Early Vents as Electrochemical Reactors

Russell and colleagues (Russell et al. 1988, 1989, 1993, 1994; Russell and Hall 1997) predicted the existence and properties of deep-ocean alkaline hydrothermal systems more than a decade before their discovery, pointing out their suitability as natural electrochemical reactors capable of driving the origin of life. While fossil vent systems had been reported in Ireland (Boyce et al. 1983), the discovery of the first active submarine system, Lost City hydrothermal field (Kelley et al. 2001, 2005), was remarkable in that its properties corresponded almost exactly to those postulated by Russell et al. (1993). Lost City is powered by a process called serpentinization, the exothermic reaction of ultramafic minerals from the upper mantle, in particular olivine, with water (Bach et al. 2006; Sleep et al. 2004; Martin et al. 2008; Russell et al. 2010). This reaction produces large volumes of H 2 (the presence of the mineral awaruite in some serpentinizing systems indicating as much as 200 mM (McCollom and Bach 2009) dissolved in warm (45–90 °C) alkaline (pH 9–11) fluids containing magnesium hydroxides (Kelley et al. 2001, 2005). Alkaline vents do not form chimneys, as in black smokers (and indeed do not normally ‘smoke’ at all) but rather are labyrinthine networks of interconnected micropores bounded by thin inorganic walls, through which hydrothermal fluids (and ocean waters) percolate.

Such vents should have been more common on the early Earth, as the mantle was less differentiated from the crust, hence ultramafic minerals could have been found across much of the ocean floor (Fyfe 1994; Jaffrés et al. 2007; Shields and Kasting 2007). In contrast, ultramafic minerals are mostly exposed close to the mid-ocean spreading centres today (Schrenk et al. 2013). Alkaline vents are highly stable geological systems; Lost City is estimated to be about 100,000-years old (Ludwig et al. 2005), which as noted by Russell, is 1017 microseconds, a time unit more consonant with chemistry. That gives plenty of time for abiotic chemistry to develop, especially if early vents were indeed contiguous across the ocean floor (Sleep 2010; Shields and Kasting 2007). Moreover, the fact that olivine and water are both abundant in space (de Leeuw et al. 2010), and so presumably on all wet, rocky Earth-like planets, implies that equivalent conditions could be projected to occur on as many as 40 billion exoplanets in the Milky Way alone (Lane 2015).

Lost City is composed of carbonate minerals, mostly aragonite, and magnesium hydroxide, brucite, (Kelley et al. 2001, 2005) but this is unlikely to represent the composition of ancient vents. That difference is critical and relates not to serpentinization as a process (which should have been the same), but to ocean chemistry in the Hadean and Archaean, around 4 billion years ago (Pinti 2005). There were two critical differences: oxygen was absent (Bekker et al. 2004; Kasting 2013); and the CO 2 concentration in the oceans was substantially higher (although there is little consensus on how much higher; see Russell and Arndt 2005; Sleep 2010; Arndt and Nisbet 2012). Anoxia is necessary for both thermodynamic and kinetic reasons. Thermodynamic, because the reaction between H 2 and CO 2 is only favoured under anoxic conditions (Amend et al. 2013); and kinetic, because the solubility of catalytic transition metals, notably Fe2+ and Ni2+ is much greater when oceans are anoxic (Russell and Arndt 2005; Arndt and Nisbet 2012). That the Hadean oceans were indeed replete in Fe2+ and Ni2+ (derived from volcanic systems such as black smokers) are indicated by the precipitation of vast banded-iron formations throughout the Archaean (Anbar and Holland 1992; Zahnle et al. 2007). The great availability of transition metals (along with bisulphide ions within alkaline vents; Nitschke and Russell 2009) must have resulted in the precipitation of catalytic Fe(Ni)S minerals such as mackinawite and greigite in the walls of the vents themselves; but equivalent catalytic Fe(Ni)S minerals are not found in modern vents. In early vents then, H 2 -rich hydrothermal fluids must have percolated through labyrinths of micropores bounded by thin inorganic walls containing catalytic Fe(Ni)S minerals (Nitschke and Russell 2009; Lane and Martin 2012).

The higher CO 2 concentration in Hadean oceans should have increased carbon availability (modern alkaline hydrothermal vents are often carbon limited, from carbonate precipitation and removal by living cells; Proskurowski et al. 2008; Bradley et al. 2009) and lowered the pH of the oceans, probably to around pH 5–7 (Arndt and Nisbet 2012). That could have produced pH gradients of 5 or 6 pH units between the alkaline hydrothermal fluids and acidic oceans. While mixing could prevent such steep gradients being juxtaposed across single barriers, laminar flow in elongated hydrothermal pores does make it feasible for sharp gradients of several pH units to exist across distances of a few micrometres.

The Driving Force for Organic Synthesis

Steep natural proton gradients across thin catalytic Fe(Ni)S barriers could theoretically promote organic synthesis by lowering the energetic barrier to CO 2 reduction (Lane 2014; Yamaguchi et al. 2014). Amend and McCollom (2009) calculated that anoxic alkaline hydrothermal conditions (between 25 and 125 °C) are thermodynamically conducive to the synthesis of total cell biomass (i.e. amino acids, fatty acids, carbohydrates, nucleotides) from H 2 and CO 2 . Nonetheless, experimental attempts to drive the reaction of H 2 and CO 2 using Fe(Ni)S catalysts have proved unsuccessful, even at high pressures (Shock and Canovas 2010), as the reduction potential of the H 2 /2H+ couple is not sufficiently low to reduce CO 2 to CO, formate (HCOO−), formaldehyde (HCHO) or similar organics with equivalent reduction potentials (Lane 2014; Lane and Martin 2012).

