ARTICLE pubs.acs.org/Langmuir
Characterization of Iron Phosphate Silicate Chemical Garden Structures Laura M. Barge,*,† Ivria J. Doloboff,† Lauren M. White,†,‡ Galen D. Stucky,‡,§ Michael J. Russell,† and Isik Kanik† † ‡
Jet Propulsion Laboratory, California Institute of Technology, 4800 Oak Grove Drive, Pasadena, California 91109, United States Department of Chemistry & Biochemistry and §Department of Materials, University of California—Santa Barbara, Santa Barbara, California 93106, United States ABSTRACT: Chemical gardens form when ferrous chloride hydrate seed crystals are added or concentrated solutions are injected into solutions of sodium silicate and potassium phosphate. Various precipitation morphologies are observed depending on silicate and phosphate concentrations, including hollow plumes, bulbs, and tubes. The growth of precipitates is controlled by the internal osmotic pressure, fluid buoyancy, and membrane strength. Additionally, rapid bubble-led growth is observed when silicate concentrations are high. ESEM/EDX analysis confirms compositional gradients within the membranes, and voltage measurements across the membranes during growth show a final potential of around 150 200 mV, indicating that electrochemical gradients are maintained across the membranes as growth proceeds. The characterization of chemical gardens formed with iron, silicate, and phosphate, three important components of an early earth prebiotic hydrothermal system, can help us understand the properties of analogous structures that likely formed at submarine alkaline hydrothermal vents in the Hadean—structures offering themselves as the hatchery of life.
’ INTRODUCTION Chemical gardens are plantlike hollow structures that form when a hydrated metal salt is introduced into a solution containing another reactive ion. Depending on the experimental conditions, a variety of morphologies such as tubes and bulbous growths are produced. Such precipitates have been studied in a number of reactant systems.1 6 In the experiments reported here, metal salt FeCl2 3 4H2O is introduced into solutions of sodium silicate and potassium phosphate, whereupon a membrane of a gel precipitate immediately forms around the surface of the grain. The membrane, swelling osmotically as water molecules are drawn through the membrane, eventually ruptures at the weakest spot, generally at the apogee. The exhaling solution rises buoyantly if the outer solution (e.g., silicate) is denser, and a new layer continues to precipitate at the fluid interface. This process of osmotic pressure buildup leading to membrane rupture repeats and a precipitate structure grows until the reactants are exhausted or a state of near equilibrium is reached. Chemical garden precipitates can alternatively be formed by the slow inlet of a solution containing one reactive ion into a reservoir containing another reactive ion. A precipitate membrane forms at the interface between the two contrasting fluids that again grows according to fluid pressure and buoyancy.7 12 Chemical garden precipitates typically form vertical structures as a result of the buoyancy of the r 2011 American Chemical Society
less-concentrated inner fluid. Similar experiments, performed in microgravity, produced complex structures with no particular orientation, and flow was directed only by relative osmotic pressures at any given point.13,14 The viscosity of the solutions also affects the precipitation process. For example, in a gelatinous medium where convection is inhibited and the movement of reactants is controlled by diffusion, the interface between two reactive fluids can lead to self-ordered periodic precipitates such as Liesegang bands15 rather than the growth of chemical garden structures. Chemical-garden-type precipitates can be found in various natural settings, including hydrothermal vent systems, where hydrothermal fluid (altered from seawater composition by the process of serpentinization) interfaces with ocean water to form towering mineral structures at the Lost City hydrothermal vent field.16,17 Similar chemical-garden-type structures likely formed at off-axis hydrothermal vents on the early earth containing, along with other deposits, ferrous iron sulfides precipitated from the mixing of warm, alkaline, HS -bearing hydrothermal fluid with the anoxic, acidic, Fe2+-bearing Hadean ocean.7,18 The semipermeable membranes of these chemical garden structures in hydrothermal Received: September 22, 2011 Revised: October 25, 2011 Published: October 29, 2011 3714
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Langmuir systems have been proposed to be a possible environment for the emergence of life,18,19 primarily because they could maintain steep pH and chemical gradients at the interface between mildly acidic ocean and alkaline hydrothermal effluents, as demonstrated in laboratory simulations.7,11,12 It has been suggested that the proton gradient across an inorganic membrane separating solutions of different pH and composition would be capable of providing a natural protonmotive force sufficient to drive prebiotic chemical reactions such as the formation of pyrophosphate and peptides in a synergetic feedback cycle.20 Regarding such a condensation of pyrophosphate, a static membrane-bound pyrophosphatase was discovered in the purple nonsulfur bacterium Rhodospirillum rubrum that might well be the precursor to the rotary pump phosphatases that generate adenosine triphosphate (ATP) from adenosine diphosphate (ADP) via an enzymatically created protonmotive force.21 Since then, similar static H+-pumping inorganic pyrophosphatases have been discovered in the hyperthermophilic archaeon Pyrobaculum aerophilum and the hyperthermophilic bacterium Thermotoga maritima.22 Chemical garden structures grown in the laboratory may also maintain commensurate chemical and pH gradients between the inner and outer solutions. However, the self-assembling structures that form under the control of fluid dynamics and reactant concentrations may affect the gradients present in these systems. In this article, we have examined the growth of chemical garden structures formed with Fe2+, silicate, and phosphate—three important components of an early earth prebiotic hydrothermal system—to understand better the properties of similar structures that may have formed at Hadean alkaline hydrothermal vents.
