Implications for TAA and MTA in Prebiotic Chemistry

Modern submarine HT systems are diverse, displaying extreme variability in the composition of their effluent depending on their host mineralogies and hydrodynamics, which have been studied extensively (Table 2 and references provided therein). Effluents range in temperature from several hundred degrees C to the temperature of ambient seawater (~2 °C) and in pH from ~2 to >10 12.

Table 2 Measured physical parameters and concentrations of species relevant to this discussion in various marine HT vents and modern bulk seawater. aRefs 43,45; bRefs 84, 85, 86; cRef. 87, dRefs 39,88, eRef. 59, fRef. 45, −.= not determined, bd = below detection limit as reported. Full size table

A variety of low molecular weight organic species have been detected in HT vent effluents39,40, including various hydrocarbons, as well as variable amounts of formic acid (Table 2). Formic acid may be derived from the hydration of CO41, which can itself can be derived from the water-gas shift reaction of CO 2 and H 2 , both of which are abundant in some HT settings (Table 2)41.

At least some of the simple organics detected in modern vent effluents are generally agreed to have an abiotic origin based on their isotope systematics, though it is also acknowledged that this signal can be difficult to discern for other organics42,43. Still other organics have been convincingly determined to be of biological origin. For example, the isomer distribution of amino acids detected in several HT vent fluids from the Izu-Bonin Arc strongly suggests a biological origin44.

Despite laboratory experiments demonstrating the production of MTA from CO and CH 3 SH25, evaluation of modern HT vent effluents has not provided evidence for abiotically derived CH 3 SH45 or acetate39. CH 3 OH, the hydroxy analogue of CH 3 SH, does not appear to be a stable form of carbon under most HT vent conditions, being at best a transient intermediate in the inter-conversion between CO and CH 4 15. Thus the reaction of aqueous H 2 S and CH 3 OH is likely not a major contributor to environmentally measured CH 3 SH concentrations.

Sulfide concentrations in vent fluids are likely governed by concentrations of soluble metal species such as Ni and Fe, among others46. For example the K sp values at 25 °C for FeS and NiS are 4.9 × 10−18 and 3 × 10−21 respectively47, with these values shifting as a function of temperature and pH. Though concentrations of sulfide (Σsulfide = H 2 S + SH− + S2−) can be significant in high temperature fluids, these are precipitated rapidly upon cooling due to the formation of metal sulfides48. Thus Σsulfide speciation in modern HT systems has been measured variably between ~0 and a maximum near 20 mM (Table 2). In off-axis serpentinizing vent systems such as Lost City, sulfide concentrations are typically much lower, often less than 1 mM (Table 2) and the majority of S is often found in the form of sulfate, despite the fact that these vents often discharge considerable amounts of dissolved H 2 45.

With regard to the propensity of HT vent chemistry to produce organics beyond the simple hydrocarbons which may be produced in trace amounts in such systems43, it is worth noting that HT systems chemistry may be self-regulating in many respects. High H 2 systems, which may contain large amounts of CH 4 , may inherently limit the production of higher hydrocarbons due to equilibria such as those obtained in Equation 349.

The estimated ΔrG′° for this reaction is −68.9 ± 14.2 kJ mol−1 50, giving K eq values of ~1.2 × 1012, 4.4 × 109 and 4.0 × 107 at 25, 100 and 200 °C, respectively.

Likewise, high CO 2 /reduced Fe systems are limited in their ability to supply H 2 or reduced C (including CO, which appears to be the active species for Fischer Tropsch Type synthesis)16 due to the precipitation of siderite (FeCO 3 )51. Thus, fluids with high dissolved inorganic carbon limit the ability of Fe2+ to serve as a reducing agent, even though high concentrations of C species might allow for escape from the kinetic limitations of forming higher C-species.