A clue might lie in the strict dependence of methanogens and acetogens on proton gradients to drive CO 2 reduction (Buckel and Thauer 2013). In methanogens, the membrane-integral energy converting hydrogenase (Ech) uses the proton-motive force to reduce ferredoxin directly, which in turn reduces CO 2 , ultimately to a methyl group (Buckel and Thauer 2013). Ech could conceivably utilise proton gradients to modulate pH within the active site of the enzyme, thereby altering the reduction potential locally. Whenever protons are involved in a reduction, the reduction potential depends on pH, falling by ~59 mV per pH unit rise, according to the Nernst equation (Nicholls and Ferguson 2013). Such pH dependence is true of both H 2 and CO 2 , hence at any particular pH, the reduction remains equally difficult (Fig. 1a). However, in alkaline vents, H 2 is dissolved in hydrothermal fluids at pH 10, whereas CO 2 is dissolved in ocean waters at pH 6. This sharp difference should modulate both reduction potentials sufficiently to drive the reduction of CO 2 with H 2 . If fluids of pH 6 and 10 are juxtaposed across a thin semi-conducting Fe(Ni)S barrier, it should be possible in principle to reduce CO 2 to CO, HCOO− and even HCHO (Fig. 1b).

Fig. 1 a Standard reduction potentials of H 2 and CO 2 at pH 7. Transfer of electrons from H 2 to CO 2 is unfavourable as the reduction potential for CO 2 at this pH is lower (more negative) than H 2 . b With H 2 dissolved in waters at pH 10 and dissolved CO 2 in waters at pH 6 however, the reduction potential for CO 2 becomes higher (more positive) than that of H 2 making the reduction of CO 2 favourable. This would theoretically allow for the reduction of CO 2 to form organic compounds such as formate, formaldehyde, methanol and methane. c How acid and alkaline fluids could interact inside hydrothermal vents across thin semi-conducting Fe(Ni)S walls, leading to the reduction of CO 2 to formaldehyde via formate Full size image

Once the energetic barrier to CO 2 reduction has been overcome, the ensuing steps of the acetyl CoA pathway are exergonic, and in methanogens and acetogens drive carbon and energy metabolism via acetyl CoA and ATP, respectively (Fuchs 2011). An abiotic equivalent of this pathway could arguably generate the reactive thioester methyl thioacetate, a simple analogue of acetyl CoA, which has been synthesised from CO and CH 3 SH by Huber and Wäctershäuser (1997) using Fe(Ni)S catalysts. In modern cells, acetyl CoA can be phosphorylated without an enzyme to form acetyl phosphate, a reactive acyl phosphate that could act as an abiotic equivalent to ATP, with a higher phosphorylating potential (AcP ∆G′ 0 = −43 kJ mol−1, ATP ∆G′ 0ADP = −31 kJ mol−1), providing a source of metabolic energy for phosphorylation and condensation to form polymers such as polypeptides and RNA (de Duve 1988, 1995; Martin and Russell 2007; Lane and Martin 2012). Overall, substrate-level phosphorylation produces acetyl phosphate, as argued by Ferry and House (2006), but in this case the whole process is driven by natural proton gradients.

Further phosphorylation and condensation reactions are only favoured if the concentration of monomers is high. That is possible, despite the anticipated low yields of most of these reactions, because alkaline hydrothermal vents should provide a dynamic concentration mechanism known as thermophoresis (Braun and Libchaber 2002; Baaske et al. 2007). Convection currents and thermal diffusion across the interconnected microporous matrix of alkaline vents produce thermal gradients that can concentrate organic molecules in the cooler regions. In closed experimental systems, even small thermal gradients (2.3–4.4 K) concentrate large molecules, notably DNA (Reineck et al. 2010) and RNA (Mast and Braun 2010; Mast et al. 2013), while fatty acids can be concentrated sufficiently to precipitate into vesicles (Budin et al. 2009). Thermophoresis is predicted to concentrate organics in open systems such as alkaline vents, but this has not previously been tested.

At a later stage, some form of compartmentalization is also crucial for selection to act on groups of replicators (e.g. RNAs) encoding functions such as metabolism and cooperation, rather than replication speed alone, which invariably leads to the formation of ‘Spiegelman’s monsters’ (Mills et al. 1967; Branciamore et al. 2009). The natural inorganic compartments in alkaline vents could facilitate not only the concentration of organics by thermophoresis, but also the beginnings of selection for metabolism (Branciamore et al. 2009; Koonin and Martin 2005). The two processes combined could potentially drive the replication of simple organic vesicles composed of mixed amphiphiles enclosing primitive replicators within vent pores (Budin et al. 2009; Mauer and Monndard 2011). Such vesicles are capable of growth and division, while retaining RNA (Hanczyc et al. 2003; Mansy et al. 2008) and are en route to the known end-point, modern cells with lipid membranes.