’ EXPERIMENTAL SECTION Two hundred milligrams of FeCl2 3 4H2O crystals (procured from Sigma-Aldrich) was introduced into 15 mL aliquots of solutions (in 15 125 mm2 tubes) containing diluted sodium silicate (water glass, 10.6% Na2O/26.5% SiO2, procured from Sigma-Aldrich) and/or potassium phosphate (K2HPO4, Fisher Scientific). Alkaline silicate/phosphate solutions were made simply by mixing K2HPO4 salt with water and then adding concentrated sodium silicate solution. As soon as the seed FeCl2 3 4H2O crystals settled down to the bottom of the test tube, a precipitate membrane immediately formed around the crystal surface. The membrane expanded as water was osmotically drawn into the membrane’s interior, forcing it to rupture upward, thus creating vertically extending structures controlled (partially) by the buoyancy of the expanding fluid.22 In these experiments, we varied the concentrations of silicate (between 0 and 5 M) and phosphate (between 0 and 0.7 M). The pH of the phosphate/silicate solutions varied between 11 and 12 depending on the reactant concentrations before the FeCl2 3 4H2O crystals were added. (We were not able to measure the pH of the fluid inside the membrane.) Certain experimental conditions that were observed to give reproducible morphologies at room temperature were repeated at 70 °C, an appropriate temperature for an off-axis alkaline hydrothermal vent.24,25 After silicate/phosphate solutions were prepared, the 15 mL test tubes were immersed in a water bath at 70 °C for 5 min to heat the whole solution uniformly before the FeCl2 3 4H2O crystals were added. Precipitates were allowed to form for 5 10 min (enough time for the precipitate to reach the top of the test tube) before products were removed from the hot bath and photographed. We also performed experiments in which an aqueous solution of FeCl2 was fed slowly into the silicate/phosphate solution via a syringe. A 2 M FeCl2 solution (1.5 mL) was injected via syringe pump (at 50 or 80 mL/h) into 50 mL of a 2 M silicate/0.5 M phosphate solution. Such
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Figure 1. Experimental setup for syringe pump experiments. an arrangement was utilized to (1) to determine the effect of the flow rate on the morphology and (2) to allow for measuring the voltage across the membranes. Membrane potentials were measured by feeding the FeCl2 seed solution from beneath the silicate/phosphate solution into a small 1-cm-long open-ended tube (∼5 mm diameter) placed at the bottom of a glass container. A wire connected to a voltmeter was inserted into the top of this tube, and a second wire was placed into the bulk silicate/phosphate solution. After the syringe tube was flushed with distilled/deionized H2O to remove any air bubbles, FeCl2 solution was fed in slowly so that the chemical garden enveloped the inner wire as it grew (Figure 1). The voltage across the membrane was measured until the feed of FeCl2 was halted. Membrane potentials were measured using a Fluke 87 multimeter with 26 gauge tinned copper wires. The pH of the outer and syringe solutions was measured (syringe solution pH ∼2.5, outer solution pH ∼11 12) before injection began. Images of the resulting precipitates were obtained by using a Nikon SMZ-10A optical microscope at 20 magnification. High-resolution imaging and chemical analysis were also carried out on the resulting structures using an environmental scanning electron microscope (ESEM) with an attached energy-dispersive X-ray tube (EDX). ESEM images were obtained using a voltage of 20 kV and a working distance of 10 mm. EDX spectra were collected at the same voltage with a point dwell time of 30 s. Semiquantitative atomic weight percents were calculated from EDX spectra using INCA microanalysis software. Time lapse photographs were also taken at 5 s intervals throughout the growth of the precipitate.
