Thermodynamic Potential for the Abiotic Synthesis of Adenine, Cytosine, Guanine, Thymine, Uracil, Ribose, and Deoxyribose in Hydrothermal Systems
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The thermodynamic potential for the abiotic synthesis of the five common nucleobases (adenine, cytosine, guanine, thymine, and uracil) and two monosaccharides (ribose and deoxyribose) from formaldehyde and hydrogen cyanide has been quantified under temperature, pressure, and bulk composition conditions that are representative of hydrothermal systems. The activities of the precursor molecules (formaldehyde and hydrogen cyanide) required to evaluate the thermodynamics of biomolecule synthesis were computed using the concentrations of aqueous N2, CO, CO2 and H2 reported in the modern Rainbow hydrothermal system. The concentrations of precursor molecules that can be synthesized are strongly dependent on temperature with larger concentrations prevailing at lower temperatures. Similarly, the thermodynamic drive to synthesize nucleobases, ribose and deoxyribose varies considerably as a function of temperature: all of the biomolecules considered in this study are thermodynamically favored to be synthesized throughout the temperature range from 0°C to between 150°C and 250°C, depending on the biomolecule. Furthermore, activity diagrams have been generated to illustrate that activities in the range of 10−2– 10−6 for nucleobases, ribose and deoxyribose can be in equilibrium with a range of precursor molecule activities at 150°C and 500 bars. The results presented here support the notion that hydrothermal systems could have played a fundamental role in the origin of life, and can be used to plan and constrain experimental investigation of the abiotic synthesis of nucleic-acid related biomolecules.
KeywordsNucleobases Ribose Deoxyribose Hydrothermal systems Thermodynamics
In recent years many theoretical and experimental studies have tested the hypothesis that ancient deep sea hydrothermal systems provided an environment conducive to the abiotic synthesis of biomolecules that are essential for the emergence of life (Bock and Goode 1996; Hazen et al. 2002; Holm 1992; Holm and Andersson 1995, 2005; Holm et al. 2006; McCollom and Seewald 2007; Nisbet and Fowler 1996; Shock 1990, 1992b, 1996; Shock et al. 2000; Simoneit 2004; Woese 1998; Woese et al. 1990). As a result, abiotic synthesis studies involving amino acids (Amend and Shock 1998, 2000; Hennet et al. 1992; Marshall 1994; Shock and Schulte 1990), lipid-like compounds (McCollom et al. 1999; Rushdi and Simoneit 2001), aldehydes (Shock and Schulte 1993), carboxylic acids (McCollom and Seewald 2001, 2003a, b), alcohols, ketones (Shock and Schulte 1995, 1998), polycyclic, alkylated and hydroxylated aromatic hydrocarbons (McCollom 2003; Williams et al. 2005; Zolotov and Shock 1999), thiols (Rushdi and Simoneit 2005; Schulte and Rogers 2004) and other organic compounds (Foustoukos and Seyfried 2004; McCollom and Simoneit 1999; Rushdi and Simoneit 2004; Shock and McKinnon 1993) have been carried out under hydrothermal conditions using experimental and/or computational–thermodynamic techniques. However, the common organic monomers constituting nucleic acids, that is, adenine, cytosine, guanine, cytosine, thymine, uracil, ribose, and deoxyribose, have received far less attention. A notable exception is the recent work carried out by Franiatte and coworkers in which the stability of aqueous adenine was measured at 300°C under controlled fugacities of H2, CO2, and N2 (Franiatte et al. 2008). Exploring potential extraterrestrial sources of nucleobases, Saldino and coworkers have synthesized adenine cytosine, thymine and uracil in one-pot experiments from 0.12 mM formamide (CH3NO) at 160°C in the presence of cosmic dust analogues (amorphous olivines), TiO2 and montmorillonites (Saladino et al. 2003, 2004, 2005b) (for a review of experimental abiotic nucleobase synthesis see Saladino et al. 2005a). Similarly, several other experiments, carried out using high concentrations of precursor molecules, organic solvent extractions and a variety of catalysts under unspecified oxidation states, have produced nucleobases in gas, solid and aqueous phases (Ferris et al. 1968; Hayatsu et al. 1968; Hill and Orgel 2002; Miyakawa et al. 2000; Wakamatsu et al. 1966). But because the conditions under which these experiments were performed do not reflect those of any known current or past hydrothermal systems, their relevance to natural systems is unclear. The purpose of the present study is to explore the thermodynamic potential for the abiotic synthesis of the five common nucleobases (adenine, guanine, cytosine, thymine and uracil) and two sugars (ribose & deoxyribose) that make up nucleic acids (DNA & RNA) from two precursor molecules, formaldehyde (CH2O) and hydrogen cyanide (HCN), over a range of pressures, temperatures, and bulk compositions that are characteristic of hydrothermal systems. This is accomplished by first quantifying the thermodynamic potential to synthesize the precursor molecules from N2, H2, CO2 and CO, and then calculating the energetics of biomolecular synthesis from the two precursor compounds.
