The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front

Abstract

Here we argue that life emerged on Earth from a redox and pH front at c. 4.2 Ga. This front occurred where hot (c. 150 degrees C), extremely reduced, alkaline, bisulphide-bearing, submarine seepage waters interfaced with the acid, warm (c. 90 degrees C), iron-hearing Hadean ocean. The low pH of the ocean was imparted by the ten bars of CO2 considered to dominate the Hadean atmosphere/hydrosphere. Disequilibrium between the two solutions was maintained by the spontaneous precipitation of a colloidal FeS membrane. Iron monosulphide bubbles comprising this membrane were inflated by the hydrothermal solution upon sulphide mounds at the seepage sites. Our hypothesis is that the FeS membrane, laced with nickel, acted as a semipermeable catalytic boundary between the two fluids, encouraging synthesis of organic anions by hydrogenation and carboxylation of hydrothermal organic primers. The ocean provided carbonate, phosphate, iron, nickel and protons; the hydrothermal solution was the source of ammonia, acetate, HS-, H2 and tungsten, as well as minor concentrations of organic sulphides and perhaps cyanide and acetaldehyde. The mean redox potential (delta Eh) across the membrane, with the energy to drive synthesis, would have approximated to 300 millivolts. The generation of organic anions would have led to an increase in osmotic pressure within the FeS bubbles. Thus osmotic pressure could take over from hydraulic pressure as the driving force for distension, budding and reproduction of the bubbles. Condensation of the organic molecules to polymers, particularly organic sulphides, was driven by pyrophosphate hydrolysis. Regeneration of pyrophosphate from the monophosphate in the membrane was facilitated by protons contributed from the Hadean ocean. This was the first use by a metabolizing system of protonmotive force (driven by natural delta pH) which also would have amounted to c. 300 millivolts. Protonmotive force is the universal energy transduction mechanism of life. Taken together with the redox potential across the membrane, the total electrochemical and chemical energy available for protometabolism amounted to a continuous supply at more than half a volt. The role of the iron sulphide membrane in keeping the two solutions separated was appropriated by the newly synthesized organic sulphide polymers. This organic take-over of the membrane material led to the miniaturization of the metabolizing system. Information systems to govern replication could have developed penecontemporaneously in this same milieu. But iron, sulphur and phosphate, inorganic components of earliest life, continued to be involved in metabolism.

The rocky roots of the acetyl-CoA pathway

“…it releases energy and thus will tend to occur), it is a linear pathway that does not require complicated biochemical intermediates to operate, and its biochemistry today involves organic reactions that are catalysed primarily by FeS and (Fe,Ni)S centres in proteins. These properties are highly compatible with the geochemically founded view that biochemistry arose within a hydrothermal mound made initially, among other things, of FeS and (Fe,Ni)S minerals [10,11].…”

“…Such naturally forming 3D FeS compartments, analogues of which have been reported from natural hydrothermal systems [10] (Figure 1), could have retained and ordered organic molecules produced by prebiotic reactions, rather than releasing them to dilution in the primordial ocean as in the organic soup or surface metabolism theories. By allowing sufficient concentrations of reactants to be generated and to accumulate, the hydrothermal reactor would permit the building blocks of life (bases, amino acids and sugars) to accumulate through continuous supply at their site of synthesis up to concentrations sufficient to support the origin of early selfreplicating systems until genuine, genetically encoded biological compartments -namely, membranes and cell walls -arose [11].…”

“…Its dual active-site reaction mechanism is thought to entail the reduction of CO 2 to CO with the help of electrons (most commonly stemming from H 2 ) at an Fe 4 NiS 5 cluster called the 'C-cluster' [16], and the subsequent condensation at the 'A-cluster' of the carbonyl group (CO) with a methyl group (donated by a corrinoid FeS protein) to produce a metal-bound acetyl group, which is released from the enzyme via thiolysis, yielding a thioester product [16 -20] (Figure 2). In the hydrogen-fermenting eubacterium Carboxydothermus hydrogenoformans, the acetyl-binding metal of ACS is [10]. It comprises botryoids (the bubble-laden surface) and chimneys (arrows), through which the hydrothermal waters exhaled, leading to the iron sulphide deposit.…”

“…For the setting, we suggest a mineral mound that channelled a highly reduced (H 2 -containing) hydrothermal fluid to meet the CO 2 -rich ocean bottom water in a compartmentalized reactor consisting of freshly and continuously formed (Fe,Ni)S walls [10,11] (Figure 3). H 2 is a significant constituent of hydrothermal fluid at deep-sea vents today [26], and at the origin of biochemistry some 4 billion years ago the concentration of H 2 in hydrothermal fluid that vented into the Hadean ocean would have been even higher [10]. Furthermore, the Hadean ocean had higher concentrations of CO 2 than have today's oceans [27].…”

“…The type of vent central to this model is not the familiar 'black smoker', because black smokers are much too hot (350 8C) for biochemical-like reactions [10]. And where, one might ask, did the metal sulphide colloidal barrier and compartments come from?…”