’ RESULTS When the FeCl2 3 4H2O seed crystals were introduced into a solution containing silicate and phosphate, a layer of precipitate immediately formed around the crystal and began to expand as water was osmotically drawn across the membrane from the outside salt solution. The membrane ruptured (usually in more than one place) and expanded vertically, producing various interconnected structures extending toward the top of the tube. Our observations indicate that the concentrations of silicate and phosphate determine, or at least strongly influence, the varying precipitate morphologies and the structures formed. On the basis of the concentration of phosphate and silicate, the structures formed were reliably predictable and reproducible, although the exact morphology varied between experiments. Generally, the precipitated chemical garden structures reached the top of the test tube within 5 10 min (growing at ∼1 2 cm/min to a total 3715
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Figure 2. Examples of precipitate morphologies. (A) Bulbs (dashed arrow) and plumes (solid arrow) formed with 1 M silicate and 0.7 M phosphate. (B) Hairs formed with 1 M silicate and 0.5 M phosphate. (C) Tubes formed with 3 M silicate and 0.5 M phosphate.
height of ∼10 cm, though exact growth rate varied depending on the experiment and type of morphology) (Figure 2A). Precipitate Morphology. Precipitate morphologies fell into four general types, termed here as (i) hairs (thin, fragile hairlike structures extending vertically from the crystal surface (Figure 2B)); (ii) bulbs (smooth rounded bulbous structures, several millimeters across, that grew both vertically and in random directions (Figure 2A)), (iii) plumes (larger structures several millimeters across that always grew vertically (Figure 2A)), and (iv) tubes (millimeters-sized hollow tubular structures generally exhibiting bubble-led growth (Figure 2C)). Examples of these are shown in Figure 2. In many cases, these four structures grew superimposed on one another. For example, plumes often grew vertically from the top surface of a bulb (Figure 2A). The growth of bulbs did take place in bursts as the membrane ruptured, but no pulsating growth exhibiting a periodic pattern was observed. We also observed color changes that varied with the morphology. Specifically, most precipitates were white immediately after formation. However, the plumes gradually turned dark green over several hours while the bulbs turned dark green almost immediately after formation (possibly indicating the rehydration of Fe2+). Varying Silicate Concentration. The concentrations of sodium silicate and potassium phosphate (Table 1) appeared to affect the resulting morphology of the precipitate strongly. In experiments with no silicate and 0.5 M phosphate, only hairs formed. However, experiments with no phosphate and 2 M silicate produced bulbs and attached plumes (similar in appearance to Figure 2A). To understand this dependence on concentration better, a series of experiments were performed in which the phosphate concentration was kept constant at 0.5 M while the silicate concentration was varied between 0 and 5 M. As the silicate concentration increased, the precipitate morphology
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progressed from hairs (between 0 and 1 M silicate) to bulbs and plumes with occasional tubes (between 1 and 2 M silicate) to only tubes (3 M silicate) (Figures 3 5). At 4 and 5 M silicate, the phosphate/silicate solution was too viscous to allow the FeCl2 3 4H2O crystals to settle to the bottom of the tube. In experiments where the silicate was below 1 M, a silica gel formed throughout the entire tube within 1 h, causing the vertical growth of the precipitation structure to be impeded by the increased viscosity. This is probably a result of the acidification of the silicate solution by the dissolution of FeCl2 3 4H2O crystals, which causes silicate molecules to protonate and form a gel lattice.15 In experiments where a gel formed, precipitation continued in the gel until the reactants were exhausted, forming structures that were controlled by diffusion instead of fluid buoyancy. Varying Phosphate Concentration. Another series of experiments were performed in which the silicate concentration was kept constant at 1 M but the phosphate concentration was varied between 0.1 and 0.7 M. Below 0.3 M phosphate, only hairs were formed, but above about 0.4 M phosphate, bulbs and plumes formed (Figure 6). To test whether morphologies were controlled by the relative ratios of silicate/phosphate rather than absolute concentrations, we repeated this series of experiments with a constant silicate concentration at 2 M and varied the phosphate concentration from 1.1 to 1.4 M, leaving the ratios of silicate/phosphate unchanged. At 2 M silicate and 1.1 M phosphate, bulbs formed that were smaller than the bulbs formed at 1 M silicate and 0.55 M phosphate; however, above 1.2 M phosphate, only tubes formed. Heated Experiments. Through trial and error, we determined several experiments that yielded the most reproducible morphologies. These specific experiments were then repeated at 70 °C to determine the effects (if any) of temperature on the precipitate morphology. A general trend was observed where only plumes and hairs formed at the higher temperature