Chemical Evolution II - American Chemical Society

Chapter 4

Downloaded by UNIV OF GUELPH LIBRARY on June 28, 2012 | http://pubs.acs.org Publication Date (Web): December 20, 2009 | doi: 10.1021/bk-2009-1025.ch004

Energetics of Biomolecule Synthesis on Early Earth Jan P. Amend1 and Tom M. McCollom2 1

Department of Earth and Planetary Sciences, Campus Box 1169, Washington University, St. Louis, MO 63130, USA 2 Laboratory for Atmospheric and Space Physics, Campus Box 392, University of Colorado, Boulder, CO 80309-0392, USA

Among the most plausible environments for the origin of life are marine hydrothermal systems, where geochemical energy sources and refugia from sterilizing meteorite impacts would have been plentiful. Here, values of Gibbs energy were calculated for the formation of individual cellular building blocks from inorganic reactants. In our model, corresponding redox reactions occurred at the interface between two endmember fluids─low temperature (25 °C), mildly acidic (pH 6.5), relatively oxidized (Eh -0.30 mV) seawater and moderately hot (140 °C), alkaline (pH 9), reduced (Eh -0.71 mV) hydrothermal vent fluid. The thermodynamic calculations demonstrate that biomass synthesis is most favorable at moderate temperatures, where the energy contributions from HCO3- and H+ in seawater coupled to the reducing power in hydrothermal fluid are optimized. The models further show that the net synthesis of cellular building blocks may yield small amounts of energy over the ranges of temperature and chemical composition investigated. This is counter to conventional wisdom for anabolic processes and lends further support to marine hydrothermal systems as particularly favorable sites for the emergence of life.

© 2009 American Chemical Society In Chemical Evolution II: From the Origins of Life to Modern Society; Zaikowski, L., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2009.

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Background There is accumulating evidence that life emerged on Earth during the late Hadean era (~4.2-3.8 Ga), and that microorganisms thrived by the early Archean era (3.8-3.4 Ga). In one study, isotopically light carbonaceous inclusions in phosphate mineral (apatite) grains from ~3.8 Ga sediments in West Greenland were interpreted as robust evidence of biological activity (1). Carbon isotopes were also used as a biosignature of planktonic organisms in slightly younger (~3.7 Ga) pelagic sediments from Greenland (2). These data further suggested that oxygenic photosynthesis had evolved by this time, a conclusion which is vigorously debated. In still younger rocks, the ~3.5 Ga Apex chert in the Warrawoona Group of Western Australia, putative microfossils were interpreted as oxygen-producing cyanobacteria (3, 4). However, in a reinterpretation of these cherts, the microfossil-like structures were labelled as artifacts from amorphous graphite (5), and it was shown that Raman spectroscopy, the analytical tool used by Schopf and co-workers, cannot unambiguously identify biogenicity (6). Although organic biomarkers, ancient soils, and stromatolites provide strong evidence for the advent of oxygenic photosynthesis by ~2.5-2.7 Ga, these interpretations also are not entirely without controversy (7-10). Regardless of when oxygenic photosynthesis evolved, it is widely accepted that it was preceded by its anoxygenic counterpart. Evidence for this comes from analyses of numerous photosynthesis genes and whole genomes of all five recognized groups of photosynthetic bacteria─cyanobacteria, purple bacteria, green sulfur bacteria, green non-sulfur bacteria, and heliobacteria (11-13). In addition, two geochemical studies suggest that H2-based carbon fixation via anoxygenic photosynthesis occurred in microbial mats that are preserved in the ~3.4 Ga Buck Reef Chert, South Africa (14, 15). There, the evidence includes the presence and absence of certain trace minerals (e.g., iron-carbonates and iron-oxides), and specific rare earth element patterns, which imply an anoxic water column despite the apparent presence of phototrophs. Predating both oxygenic and anoxygenic phototrophy appears to be chemotrophy, and in particular, chemolithoautotrophy (in this metabolic process, organisms utilize inorganic energy sources, in part, to synthesize their own biomass from CO2 and other inorganic carbon sources). As noted by Martin and Russell (16), Mereschkowsky (17) was the first to argue that the earliest organisms were anaerobic and autotrophic, with the ability to synthesize carbohydrates without the aid of chlorophyll. A chemolithoautrophic origin of life is now supported by biochemical, geochemical, and phylogenetic evidence. For example, Martin and Russell (16) and Russell and Hall (18) built on a study by Fuchs (19) to argue for an ancient CO2-fixation pathway, perhaps similar to the acetyl-CoA (Wood-Ljungdahl) pathway. Support comes from this pathway’s occurrence in anaerobic and thermophilic bacteria and archaea, its low energy requirements, and the positions of acetogens and methanogens deep in the tree of life. Geochemical considerations favor chemolithoautotrophy, especially in hydrothermal systems, on energetic grounds. Numerous studies calculated the thermodynamic drive for abiotic organic synthesis and the energy yields from chemolithotrophy (20-26). Phylogenetic arguments include those of Pace (27, 28), who constructed a global tree of life from which he concluded

