Abstract
BackgroundThe RNA world concept has wide, though certainly not unanimous, support within the origin-of-life scientific community. One view is that life may have emerged as early as the Hadean Eon 4.3-3.8 billion years ago with an atmosphere of high CO2 producing an acidic ocean of the order of pH 3.5-6. Compatible with this scenario is the intriguing proposal that life arose within alkaline (pH 9-11) deep-sea hydrothermal vents like those of the 'Lost City', with the interface with the acidic ocean creating a proton gradient sufficient to drive the first metabolism. However, RNA is most stable at pH 4-5 and is unstable at alkaline pH, raising the possibility that RNA may have first arisen in the acidic ocean itself (possibly near an acidic hydrothermal vent), acidic volcanic lake or comet pond. As the Hadean Eon progressed, the ocean pH is inferred to have gradually risen to near neutral as atmospheric CO2 levels decreased.Presentation of the hypothesisWe propose that RNA is well suited for a world evolving at acidic pH. This is supported by the enhanced stability at acidic pH of not only the RNA phosphodiester bond but also of the aminoacyl-(t)RNA and peptide bonds. Examples of in vitro-selected ribozymes with activities at acid pH have recently been documented. The subsequent transition to a DNA genome could have been partly driven by the gradual rise in ocean pH, since DNA has greater stability than RNA at alkaline pH, but not at acidic pH.Testing the hypothesisWe have proposed mechanisms for two key RNA world activities that are compatible with an acidic milieu: (i) non-enzymatic RNA replication of a hemi-protonated cytosine-rich oligonucleotide, and (ii) specific aminoacylation of tRNA/hairpins through triple helix interactions between the helical aminoacyl stem and a single-stranded aminoacylating ribozyme.Implications of the hypothesisOur hypothesis casts doubt on the hypothesis that RNA evolved in the vicinity of alkaline hydrothermal vents. The ability of RNA to form protonated base pairs and triples at acidic pH suggests that standard base pairing may not have been a dominant requirement of the early RNA world.ReviewersThis article was reviewed by Eugene Koonin, Anthony Poole and Charles Carter (nominated by David Ardell).
Highlights
The RNA world concept has wide, though certainly not unanimous, support within the origin-of-life scientific community
Testing the hypothesis: We have proposed mechanisms for two key RNA world activities that are compatible with an acidic milieu: (i) non-enzymatic RNA replication of a hemi-protonated cytosine-rich oligonucleotide, and (ii) specific aminoacylation of tRNA/hairpins through triple helix interactions between the helical aminoacyl stem and a single-stranded aminoacylating ribozyme
Michael Russell and colleagues have proposed that life arose within alkaline deep-sea hydrothermal vents similar to those of the Lost City [8,9], with the interface with the acidic ocean forming iron sulfide structures that functioned as proto-membranes, across which a proton gradient occurred sufficient to drive the first metabolism
Summary
The concept of an RNA world - an early stage of evolution where RNA functioned as both gene and catalyst has wide, though certainly not unanimous, support among those who study the origin of life. Ribozymes active at acidic pH sometimes maximally - catalyse RNA ligation [13,14,16], self-cleavage [11] (Figure 3) and amino acid-activation (similar to the synthesis of aminoacyladenylates by modern protein aminoacyl-tRNA synthetases) [17] This is a limited number of activities but all would have been important in the context of an RNA world. The results indicate that the peptide bond is stable over the range pH 4-7.5, with optimum stability at pH 6 This is consistent with our current understanding that protein synthesis arose within the RNA world, which, according to our hypothesis, would have been when conditions were still relatively acidic (see Figure 2). It is possible that the rise in ocean pH as
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