whereas the bulbs and tubes prominent in room-temperature experiments did not form. In one heated experiment containing 1 M silicate and 0.7 M phosphate, bulbs did form with plumes, but these bulbs were much smaller in diameter and height than those formed in the same experiment at room temperature. Fluid Flow Rate. Additional experiments were performed where, instead of introducing FeCl2 into the system as solid crystals, an FeCl2 solution was slowly fed via syringe pump into the silicate/phosphate solution. In FeCl2 solution experiments where concentrations of 1 M silicate and 0.5 M phosphate were used, bulb growth occurred at a flow rate of 80 mL/h and plume growth occurred when the flow rate was lowered to 50 mL/h. Upon increasing the silicate concentration to 2 M, bulbs with attached plumes formed at both 80 and 50 mL/h. Identical results were observed when these experiments were repeated without phosphate. Additionally, a separate FeCl2 experiment containing 0.5 M silicate/0.5 M phosphate and using a flow rate of 80 mL/h yielded plume growth, but because of the low silicate concentration, a gel formed throughout the entire vessel. Visual and Compositional Analysis. In some cases, the precipitation structures were removed from the tubes after 24 h and examined under an optical microscope. Optical imaging revealed that the plumes contained a solid outer wall and an interior filled with white gelatinous material. However, images of tubular and bulbous precipitates revealed a hollow structure filled with clear fluid (Figure 3). Time-lapse photographs show that fluid flows up through the entire bulb structure as it grows and continues to flow upward as plumes grow directly from bulb 3716
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Table 1. Experimental Conditions and Resulting Morphologiesa Crystal Dissolution Experiments: 25 °C phosphate (M) morphology
silicate (M) 0
0.5
0.25
0.5
hairs hairs (gel formed)
1
0.5
hairs, some bulbs and plumes.
2
0.5
bulbs, some plumes.
2
0
bulbs, plumes
3 1
0.5 0.1
tubes, some bulbs hairs
1
0.2
hairs
1
0.3
hairs, some bulbs and plumes
1
0.4
hairs, plumes, no bulbs
1
0.55
bulbs, plumes
1
0.6
bulbs, plumes
1
0.65
bulbs, plumes
1 2
0.7 1.1
bulbs, plumes smaller bulbs
2
1.2
tubes
2
1.3
tubes
2
1.4
tubes
Crystal Dissolution Experiments: 70 °C phosphate (M) morphology
silicate (M) 0
0.5
hairs
1
0.7
plumes, some small bulbs
2
0
hairs, plumes
2
0.5
plumes
2
1.4
plumes
silicate (M)
Fluid Flow Experiments: 25 °C phosphate flow rate (M) (mL/h) morphology
0.5
0.7
50
plumes (solution gelled after 5 min)
1
0.5
50
plumes
1
0.5
80
bulbs
2
0
80
bulbs and plumes
2
0.5
50
bulbs and plumes
2
0.5
80
bulbs and plumes
a
Morphologies are denoted as hairs, bulbs, plumes, and tubes as described in the Results section. In crystal dissolution experiments, 0.2g of FeCl2 3 4H2O crystals was dropped into 15 mL aliquots of silicate/ phosphate solution. In fluid flow experiments, 1.5 mL of a 2 M FeCl2 solution was injected slowly into 50 mL aliquots of silicate/phosphate solution.
surfaces (Figure 4). In experiments where tubes were produced, time lapse images revealed bubble-directed growth (Figure 5). For experiments containing 2 M silicate and 0.5 M phosphate (which gave bulbs and plumes at room temperature), the precipitates were removed from the tube after 2 h for ESEM imaging. ESEM images of the hollow bulbs show that the interior of the membrane is particulate whereas the exterior appears to be smooth and amorphous (Figure 7). Semiquantitative ratios were calculated from EDX spectra collected over the inner membrane
of the bulb (Figure 7C) and yielded an Fe/P/Si ratio of approximately 1:0.1:0.6. In contrast, ratios calculated for the smooth exterior layer of the bulb (Figure 7A) yielded an Fe/P/Si ratio of approximately 1:2.9:3.6. These ratios indicate that the inner particles are relatively iron-rich and the outer membrane is silicate- and phosphate-rich. Average Fe/P/Si ratios obtained from the outer surface of the large plume (Figure 7D) gave values of 1:1.3:3.7. Membrane Potentials. To measure voltage across growing membranes, a 26 gauge tinned copper wire was introduced through the injection aperture such that it would be enveloped within the chemical garden as it grew (Figure 1). A second wire was also inserted into the external solution. For all experiments, the starting voltage was between 0 and 10 mV. Over the course of precipitate growth, the voltage was observed to increase in the outer solution and decrease inside the membrane. The increase in electric potential across the membrane was measured with time (as the difference in exterior (VE) and interior (VI) voltage) for various silicate concentrations and injection rates of FeCl2 of 50 or 80 mL/h. When exterior solutions contained 1 M silicate and 0.5 M phosphate, the voltage remained largely constant (between 150 and 200 mV) after the precipitates stopped growing (i.e., when growth met the liquid surface) (Figure 8). For exterior solutions containing 2 M silicate and 0.5 M phosphate, the final potential was between 150 and 200 mV for a flow rate of 50 mL/h but only ∼100 mV for a flow rate of 80 mL/h. A control experiment was also performed where only 2 M silicate, and no phosphate, was included in the exterior solution. For this experiment, the final voltage was higher at ∼200 250 mV.