In Chemical Evolution II: From the Origins of Life to Modern Society; Zaikowski, L., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2009.


65 that the last common ancestor, and by inference the earliest organism, was chemotrophic, autotrophic, and thermophilic. This is the most parsimonious interpretation of the organisms that occupy the deepest and shortest branches in the archaea and bacteria domains. The majority of subsequent investigations have confirmed or complemented these views, concluding consequently that organoheterotrophy—the reliance on organic compounds as energy and carbon sources—evolved after lithoautotrophy. Ever since their discovery, marine hydrothermal systems have been put forth as possible environments for the origin of (thermophilic) life (29-33). In addition to the phylogenetic and thermodynamic inferences mentioned above, support for this theory also comes from planetary arguments. Until ~3.8 Ga, the Earth was subject to heavy bombardment by massive meteorites that could have sterilized all near-surface environments. It has been proposed that deep-sea hydrothermal systems could have served as refugia for the survival and evolution of early life (34-36). It perhaps should be noted, however, that some researchers continue to argue against hydrothermal system theories and prefer the primordial ocean as the spring of life, with heterotrophy as the first metabolic strategy (37). Nevertheless, based on the abundance of evidence from numerous and disparate sources, we adopt as most likely that the first organism was a chemolithoautotroph, and that its niche was a marine hydrothermal system. The focus then shifts to describing the physicochemical properties of that system. Because metabolic processes are primarily electron transfer processes, redox disequilibria must have existed in such a system to facilitate the transition from a sterile, prebiotic world to one inhabited by single-celled life forms. A reaction zone can be envisioned where hot, chemically reduced, perhaps slightly alkaline hydrothermal fluids mixed with cooler, more oxidized, arguably acidic seawater to generate a redox front (18). It is at such an interface that inorganic compounds may have reacted to form simple organic molecules, which then polymerized and ultimately led to something that resembled a compartmentalized cell and the origin of life. In an effort to better understand potential metabolic reactions in such an environment, we calculate the Gibbs energy of reaction (ΔGr) for the synthesis of individual molecular building blocks (amino acids, nucleotides, fatty acids, saccharides, amines) that constitute prokaryotic biomass. The reactants are inorganic compounds, and the energetics apply to a hydrothermal solution with seawater and vent fluid end-members.

Mixing of Seawater and Vent Fluid Rapid mixing of two chemically distinct fluids yields a solution that is, at least temporarily, out of thermodynamic equilibrium. Here, we propose the formation of a hydrothermal solution that is the product of late Hadean vent fluid mixing into late Hadean seawater. In this mixed solution, disequilibria among redox sensitive compounds represent an energetic drive for the abiotic synthesis of organic compounds. Similar mixing scenarios have been used effectively to model the energetic yields of chemolithotrophic metabolisms on Earth (21), Mars (38, 39), and Jupiter’s moon Europa (40), and to evaluate the


66 energetics of organic synthesis (23, 41), including amino acids (22, 42). The models first require that the compositions of the two end-member fluids be defined.