The successful experimental synthesis of organic compounds from the condensation of CH2O and HCN, usually referred to as Strecker synthesis, has lead to the hypothesis that reactions involving these precursor molecules were responsible for the abiotic synthesis of biomolecules on the early Earth (Miller 1957; Ferris et al. 1978; Schulte and Shock 1993, 1995). Oró and coworkers were among the first to contribute to this idea by synthesizing adenine, C5H5N5, from HCN (Oró 1960; Oró and Kimball 1961). In addition, it has long been established that carbohydrates of varying carbon number, such as ribose, C5H10O5, can be made abiotically from formaldehyde according to the formose reaction (Butlerov 1861). More recently, Hennet et al. (1992) synthesized several amino acids from CH2O and HCN at 150°C. The prevalence of CH2O and HCN in ancient or modern hydrothermal systems is not known, but the amount of these compounds that could have existed in prebiotic hydrothermal systems can be estimated by taking into account reactions among simple sources of N, C, H and O in these environments that can be relatively well-constrained.
Concentrations of selected species from Rainbow hydrothermal field (Charlou et al. 2002)
Formaldehyde, CH2O, is often cited as a common prebiotic molecule (Orgel 2004; Shapiro 1988), but the concentration of this compound on the early earth is not known. In order to quantify possible concentrations of aqueous CH2O in hydrothermal systems, as with the HCN, equilibrium activities of this species have been calculated using the H2, CO and CO2 concentrations from the Rainbow site (Fig. 1c,d). Although the equilibrium activity of CH2O follows the same qualitative trend with temperature as the activity of HCN shown in Fig. 1a,b, these calculations show that higher pressure (500 bars) favors higher equilibrium activities of CH2O relative to lower pressure conditions (Psat). However, even under the most favorable conditions of low temperatures and high pressure, the equilibrium activity of CH2O, with respect to H2 and CO and CO2, is much less than HCN and 10−5. These results reflect the conditions in one modern hydrothermal system only so if the concentrations of H2, CO and CO2 would have been higher in ancient hydrothermal systems, the activity of CH2O in equilibrium with these reactants could also have been greater. Kasting (1993) estimated that during the first several hundred million years of Earth’s history the atmosphere contained CO + CO2 equal to 10 bars, a result which suggests that the concentration of precursor carbon molecules in hydrothermal systems could have been different from those today.
The equilibrium activities of HCN and CH2O shown in Fig. 1 are used in the following section to calculate the thermodynamic drive for the abiotic synthesis of nucleobases, ribose and deoxyribose.
Nucleobase, Ribose and Deoxyribose Synthesis
In this section, the thermodynamic drive to synthesize the five common nucleobases, ribose and deoxyribose is quantified by calculating the Gibbs energy of reaction for each of these compounds from the precursor molecules HCN and CH2O as a function of temperature and temperature.
The nucleobases considered in this study are the common purines (adenine and guanine) and pyrimidines (cytosine, thymine, and uracil) found in DNA and RNA. Experimental attempts to synthesize these compounds abiotically have been less successful than for amino acids, especially guanine and uracil (Saladino et al. 2005a).