’ DISCUSSION Chemical garden structures form by precipitation at the interface between two solutions containing reactive ions, which create self-ordering structures. The physical properties of these structures primarily depend on the relative density of the two solutions, the respective concentrations, the osmotic flow across the membrane, the temperature/viscosity of the ambient fluid and the structural resistance of the membrane precipitate. In the experiments presented here, the reactive ions include Fe2+ in the inner solution and phosphate as well as silicate in the outer solution. Precipitates formed from these solutions were structurally stable while maintaining steep chemical and pH gradients across the mineral membranes. Processes of Membrane Growth. We observed general trends in the conditions required for the occurrence of the four types of observed precipitates (hairs, bulbs, plumes, and tubes) in iron silicate phosphate chemical garden experiments. Hairs formed at very low silicate concentrations and in experiments with only iron and phosphate. Bulbs tended to form exclusively at intermediate silicate concentrations (∼2 M). However, bulb growth was induced with the addition of 0.5 M phosphate to a 1 M silicate experiment (Figure 6). The fact that 1 M silicate experiments did not form bulbs until 0.5 M phosphate was added is curious but may be due to phosphate increasing the durability and lowering the permeability of the precipitate. In all of our experiments, the bulb structures allowed for the visible flow of fluid throughout the entire structure (and feeding into the plume). Higher silicate concentrations led to hollow tube growth directed vertically by air bubbles (Figure 5), a phenomenon that has been observed in several other reaction precipitation systems,5,6,26,27 3717
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Figure 3. Precipitates at 20 magnification (for an experiment containing 2 M silicate and 0.5 M phosphate). (A) Bulb, (B) plume, and (C) tube.
Figure 6. Effect of phosphate concentration. Experiments with 1 M silicate plus (A) no phosphate, (B) 0.1 M phosphate, (C) 0.2 M phosphate, (D) 0.3 M phosphate, (E) 0.5 M phosphate, and (F) 0.7 M phosphate.
Figure 4. Time-lapse photographs of bulb and plume growth in an experiment containing 2 M silicate and 0.5 M phosphate. Fluid flows up the entire bulb structure as it grows. At a certain point, bulb growth stops and the fluid is released more steadily through a membrane rupture, forming a vertical plume.
Figure 5. Time-lapse photographs of bubble-directed tube growth (in an experiment containing 2 M silicate and 0.5 M phosphate). Bubbledirected tubes occasionally grew along with bulbs and plumes in 2 M silicate experiments, but above 2 M silicate, only bubble-led tubes formed.
and may have been caused by the trapping of air bubbles close to the seed crystals by the high-viscosity silicate solution.6 Upon obtaining time-lapse images, trends in growth mechanisms were also observed for the different morphologies. Bulb growth occurred in both vertical and random directions depending on the solution viscosity. This suggests that bulb growth is
primarily determined by the fluid inside the membrane, which causes ruptures at points of weakness. In the case of the precipitation of plumes, time-lapse imaging shows only vertical growth, suggesting that plumes are controlled by fluid buoyancy. This difference in bulb and plume growth patterns may be due to the fact that the bulb membrane is more structurally resistant than the walls of the plumes (a fact that was evident when we removed the structures from tubes for analysis). This would allow more fluid pressure buildup inside the bulb wall, even though the osmotic flow is higher in experiments with lower silicate concentrations (i.e., higher water content).6 Certain initial conditions were further studied in fluid flow experiments (where concentrated FeCl2 solution was slowly fed into the outer solution with a syringe pump). These fluid flow chemical garden experiments are not precisely analogous to the experiments where metal crystals are dropped directly into the external solution because in a fluid flow experiment the pressure inside the membrane is a combination of the syringe pump rate and the osmotic pump of the membrane itself whereas in crystal dissolution experiments the internal pressure is purely osmotic. However, the fact that decreasing the flow rate in 1 M silicate experiments induced a morphology transition from bulb to plume implies that the transition from bulb to plume in a similar crystal dissolution experiment is caused by the internal fluid pressure reaching a critical value. In similar experiments in a CuSO4/silicate system (where CuSO4 solution was injected into a silicate solution), others have found that keeping flow rate constant but increasing the CuSO4 concentration in the seed solution led to a transition from smooth vertical growth to bulbous structures.2,8 It is to be expected that increasing the flow rate or increasing the concentration of metal salt in the seed solution may have a similar effect because the result of both is to increase the internal fluid pressure (a higher salt concentration 3718
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Figure 7. ESEM images of a bulb (dashed arrow) and plume (solid arrow) grown with 2 M silicate and 0.5 M phosphate. (A) The outer surface of the hollow bulb. (B) View into the inside of the bulb. (C) Magnified view of the edge of the membrane in B, showing the particulate character of the inner membrane. The inside of the bulb membrane has an approximate Fe/P/Si ratio of 1:0.1:0.5, and the outer wall has an approximate Fe/P/Si ratio of 1:2.9:3.6. (D) The outer wall of the large plume. For the plume interior, Fe/P/Si = 1:0.6:1.8, and for the plume exterior, Fe/P/Si = 1:1.3:3.7.