If the upper mantle had already largely reached its modern oxidation state by 4.35 Ga, as appears to be true from recent measurements of rare earth elements in zircons52 then modern HT vent chemistry is likely similar to what one could expect for early Earth geochemistry12,53, though the composition of bulk seawater may have been markedly different. The heat flux on the primitive Earth was likely somewhat higher, making mean oceanic circulation times through seafloor HT vent systems on the whole shorter54, nevertheless the residence times of fluids at high temperatures would still be on average long enough to ensure equilibration of seawater with host mineralogies. There is little evidence that mantle-derived rocks have ever contained markedly higher C or S concentrations55,56, though there have been significant changes in bulk ocean water composition over time57. pH and Fe, C and S species concentrations in the oceans between 3.5 Ga and 4.4 Ga are poorly constrained due the lack of corroborating geological evidence.

Nevertheless, high- and low-end estimates for the concentrations of some species can be broadly constrained. Sulfide concentrations in the bulk Archaen ocean (~4-2.5 Ga) have been suggested to have been in the low mM range48, which is similar to concentrations observed in modern HT vent fluids (Table 2).

For the sake of subsequent calculations, we will assume a generous 20 mM sulfide concentration for vent fluid or the bulk ocean, acknowledging that this value may be overestimated by orders of magnitude depending on the exact geochemical setting under consideration. Due to metal sulfide solubility product constraints, these values are unlikely to be underestimated in any environment.

Equilibrium TAA concentrations would be limited by H 2 S concentrations, MTA concentrations similarly by CH 3 SH concentrations. Except under strongly acidic conditions, TAA is generally more stable than MTA, but TAA is undoubtedly more plausible simply due to the likely much higher abundance of H 2 S, which is more abundant than CH 3 SH in modern HT vent fluids by a factor of 1000 or more (Table 2). It is difficult to envision a geochemical setting in which H 2 S concentrations are lower than CH 3 SH concentrations, due to the equilibria involved in making CH 3 SH in the first place58.

Figure 4 shows estimates for maximal equilibrium concentrations of TAA in various HT settings, as a function of possible ΣH 2 S and Σacetate concentrations and using the K eq values for TAA formation derived from the calculated free energy values in Table 1. Much of the area shown in this figure represents parameter combinations which are unlikely to be attainable in natural HT systems. Measured concentrations (Table 2) of acetate and H 2 S in fluids from Lost City39 and hydrothermally altered biologically organic-enriched sediments from Guaymas basin59 would yield TAA concentrations of 1.4 × 10−49 and 2.1 × 10−11 M, respectively. These rough equilibrium calculations do not take into account potential competing side reactions (which could only lower these values) and mineral or other types of catalysis (which in principle would only speed the time to equilibration), nevertheless the equilibria cannot be high due to the factors discussed above.

Given the second order rate and yield dependencies of condensation reactions, which typically decline inversely as a function of reactant concentrations, these concentrations are very low for the sake of performing more complex organic chemistry in HT environments. In our study, even examining the behavior of TAA or MTA concentrated far beyond what is plausible in natural marine environments, we note that only the predicted hydrolysis products are observed by NMR.

Huber and Wächtershäuser25 reported ~0.5% acetate yields based on input CH 3 SH (8 mM) in the presence of 350 mM CO. This is ~500 times and ~3700 times the highest CH 3 SH and CO concentrations respectively measured to date in a natural vent fluid45. All isotopic measurements to date suggest that acetate detected in HT vent fluids is derived from biological material39 despite being predicted to form abiotically under HT conditions13.

Reduced carbon species in modern HT vent fluids have not been measured outside of the mM range (Table 2) and it is clear that in some cases, for example the Guaymas Basin, high organic contents are due to the liberation of biological material from sediments59. These fluids contain the highest concentrations of acetate measured in submarine HT fluids to date, but acetate is a common component of naturally cracked petroleum60.

The redox equilibrium between H 2 released by serpentinization reactions and one-C species can be constrained. C-C bond forming reactions are most kinetically favorable from formate/CO and as would be expected the equilibrium between CO and formate, a simple hydration, is obtained rapidly, while that between CO 2 and CH 4 is not15. Thus CO (or its hydrate) is likely the limiting reagent for higher hydrocarbon formation.

