The inevitable journey to being

Abstract

Life is evolutionarily the most complex of the emergent symmetry-breaking, macroscopically organized dynamic structures in the Universe. Members of this cascading series of disequilibria-converting systems, or engines in Cottrell's terminology, become ever more complicated-more chemical and less physical-as each engine extracts, exploits and generates ever lower grades of energy and resources in the service of entropy generation. Each one of these engines emerges spontaneously from order created by a particular mother engine or engines, as the disequilibrated potential daughter is driven beyond a critical point. Exothermic serpentinization of ocean crust is life's mother engine. It drives alkaline hydrothermal convection and thereby the spontaneous production of precipitated submarine hydrothermal mounds. Here, the two chemical disequilibria directly causative in the emergence of life spontaneously arose across the mineral precipitate membranes separating the acidulous, nitrate-bearing CO2-rich, Hadean sea from the alkaline and CH4/H2-rich serpentinization-generated effluents. Essential redox gradients-involving hydrothermal CH4 and H2 as electron donors, CO2 and nitrate, nitrite, and ferric iron from the ambient ocean as acceptors-were imposed which functioned as the original 'carbon-fixing engine'. At the same time, a post-critical-point (milli)voltage pH potential (proton concentration gradient) drove the condensation of orthophosphate to produce a high energy currency: 'the pyrophosphatase engine'.

Keywords: alkaline hydrothermal; carbon fixation; disequilibria; origin of life; pyrophosphatase.

Figure 1.

The oxidation state of the upper mantle 100 Myr after its formation was controlled by the quartz/magnetite/fayalite buffer (QFM = SiO₂/Fe^II₂SiO₄/Fe^IIFe^III₂O₄) [3,40,42]. The dominant state of carbon in the upper mantle was as its full oxide with vanishingly small concentrations of methane (black diamonds) [41], explaining why the early atmosphere, mainly supplied by volcanoes, was dominated by CO₂ along with nitrogen and lesser SO₂ and NO. However, as shown by Shock [43], there is a cross-over of the oxidation states of carbon and iron very approximately at around 400°C. At the lower temperatures towards and at the surface of our planet the equilibrium state is methane (grey diamonds) as produced in hydrothermal systems through serpentinization [44,45], though the abiotic reduction of CO₂ at the Earth's surface is thermodynamically challenged. It is this metastable field (grey diamonds) that Shock [43] termed ‘the locus of biochemistry within geochemistry’. However, iron minerals comprising the QFM buffer would also tend to catalyse the reduction/hydrogenation of CO₂ to formate and methane. A further buffer (PPM = pyrite/pyrrhotite/magnetite or Fe^IIS₂/Fe^II_0.95S/Fe^IIFe^III₂O₄) operating where sulfide is concentrated would also tend to control the oxidation state of carbon at lower hydrogen fugacities and might be expected to catalyse redox reactions. The even more oxidized HM buffer (haematite/magnetite or Fe^III₂O₃/Fe^IIFe^III₂O₄) would be comparable to the mixed valence mineral green rust (e.g. [Fe^IIFe^III(OH)₄]⁺[OH]⁻) which might oxidize methane to organic intermediates at temperatures around 40°C [46]. Note how the redox state of iron contributes to the geochemical conditions that drove life into being and thereafter was central to its further evolution. Based on Shock [43].

Figure 2.

Diagram to show how a mantle convection engine continually provided new and reactive ocean floor in the Hadean as well as oxidized volatiles to feed the hydrosphere and atmosphere [24,27]. Hot buoyant updraughts of partially molten mantle transfer heat to the surface, so dividing and pushing the ocean floor apart. At the same time, a density inversion drives the basalt-to-eclogite transition which, in turn, produced further gravitational energy to the downward-pulling limbs with friction regulating flow rate [58]. Thick ocean lava plateaus were another result of mass transfer of heat in mantle plumes towards the Earth's surface. The atmosphere was relatively oxidized though the proportions of its components are not well constrained [3,42,52,55]. The figure provides a framework in which to understand the chemical and thermal energies produced in such an environment from submarine water–rock interactions that drove anaerobic litho-chemosynthetic life into being in a submarine hatchery around 4.4 Ga. It took more than another billion and a half years for wide littoral continental areas to develop and provide a nursery for burgeoning oxygenic photosynthesizers around 2.7 Ga [,–63]. Adapted from Russell et al. [24].

Figure 3.

The final cascade of engines leading to the emergence of life. The mantle convection engine (figure 2) delivers heat to the near surface and stresses the crust to effectively feed the serpentinization engine. The photographic montage of a typical, scale invariant example of serpentinite, offers us a gallery view of the composite engine responsible for driving life into being. The olivine-rich crustal rock fractures in response to the convective stress. The initial fractures propagate and anastomose as carbonic ocean water gravitates to depth and interacts with the hot rock. The hydrodynamic pressure increases the effective stress while at the same time exothermically oxidizing, carbonating, hydrating and hydrolysing the mineral constituents so allowing further access of water to rock. The force of crystallization causes large-scale expansion of the rock body, further fracturing and lowering the density of the rock, leading to diapirism and yet further fracturing. Apart from the physical free energy released as heat [95] by this disorganization, chemical free energy is also released, particularly at the propagating fracture tips. Here fresh iron–nickel-bearing mineral surfaces reduce water to hydrogen, whereas carbon dioxide is reduced to formate and methane, fuels for emerging life [,–98]. At the same time, calcium and some magnesium and sulfide ions are released to the fluids rendering them highly alkaline. Temperature is regulated by rock strength at the base of the cell while pH is buffered to approximately 11 units by brucite (Mg(OH)₂). This well-ordered hydrothermal effluent is driven convectively to the ocean floor where, on interaction with mildly acidic ocean water, porous mounds comprising iron–magnesium hydroxides and silicates, iron–nickel–cobalt–molybdenum sulfides and ephemeral iron–calcium–magnesium carbonates are precipitated [24,25,99]. We argue here that some of the marginal compartments, subjected to redox, pH and thermal gradients, assemble natural engines to dissipate these disequilibria while driving endergonic (anti-entropic) reactions: (i) a nickel/iron/molybdenum sulfide engine reducing CO₂ to CO, (ii) an electron bifurcating mixed valence molybdenum-bearing iron sulfide composite engine dissipates redox energy through the reduction of nitrite while oxidizing hydrothermal methane and reducing oceanic carbon dioxide, resulting in the generation of activated acetate [46], (iii) a pyrophosphatase engine comprising green rust interlayers [100,101] that clamp contiguous orthophosphates (2 × HPO₄²⁻ or Pi²⁻) in a natural metal ion mediated binding site where they condense, only to be released in the proton flux [19].