in the interior would increase osmotic flow to the inside of the membrane). Chemical Gradients and Membrane Potentials. Compositional gradients in chemical garden structures have been observed in a number of systems, supporting the osmotic pump theory.2 4,6,27 In the experiments reported here, the compositional gradient from the membrane exterior to interior varied depending on the type of precipitation structure formed. In an experiment where the external fluid contained 2 M silicate and 0.5 M phosphate, the changes in Fe/Si and Fe/P ratios were larger across the bulb membrane than across the plume membrane. This indicates that there is a steeper chemical gradient across the bulb membrane than across the plume. The concentration of Fe2+ in the inner solution presumably decreases with distance from the original crystals; concomitantly, the Fe2+ concentration and acidity in the interior should decrease with height inside the bulb, assuming that there is not much convective mixing within the bulb. The plumes usually start growing from the surface of a bulb (though occasionally they grow directly from the bottom of the tube), and the relatively high silicate content of the plume interior suggests that the interior/exterior gradients of the Fe2+ concentration and pH are probably much smaller than in the interior of the hollow bulb below. In the fluid flow experiments, we observed an increase in the membrane potential from ∼0 10 mV to about 150 200 mV during the period of growth of the chemical garden structures (Figure 8). In 1 M silicate/0.5 M phosphate solutions, the final potential maintained across the membrane was similar regardless of the flow rate (i.e., it did not depend on whether the precipitate formed a bulb or a plume). (We did observe that the increase in potential was slightly delayed when plumes formed, but plumes and bulbs eventually reached similar stable values.) The pH of the outer solution was monitored concurrently and remained constant in all experiments. This observed voltage change also supports the osmotic pump theory because OH ions are being drawn into the interior of the membrane,13,23 creating a charge difference.
Figure 8. Voltage measured across the membranes. Voltage was measured across the chemical garden membranes as they grew, from one wire enveloped inside the membrane precipitate and another wire in the external solution. Measurements were made until the precipitate stopped growing.
Implications for a Hydrothermal Origin of Life Model. We have seen clear evidence for compositional and electrochemical gradients in our chemical garden structures and can surmise a steep pH gradient as well because of the dissolution of the hydrated metal salt. The precipitate membranes produced in most of the laboratory chemical garden scenarios are semipermeable, and some ions can be transported across them,6 similar to the osmotic properties of biological membranes. Membrane potentials and pH gradients across inorganic membranes may be able to drive chemical reactions in the same manner that the protonmotive force (PMF) across organic membranes drives ATP synthesis from ADP and inorganic phosphate.18,22,28,29 3719
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Langmuir We suggest the possibility that a similar phenomenon could occur in chemical garden structures if the reactants were directly incorporated into the precipitate and/or the wall of the precipitate structure itself incorporated catalytic entities (e.g., iron sulfide minerals18,19). The PMF available in our chemical garden membranes is a combination of the pH gradient and the electrical membrane potential. We were not able to measure the pH of the solution inside the precipitates, but the minimum value is the pH of the syringe solution that is initially injected (∼2.5) and the inner pH should increase as precipitation and equilibration with the outer solution (pH ∼11 12) proceed. The PMF in these inorganic membranes is certainly variable depending on time and experimental conditions, but by taking an example value of the pH gradient as 7 units and an average measured membrane potential of 175 mV, we can calculate the total PMF across the membrane at about 240 mV.30 This is comparable to the PMF in mitochondria (∼200 mV) and therefore may be sufficient