Previous models of HT origins of life have appealed to MTA as opposed to TAA based on experiments by Heinen and Lauwers61 and Huber and Wächtershäuser25 in which CH 3 SH and MTA were prepared from very high concentrations of reagents. Huber and Wächtershäuser’s25 demonstrated synthesis of acetate from CH 3 SH, CO and NiSO 4 or various metal sulfides was proposed to proceed through MTA as an intermediate. However, the conditions of the experiment are of questionable geochemical relevance: for example, 160 mM Na 2 S was employed, which is much higher than that observed in any extant natural system (Table 2).

Concentration processes would be necessary for the prebiotic synthesis of these compounds. Potential concentration mechanisms such as thermophoresis62 deserve much further experimental investigation in this context. This has become a major touchstone of models for the origin of life in HT vent systems12,63, though to date little evidence has been presented which suggests that small molecules such as TAA can be concentrated by several orders of magnitude by this mechanism in geochemical settings.

Dissolved Fe2+ catalyzes TAA hydrolysis, while solid FeS had no effect under the same conditions64. Nevertheless, mineral surface catalysis and catalysis by dissolved organic and/or inorganic species are unlikely to solve these instability problems. TAA and MTA hydrolyze rapidly and their formation equilibria are very low, thus little is gained by achieving equilibrium more rapidly through catalysis and for group transfer from very low concentration transient species the resulting acylates would have to be extremely stable to accumulate.

The effect of pH on the equilibrium constants for TAA derivatives may be attributable to pK a differences between the reacting acid and thiol species, as has been suggested in the case of amide bond formation65. Simply based on the pK a differences between H 2 S (~7.0) and CH 3 SH (~10.4) with acetic acid (~4.8) at 25 °C, one would expect the K eq for TAA to be significantly higher than for MTA, which is concordant with our DFT calculations. For reference the pK a ’s of ethane thiol (~10.6) and butane thiol (~10.5) are fairly close to those reported for CoASH (~9.6–10)33, thus there is no strong reason to think that higher thiols would have significantly different K eq values and the abundances of higher thiols can reasonably be expected to be much lower.

While the pH of vent fluids has probably always been locally controlled, the pH of the prebiotic oceans remains uncertain. The best geochemists have been able to infer is a minimum pH for the oceans, which is on the order of 5–666, though some have argued for a pH closer to neutral67. A full explanation for the pH early oceans must account for buffering systems in addition to carbonate, for example marine clays68 and there is a general need to balance species such as Ca2+ and Mg2+. It is not clear that a high, neutral or low pH environment bulk ocean is necessarily preferable for the origin of life, though in scenarios which invoke TAA or MTA, each has significant consequences.

Acidic oceans do not seem to be preponderant on icy worlds in our solar system where measurement has been possible, for example on Enceladus, as inferred from mass spectrometry of plume ejecta69. The presence of significant amounts of dissolved ammonia has been implicated as necessary to render many icy moons’ subsurface water reservoirs liquid70. The early phases of Mars’ evolution, by most accounts when Mars was most likely to have hosted surface oceans, seem to be consistent with slightly basic to circum-neutral pH, though it appears that subsequent planetary evolution drove Mars’ surface into a more acidic regime71.

It is beyond the scope of this paper to examine every conceivable reaction mechanism which could lead to thioesters in hydrothermal environments. There are other routes by which TAA derivatives could be reasonably abiotically synthesized. For example the sulfhydrolysis of acetonitrile (ACN) with H 2 S to give TAA10. ACN is a product of abiotic atmospheric synthesis from reducing gas mixtures72. The primary intermediate of the reaction of H 2 S with ACN, thioacetamide, is also unlikely to accumulate in most environments, degrading principally to TAA under basic conditions and acetamide under acidic ones73.

The addition of thiols to aldehydes followed by oxidation could also yield thioesters. However, this ignores the problem of thiol concentration already discussed and would require the presence of significant concentrations of aldehydes which are unlikely to be stable to the temperature and redox conditions prevailing in HT environments (see for example Nagai et al.74 and Schulte and Shock75; to our knowledge, there have been no reports to date of significant amounts of abiotic aldehydes in natural submarine HT environments). In any event the products would still suffer from the extreme hydrolytic instability demonstrated here. Such a mechanism may be more favorable in a low-temperature evaporative environment, but seems difficult in the context of a flow-through, elevated temperature marine environment.