Ribose and Deoxyribose
The feasibility of Reaction 16 representing a likely pathway for the abiotic synthesis of ribose has been doubted (Shapiro 1988, 1995). However, due to recent progress in determining the chemical environments that promote the abiotic synthesis of ribose (Orgel 2004; Ferris 2005; Holm et al. 2006), the likelihood that Reaction 16 represents a plausible origin of this fundamental sugar has been substantiated. Initially, a number of studies showed that, under undiscriminating laboratory conditions, the formose reaction produces dozens of aldoses, ketoses, and sugar alcohols from CH2O, i.e., very little ribose (Shapiro 1988). However, it has recently been found that in the presence of Pb2+, aldopentoses are preferentially formed during the formose reaction and some of these reaction products are isomerized to ribose (Zubay 1998; Zubay and Mui 2001). Also, Ricardo et al. (2004) showed that borate minerals preferentially bind pentoses, ribose most so, thus stabilizing and potentially concentrating them over other pentoses. Furthermore, when phosphate is present, ribose-phosphate compounds, the repetitive-unit backbone of RNA, are formed and do not readily convert into other molecules (Müller et al. 1990).
Variable CH2O and HCN Activities
Because the concentrations of N2, H2, CO, and CO2 used to calculate the activities of CH2O and HCN in this study are highly variable in modern systems (Von Damm 1995) and, likely, ancient hydrothermal systems, the activities of the precursor molecules produced in them may have also been quite variable. In order to quantitatively assess the impact that variable precursor molecule concentrations would have on the production of nucleobases, ribose and deoxyribose, the activities of these species in equilibrium with varying activities of CH2O and HCN and, where relevant, H2 and O2, were calculated under temperature and pressure conditions that favor their formation.
Thermodynamic calculations have revealed that adenine, guanine, cytosine, thymine, uracil, ribose, and deoxyribose can be synthesized from the precursor molecules CH2O and HCN under temperatures, pressures, and fluid compositions that are characteristic of hydrothermal systems. However, nucleobase and sugar synthesis is thermodynamically favored only at the lower end of the temperature range considered here. This finding corroborates previous studies which have suggested that organic synthesis in submarine hydrothermal systems most likely did not occur in black smoker vent sites where the temperatures can exceed 400°C, but more plausibly on the distal, off-axis, portions of hydrothermal systems where the temperature is lower (Shock 1990, 1992a, b). Greater activities of the precursor molecules, CH2O and HCN, can co-exist in equilibrium with CO, CO2, H2, and N2 as measured in modern hydrothermal systems at cooler temperatures. Activities of HCN corresponding to concentrations in the millimolar range have been calculated to exist at the lower end of the temperature spectrum considered in this study regardless of whether it was generated from CO or CO2. However, the concentrations of CO, CO2, H2, and N2 from a modern hydrothermal system may not be representative of past geologic conditions. If the concentrations of these building block molecules would be higher, as hypothesized for the early-Earth atmosphere (Kasting 1993), then higher activities of CH2O and HCN could then coexist in equilibrium with CO, CO2, H2, and N2. It follows that the synthetic potential for the nucleobases, ribose and deoxyribose would also be greater than what is reported in the present study. Therefore, we have explored the range of CH2O and HCN activities on the equilibrium activities of nucleobase, ribose, and deoxyribose at what can be considered one particular hydrothermal flank condition (150°C and 500 bars). Under these conditions, activities of all of the biomolecules considered here are in equilibrium with the precursor molecules at concentrations comparable to those in modern living organisms (Voet et al. 1999).
Complementing other studies that have shown that various biological and organic molecules such as amino acids (Amend and Shock 2000), carboxylic acids, alcohols, and ketones (Shock and Schulte 1998) can be synthesized in hydrothermal systems, the results of this study support the hypothesis that hydrothermal systems could have served as efficient anabolic reactors for building the molecules that are essential to living organisms. The thermodynamic calculations shown here also provide constraints on the temperature, pressure and bulk composition necessary for the synthesis of these fundamental biomolecules in hydrothermal systems. Our results provide a useful theoretical framework for the design of experiments aimed at synthesizing nucleobases and sugars from inorganic precursors.
This work is supported by the Netherlands Organization for Scientific Research (NWO) grant number 815.01.008.
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