to drive certain reactions, such as the synthesis of pyrophosphate. More work is needed to determine the extent to which this might be possible and to characterize the effects of sulfide on the growth of chemical garden structures. (The likely presence of iron sulfides in chemical garden structures at Hadean hydrothermal vents is significant because iron sulfides are known to catalyze organic reactions,31,32 and the lattice of greigite is affine with the active centers of metalloenzymes such as acetyl coenzyme-A and carbon monoxide dehydrogenase, suggesting an inorganic origin of these metabolisms.19) The osmotic gradients causing the growth of these chemical garden precipitates are eventually dissipated as the dissolution of the FeCl2 3 4H2O crystals progresses (i.e., in laboratory experiments, pH gradients and membrane potentials may be expected to decay after a period of time). In the chemical garden structures of iron sulfide silicate phosphate formed at an alkaline hydrothermal vent on the early earth,19 the chemical and pH gradients would be effectively inexhaustible because of the constant influx of the alkaline, HS -bearing hydrothermal effluent into a mildly acidic Fe2+-bearing ocean.18,19 A series of inorganic membranes formed in these systems could have maintained electrochemical and pH gradients for thousands of years.33 The 5.5 unit pH gradient between the carbonic acid Hadean ocean (thought to have a pH of around 5.5) and alkaline hydrothermal fluid (known from present day submarine springs and laboratory simulations to have a pH near 11) would yield a PMF of about 300 mV,11,16,34 which is also comparable to biological membrane potentials. The semipermeable nature of these chemical garden precipitates at off-axis hydrothermal vents may have allowed reaction products produced within the membrane via chemical/ pH gradients to accumulate there, concentrating products and driving further reactions. To form chemical garden precipitates on timescales feasible for laboratory experiments, the reactant concentrations in our work are certainly higher than would be expected in a natural setting. Moreover, the effects of adding sulfide and organic molecules were not explored but will be the subject of future work. However, our experiments demonstrate the formation of semipermeable inorganic membranes containing iron and phosphate and demonstrate the formation of pH and electrochemical gradients, providing a basis for understanding how similar structures formed in hydrothermal systems may have maintained similar gradients and fueled chemical reactions within the membrane.
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’ CONCLUSIONS We observed different precipitate morphologies in iron silicate phosphate chemical garden experiments: thin, fragile hairlike structures extending vertically from the crystal surface, hollow bubble-directed tubes (when silicate concentrations were high), hollow bulbous growths (at intermediate silicate concentrations or at low silicate concentrations when phosphate was added), and plumes (at low silicate concentrations). The bulbous and tubular membranes are the most structurally resistant and support greater internal fluid pressures than do the plumes. Compositional analysis reveals that the membranes comprising the bulbs have large compositional gradients, hosting a particulate iron-rich interior and a smooth silicate- and phosphate-rich exterior. Experiments performed with a ferrous chloride seed solution give more reproducible morphologies than do the seed crystal experiments, and the flow rate had a dramatic effect on the precipitate type. Voltage was measured across the membranes as they grew, and we measured final potentials of between 100 and 200 mV depending on the initial conditions. In these experiments, bulbs maintained the most significant chemical gradients between solutions, and membrane potentials were also maintained. The semipermeable membrane of the chemical garden formed at the interface of two solutions of different compositions and pH is similar in some ways to the iron sulfide-containing precipitates that may have formed between acidic, Fe2+- and phosphate-containing seawater and alkaline, HS -containing hydrothermal fluid in Hadean off-axis vent systems. The electrochemical gradients measured in these experiments, along with the examination of varying morphologies, are significant in understanding the growth of large-scale, self-assembling, hydrothermal precipitation structures at off-axis alkaline vents on the early earth and the rise of chemical complexity leading to the emergence of life. ’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
