in the ribonucleotides ATP and GTP, and the reactions might have become compartmentalized within lipid membranes, forming the first cell-like structures. There are difficulties in envisaging how long-chain unbranched lipids could form by chemical or ribozyme-catalyzed reactions, but once present in sufficient quantities they would have assembled spontaneously into membranes, possibly encapsulating one or more protogenomes and providing the RNAs with an enclosed environment in which more controlled biochemical reactions could be carried out.
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