Composition of Late Hadean Seawater Defining a representative composition for the ocean end-member in the models is particularly challenging because nearly every aspect of the physical and chemical state of the coupled ocean/atmosphere system on the early Earth (temperature, pH, elemental composition, salinity, oxidation state, etc.) is poorly understood at present and continues to generate vigorous debate. We adopt an ocean composition that appears consistent with the currently available constraints. The composition of the model late Hadean seawater used in this communication is given in Table I. There appears to be a general consensus that the atmosphere prior to the advent of life was mildly reducing, dominated by N2 and CO2, with minor amounts of reduced gases such as H2 and CH4, and very little or no O2 (43, 44). However, the actual abundances of these components in the early atmosphere, and consequently in the early ocean, remain uncertain. Russell and colleagues have advocated a moderately acidic early ocean, with the acidity attributable to the formation of carbonic acid in equilibrium with an atmosphere containing 110 bar CO2 (18). Elevated CO2 has also been suggested as a means of providing greenhouse warming to counter the faint young sun (43, 45). However, geologic observations and early atmosphere models suggest that several bars of CO2 might not have been tenable given geologic constraints (7). Methane (CH4) also has been suggested as an alternative to CO2 as a key greenhouse gas for the early Earth (46, 47), but perhaps a CO2-enriched atmosphere gave way to a CH4enriched atmosphere only after the onset of biological methanogenesis (44). For this study, we adopt a late Hadean ocean in equilibrium with an atmosphere that contains elevated, but not extreme, levels of CO2 (0.2 bar). This leads to a mildly acidic ocean with pH equal to 6.5.


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Table I. Compositions of End-Member Fluids Used in the Mixing Calculations T (°C) pH Eh (mV) H2(aq) ΣCO2 O2(aq) Na Cl Ca Mg Fe K CH4(aq) ΣH2S SO42SiO2(aq)

Seawater 25 6.5 -0.30 0.00054 22.7 10-9 464. 540. 14.2 31.1 0.12 0.1 0. 0.0002 0.1 0.11

Hydrothermal Fluid 140 9.0 -0.71 16. 0.01 0. 607. 650. 20. 0.001 0. 10. 2.0 0.1 0. 0.005

NOTE: All concentrations in mmol kg-1.

It has been argued, largely on the basis of oxygen isotopes, that the Archean ocean had temperatures substantially elevated relative to the modern ocean (i.e., 45-70ºC) (48, 49). Conversely, others have argued that such elevated temperatures may not be consistent with the geologic evidence, and that the isotopic observations can be accounted for by other explanations (47). In the absence of more definitive constraints, we adopt a conservative temperature of 25 ºC. Further, late Hadean seawater is taken here to have had concentrations of dissolved Na and Cl similar to modern seawater, and concentrations of Ca, Mg, and Fe set by saturation with respect to the common minerals calcite (CaCO3), magnesite (MgCO3), and siderite (FeCO3), respectively. Similarly, aqueous SiO2 and H2S are set by saturation with respect to quartz (SiO2) and pyrite (FeS2), respectively. Tian et al. (50) recently suggested that the H2 level in the early atmosphere was 0.1 bar or higher, but Catling and Claire (44) argue that an atmospheric mixing ratio on the order of 10-3 was more likely. Accordingly, our model sets the early ocean in equilibrium with 0.001 bar of atmospheric H2, leading to an aqueous concentration of 0.54 μmol kg-1. We further assume that equilibrium with dissolved H2 controls the oxidation state of dissolved Fe. Sulfur isotope signatures from the early Earth constrain O2 levels to below 10-5 bar (51), but because the precise level is unknown, we assumed a dissolved concentration of 10-12 mol kg-1. Sulfate levels in the early ocean were apparently

Chemical Evolution II - American Chemical Society

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