An origin-of-life reactor to simulate alkaline hydrothermal vents

Abstract

Chemiosmotic coupling is universal: practically all cells harness electrochemical proton gradients across membranes to drive ATP synthesis, powering biochemistry. Autotrophic cells, including phototrophs and chemolithotrophs, also use proton gradients to power carbon fixation directly. The universality of chemiosmotic coupling suggests that it arose very early in evolution, but its origins are obscure. Alkaline hydrothermal systems sustain natural proton gradients across the thin inorganic barriers of interconnected micropores within deep-sea vents. In Hadean oceans, these inorganic barriers should have contained catalytic Fe(Ni)S minerals similar in structure to cofactors in modern metabolic enzymes, suggesting a possible abiotic origin of chemiosmotic coupling. The continuous supply of H2 and CO2 from vent fluids and early oceans, respectively, offers further parallels with the biochemistry of ancient autotrophic cells, notably the acetyl CoA pathway in archaea and bacteria. However, the precise mechanisms by which natural proton gradients, H2, CO2 and metal sulphides could have driven organic synthesis are uncertain, and theoretical ideas lack empirical support. We have built a simple electrochemical reactor to simulate conditions in alkaline hydrothermal vents, allowing investigation of the possibility that abiotic vent chemistry could prefigure the origins of biochemistry. We discuss the construction and testing of the reactor, describing the precipitation of thin-walled, inorganic structures containing nickel-doped mackinawite, a catalytic Fe(Ni)S mineral, under prebiotic ocean conditions. These simulated vent structures appear to generate low yields of simple organics. Synthetic microporous matrices can concentrate organics by thermophoresis over several orders of magnitude under continuous open-flow vent conditions.

Fig. 1

a Standard reduction potentials of H₂ and CO₂ at pH 7. Transfer of electrons from H₂ to CO₂ is unfavourable as the reduction potential for CO₂ at this pH is lower (more negative) than H₂. b With H₂ dissolved in waters at pH 10 and dissolved CO₂ in waters at pH 6 however, the reduction potential for CO₂ becomes higher (more positive) than that of H₂ making the reduction of CO₂ favourable. This would theoretically allow for the reduction of CO₂ 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 CO₂ to formaldehyde via formate

Fig. 2

Photograph of the bench-top reactor containing ceramic foam within the reactor vessel. The reaction chamber is open-flow allowing for heated alkaline fluids and cool acidic fluids to be pumped into the main chamber with an outflow from the top into a collection vessel. There are several ports on the side of the reactor, which allow for addition of fluids or sampling while the reactor is in operation

Fig. 3

A series of photographs taken of the precipitates formed inside the reactor vessel over 4 h. a Initial formation of the precipitate structures. b After 20 min, the structures continue to form with the only disruption as they hit the surface of the fluid in the reactor. c After 1 h, precipitates of good structure are still forming. d After 4 h the precipitates become thicker around the base, probably inhibiting reduction across the barrier

Fig. 4

a Powder X-ray diffraction trace showing the precipitate is amorphous in character to X-rays: there are no peaks to indicate diffraction from crystal planes. b Results of elemental analysis of bulk precipitate conducted by EDX analysis. c SEM image of the precipitate collected from the reactor at ×330 magnification. d SEM image of the precipitate at ×7,000 magnification. e TEM image of the crystalline fractions of precipitate showing the presence of long, thin tetragonal crystals. f ×4 magnification of previous image showing the tetragonal crystals. g–i TEM lattice imaging of individual crystals showing visible atomic planes in the crystals. This planar difference was measured using a Gatan Digital Micrograph. The traces show light intensity at a specific cross-section of an individual micrograph indicating the spacing between the atomic planes. Average spacings measured were g 0.3 nm, h 0.5 nm and i 0.5 nm

Fig. 5

a GC–MS trace showing the analysis for formate. The formate peak at 2.45 min is the propyl-ester of formate. Estimated concentration is 50 µM based on extrapolation from calibration data. b GC–MS trace showing analysis for formaldehyde. The formaldehyde peak at 3.8 min is the PFBOA adduct. Estimated concentration is 100 nM based on extrapolation from calibration data. c Graph of formaldehyde concentration over time during the course of an experimental run. After an initial increase, the concentration remains relatively constant, though repeatability of sampling, total volume and dynamic reaction environment all impact on the repeatability and consistency of results

Fig. 6

a GC–MS trace showing sugars, with the peaks for glyceraldehyde, erythrose and ribose labelled. The internal standard (IS) used was myo-inositol. All enantiomers of ribose (arabinose, lyxose and xylose) were identified using known standards. b) The concentration over time of glyceraldehyde, erythrose and ribose. The area showing 0 to 5 h is with the reaction heated to 60 °C while the shaded area shows the reaction mixture left at ambient temperature (~20 °C) between 5 and 120 h

Fig. 7

a SEM image of the internal structure of the ceramic foam at ×70 magnification. The foam has a microporous, highly permeable structure with interconnected cavities ~100 µm in diameter. b SEM image of the foam structure at ×3,500 magnification showing ~10 µm cavities within the foam structure and also sub-micron holes inside the ceramic struts of the foam. c SEM image of a foam strut at ×6,500 magnification showing in greater detail the sub-micron cavities in a foam strut

Fig. 8

Temperature profile inside a foam exposed to vent-like conditions. The temperature graphs present axial profiles based on the division of the foam as shown (1–5, 2–6, 3–7, 4–8) in the circle diagram (inset). Fluid at 70 °C was flowing into the foam at a rate of 15 mL/h with a coolant fluid at 20 °C being pumped into the reactor at a rate of 120 mL/h. The reactor was left for a period of 1 h prior to temperature readings being taken. The warmer temperatures (red) are observed in the lower central regions with cooler temperatures (blue) in the upper outer regions of the foam. The photo (inset) shows the size of the foam before the temperature profile was taken

Fig. 9

a Fluorescent micrograph of foam soaked in a 50 µM fluorescein solution. Fluorescein enters the struts of the foam via the sub-micron pores in the structure and remains within the foam struts, not in the cavities as originally assumed. b Sections of the foam exposed to UV light. The foam has been infused with 0.1 µM fluorescein solution for a period of 4 h under vent conditions. The bright blue areas in the photos are areas of fluorescein concentration, estimated to be between ×2,500 and ×5,000 the concentration of inflow fluids (0.1 µM)