Darwin’s prescient guess

Pearce et al. (1) have made a bold and challenging attempt to provide a quantitative estimate for the accumulation of nucleobases, like adenine, on the Hadean Earth some 4 billion y ago, before life began. Why bold? There must have been a source of organic compounds for life to begin, and they chose an extraterrestrial source—carbonaceous meteorites—rather than the geochemical source more commonly assumed in origins of life research. Why challenging? The authors chose to model the origin of life in fresh-water ponds on volcanic land masses emerging from a global ocean, in direct contrast to the current paradigm that life originated in sea water using chemical energy associated with hydrothermal vents.

The reason for these choices is that so little is known with certainty about the late Hadean Era, that it was essential to impose constraints to perform a mathematical treatment. This is why Pearce et al. (1) modeled extraterrestrial delivery and lifetimes of a nucleobase in the “warm little ponds” of the article’s title. The use of this phrase, which they abbreviate WLP, alludes to the site first proposed by Darwin in 1871 in a letter to his friend Joseph Hooke. Small, fresh-water ponds are common in volcanic regions of today’s Earth, making it feasible that there were multiple volcanoes and ponds 4 billion y ago. In fact, a recent publication reported evidence that the oldest fossil evidence of life on Earth 3.5 billion y ago are stromatolites produced by microbial mats that thrived in a fresh-water hydrothermal field (2).

Pearce et al. (1) incorporated the adenine content of carbonaceous meteorites as one of the parameters and used the lunar cratering record to estimate the rate of deposition from meteorites between 4.5 and 3.7 billion y ago. They also assumed a certain area and depth of a typical WLP in which organic material would accumulate, and took into account the rate at which the ponds would go through wet–dry cycles related to precipitation and evaporation. Such cycles would be necessary to concentrate reactants and provide chemical energy required for polymerization of RNA. Finally, Pearce et al. estimated loss of adenine from ponds by seepage and degradation by UV light.

Perhaps most challenging is Pearce et al.’s (1) choice of WLPs rather than hydrothermal vents. The ponds were optimized in terms of an area that permits sufficient collection of organic material, but also of a depth that could undergo periodic cycles of evaporation and filling by precipitation. Fig. 1A shows a “black smoker” emitting a plume of iron-rich mineral particles (3). Another type of vent discovered later are the alkaline vents shown in Fig. 1B (4), and these have been the subject of a series of publications by Russell and colleagues (5–8), who proposed that such vents are plausible sites for life to originate. Fig. 1C shows a hydrothermal field on Mount Lassen, California, with an enlarged view of a small WLP.

Fig. 1.

Hydrothermal vents and WLP. There are two distinct types of hydrothermal vents. So-called “black smokers” (A) are acidic and driven by heat from underlying magma. Alkaline vents (B) are produced by a chemical reaction called serpentinization, when sea water reacts with certain minerals in olivine. Fresh-water hydrothermal fields (C) are generally acidic due to dissolved sulfur oxides and are analogous to the WLP analyzed by the Pearce et al. (1). Images courtesy of (A) Office of Ocean and Atmospheric Research/National Undersea Research Program/National Oceanic and Atmospheric Administration; and (B) Wikipedia Commons/National Science Foundation (University of Washington/Woods Hole Oceanographic Institution).

What Pearce et al. (1) propose is that an impacting carbonaceous meteorite would produce smaller fragments that fall into ponds and release soluble organic compounds, such as adenine. Something like this occurred in 1969 when a boulder-sized bolide exploded in the skies over Murchison, Australia. Hundreds of fragments fell over an area of 5 square miles and ∼100 kg were quickly collected. Carbonaceous meteorites are not rock-like but instead are composed of loosely adhering microscopic mineral grains that quickly fall apart when exposed to water and release organic compounds into solution. The Murchison meteorite fragments have been extensively investigated and contain ∼1 parts per million of adenine, along with a variety of amino acids and carboxylic acids (9).

It is obvious that similar wet–dry cycles cannot occur in the neighborhood of hydrothermal vents. Instead, organic compounds delivered by meteorites into the ocean would simply dissolve and be diluted to such low concentrations that they are unable to react. Furthermore, life uses condensation reactions to form the ester and peptide bonds that are ubiquitous in biopolymers, nucleic acids and proteins. Condensation reactions are not spontaneous in aqueous solutions, but instead require a source of chemical energy. Even if organic compounds could be synthesized in situ in hydrothermal vents, as envisaged by proponents, they are in constant contact with sea water, which means that condensation reactions relevant to the origin of life have a substantial thermodynamic hurdle to overcome. This is why Pearce et al. (1) chose to model small pools undergoing evaporation, so that solutes become sufficiently concentrated for polymerization to occur.

Plugging all of these values into a set of rate equations, Pearce et al. (1) reach some surprising conclusions. Most startling is that RNA-like polymers would need to be synthesized in just a few wet–dry cycles rather than many millions of years. Based on the estimated rates of meteoritic infall, the authors also calculate that most polymer synthesis would necessarily be underway before 4.17 billion y ago.

How skeptical should we be of these conclusions? Sherlock Holmes, in A Study in Scarlet, gave some pertinent advice to Dr. Watson: “How often have I said to you that once you eliminate the impossible, whatever remains, no matter how improbable, must be the truth?” (10). Can any of the Pearce et al.’s (1) assumptions be eliminated as impossible? Research on the origin of life does not quite work that way. Sherlock Holmes believed in “yes” and “no” answers, but scientists instead use experiments and observations to decide whether certain hypotheses are more or less plausible than others. Research on the origin of life is unusual in that Hadean conditions have relatively few constraints. The main consensus among researchers is that liquid water was essential for life to begin, and the prebiotic atmosphere lacked abundant molecular oxygen. There also must have been a source of organic compounds related to biological processes, such as the extraterrestrial infall proposed by Pearce et al. (1) and analyzed in an earlier publication by Chyba and Sagan (11).

There are a few gaps in Pearce et al.’s (1) argument. For example, they assume that it is a simple matter to synthesize nucleotides from nucleobases. Although Powner et al. (12) demonstrated a laboratory synthesis of cytosine monophosphate and potential precursors of purines, there is still no plausible reaction that could produce all four nucleoside monophosphates in a WLP setting. Pearce et al. (1) also assume that if nucleoside monophosphates could somehow be synthesized, they readily form polymers using chemical potential

Pearce et al. (1) have made a bold and challenging attempt to provide a quantitative estimate for the accumulation of nucleobases, like adenine, on the Hadean Earth some 4 billion y ago, before life began.

available in wet–dry cycles. Here the authors quote results from our laboratory (13, 14), but we have not yet demonstrated that polymerization can occur under natural conditions.

To summarize, Pearce et al. (1) have made an imaginative attempt to differentiate between WLP and the ocean in terms of plausible conditions that would be conducive to the origin of life. Some researchers will find their argument to be thought-provoking, while others will consider the number of assumptions involved and will be tempted to dismiss the results as mere speculation. My impression is that Pearce et al. make every effort to base their calculations on facts and logic. They are venturing into a huge gap in our understanding of the origin of life, and the first attempt to fill such a gap will stand until others can eliminate one or more of the underlying assumptions by demonstrating impossibility, or at least by proposing a more plausible narrative. Pearce et al. have thrown down the gauntlet. Perhaps the most testable claim is that the RNA world began in the fresh water of a hydrothermal pond rather than in salty sea water. There is experimental evidence that RNA-like polymers can be synthesized in cycling fresh-water conditions, so the proponents of hydrothermal vents must show by experiment that RNA can also be synthesized in the hot, salty seawater.