Figure 4.

Diagram to show how the entropic output from serpentinization fuels an emergent metabolic engine within the concomitantly precipitated alkaline hydrothermal mound with methane and hydrogen, augmented by pyrophosphate condensation driven by the ambient proton motive force. The natural titration of the alkaline hydrothermal solution with the acidulous ocean leads to precipitation of chemical garden-like compartments. A secondary acidulous ocean current bearing the oxidants is convectively driven by heat emanating from the mound and also pulled upward by entrainment in a manner comparable to a carburettor so that the reductants—delivered at a similar rate to the oxidants—are partially oxidized to organic intermediates [8,26,46]. Reactions are catalysed by the (dislocated) surfaces of transition metal sulfides or in the interlayers of green rust acting here as a di-iron methane monooxygenase [19,126]. The specific model engines argued here to have driven the first metabolic pathway are (i) electron bifurcation on Mo-sulfides reduced by H₂ in a two-electron reaction but ejecting these electrons in a gated manner towards a high potential acceptor (such as nitrate or nitrite) and a low potential iron–nickel–sulfur-containing mineral such as violarite [19,104,127]. This low potential mineral is considered to achieve reduction of CO₂ to CO in a reaction reminiscent of that at the catalytic metal cluster of CO-dehydrogenase (CODH); (ii) positive redox feedback loop in the reaction sequence from CH₄ through CH₃OH to CH₂O. CH₄ activation towards integration of an oxygen atom (resulting from NO produced by engine 1) requires reducing equivalents which are provided by the (lower midpoint potential) subsequent oxidation step of CH₃OH to CH₂O; (iii) condensation of the two C1-moieties issued from the high and low potential branches (i) and (ii) into acetate or an acetyl moiety on greigite [19,46]; (iv) a pyrophosphatase engine comprising green rust interlayers where water activity is close to zero, opens at the oxidized exterior through positive charge repulsion as the ferrous iron is oxidized (figure 5) [100,101], allowing protons access to the interior which pull orthophosphates by charge attraction (2×HPO₄²⁻ or P_i²⁻) into the subnanometric compartments. Clamped by the ferric iron atoms bordering the walls of the interlayers, neighbouring orthophosphates condense to the pyrophosphate (which has an overall lower charge as HP₂O₇³⁻ or PP_i³⁻) on interaction with protons. The flux of the remaining protons drives the pyrophosphates towards the rear exit of the green rust nanocrysts where they phosphorylate organic intermediates produced by engine 1.

Figure 5.

Speculative physical model of a putative green rust (fougerite H⁺-pyrophosphatase) [cf. –119], based on the generation within the mineral interlayers of redox polaron ‘quasi-particles’—manifest as localized channel dilations—that can propagate in a directed manner along the interlayer. Boundary conditions are given by the bathing of the outside of the iron hydroxide membrane in an aqueous solution of protons, carbon dioxide, nitrate and ferric iron (the Hadean Ocean simulant) while the inside, iron sulfide zone of the membrane, is bathed in hydrogen, methane and bisulfide (the alkaline hydrothermal solution simulant). The transmembrane potential—part redox and part pH gradient—totals approximately 1 V [19,140,148] and provides the vectorial free energy that drives the system's inherently endergonic processes: (i) the generation and inward propagation of localized, polaron-based, channel dilations, (ii) the confinement of phosphate under conditions of reduced water activity within a superficially positioned local dilation, (iii) the subsequent condensation to pyrophosphate which in turn permits the mobilization of the polaron dilation and (iv) the ‘pumping’ of the pyrophosphate into the interior against its own gradient. The ferrous hydroxide comprising the outer margins of the precipitate membrane begins to be oxidized by nitrate to green rust which has the effect of opening the interlayers locally as the ferric ions on either side of the interlayer repel each other, the positive charges attracting counter-ions such as chloride, nitrate, carbonate and phosphate to take up the space [,,,,–165]. The changes in local redox state locally distort the crystal structure inducing, via phonon interactions, the formation of localized polaron quasi-particles [171,172]. The polaron-based local dilations produced by the oxidation of green rust migrate through Fe³⁺ hole polaron transport, charge hopping interdependently correlating with anion migration along the interlayer towards the interior [173]. The double valent anions such as orthophosphate (Pi²⁻), confined within localized polaron distorions, are also pushed along the interlayer (acting like a protein channel or pore) which thereby acts as a peristaltic pump. Condensation of the phosphates to di- or polyphosphates takes place in the confined space of a single polaron dilation positioned at the external interface within the channel where water activity is low, in a reaction involving one proton and the generation of one water molecule per condensation and the consequent lowering of charge, thereby releasing the grip of the electron field and allowing the subsequent release of the condensed phosphates to the interior [,,,,,–175]. Re-reduction of the same green rust is through the oxidation of the hydrothermal methane and hydrogen (figure 4).