’ ACKNOWLEDGMENT L.M.W. was supported by the ConvEne IGERT Program (NSF-DGE 0801627). M.J.R. was supported by the Research and Technology Development Program of the JPL. The research described in this publication was carried out at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration with support by the NASA Astrobiology Institute (Icy Worlds). We acknowledge useful discussions with members attending the first and second meetings of the NAI-sponsored Thermodynamics Disequilibrium and Evolution Focus Group. ’ REFERENCES (1) Coatman, R. D.; Thomas, N. L.; Double, D. D. J. Mater. Sci. 1980, 15, 2017–2026. (2) Pagano, J. J.; Thouvenel-Romans, S. T.; Steinbock, O. Phys. Chem. Chem. Phys. 2006, 9, 110–116. (3) Parmar, K.; Chaturvedi, H. T.; Akhtar, M. W.; Chakravarty, S.; Das, S. K.; Pramanik, A.; Ghosh, M.; Panda, A. K.; Bandyopadhya, N.; Bhattacharjee, S. Mater. Charact. 2009, 60, 863–868. (4) Parmar, K.; Pramanik, A. K.; Bandyopadhya, N. R.; Bhattacharjee, S. Mater. Res. Bull. 2010, 45, 1283–1287. 3720
dx.doi.org/10.1021/la203727g |Langmuir 2012, 28, 3714–3721
Langmuir
ARTICLE
(5) Cartwright, J. H. E.; Escribano, B.; Khokhlov, S.; Sainz-Díaz, C. I. Phys. Chem. Chem. Phys. 2010, 13, 1030–1036. (6) Cartwright, J. H. E.; Escribano, B.; Sainz-Díaz, C. I. Langmuir 2011, 27, 3286–3293. (7) Russell, M. J.; Hall, A. J.; Turner, D. Terra Nova 1989, 1, 238–241. (8) Thouvenel-Romans, S.; van Saarloos, W.; Steinbock, O. Europhys. Lett. 2004, 67, 1:42–48. (9) Stone, D. A.; Lewellyn, B.; Baygents, J. C.; Goldstein, R. E. Langmuir 2005, 21, 10916–10919. (10) Pagano, J. J.; Bansagi, T., Jr.; Steinbock, O. J. Phys. Chem. C 2007, 111, 9324–9329. (11) Mielke, R. E.; Russell, M. J.; Wilson, P. R.; McGlynn, S. E.; Coleman, M.; Kidd, R. D.; Kanik, I. Astrobiology 2010, 10, 799–810. (12) Mielke, R. E.; Robinson, K. J.; White, L. M.; McGlynn, S. E.; McEachern, K.; Bhartia, R.; Kanik, I.; Russell, M. J. Astrobiology 2011, in press. (13) Jones, D. E. H.; Walter, U. J. Colloid Interface Sci. 1998, 203, 286–293. (14) Cartwright, J. H. E.; Escribano, B.; Sainz-Díaz, C. I.; Stocieck, L. S. Langmuir 2011b, 27, 3294–3300. (15) Henisch, H. K. Crystals in Gels and Liesegang Rings; Cambridge University Press: Cambridge, U.K., 1988; Chapter 5. (16) Kelley, D. S.; Karson, J. A.; Blackman, D. K.; Fr€uh-Green, G. L.; Butterfield, D. A.; Lilley, M. D.; Olson, E. J.; Schrenk, M. O.; Roe, K. K.; Lebon, G. T.; Rivizzigno, P.; the AT3-60 Shipboard Party . Nature 2001, 412, 145–149. (17) Kelley, D. S.; Karson, J. A.; Fr€uh-Green, G. L.; Yoerger, D. R.; Shank, T. M.; Butterfield, D. A.; Hayes, J. M.; Schrenk, M. O.; Olson, E. J.; Proskurowski, G.; Jakuba, M.; Bradley, A.; Larson, B.; Ludwig, K.; Glickson, D.; Buckman, K.; Bradley, A. S.; Brazelton, W. J.; Roe, K.; Elend, M. J.; Delacour, A.; Bernasconi, S. M.; Lilley, M. D.; Baross, J. A.; Summons, R. E.; Sylva, S. P. Science 2005, 307, 1428–1434. (18) Russell, M. J.; Daniel, R. M.; Hall, A. J.; Sherringham, J. A. J. Mol. Evol. 1994, 39, 231–243. (19) Russell, M. J.; Hall, A. J. In Geological Society of America Memoirs; Kesler, S. E., Ohmoto, H., Eds.; The Society: Boulder, CO, 2006, 198, p. 1 32. (20) Milner-White, E. J.; Russell, M. J. J. Cosmol. 2010, 10, 3217– 3229. (21) Baltscheffsky, M. Nature 1967, 216, 241–243. (22) Baltscheffsky, M.; Schultz, A.; Baltscheffsky, H. FEBS Lett. 1999, 457, 527–533. (23) Cartwright, J. H. E; García-Ruiz, J. M.; Novella, M. L.; Otalora, F. J. Colloid Interface Sci. 2002, 256, 351–359. (24) Proskurowski, G; Lilley, M. D.; Kelley, D. S.; Olson, E. J. Chem. Geol. 2006, 229, 331–343. (25) Martin, W; Baross, J; Kelley, D; Russell, M. J. Microbiology 2008, 6, 805 814. (26) Thouvenel-Romans, S.; Pagano, J. J.; Steinbock, O. Phys. Chem. Chem. Phys. 2005, 7, 2610–2615. (27) Stone, D. A.; Goldstein, R. E. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 11537–11541. (28) Lane, N. New Sci. 2009, October 17, 38 42. (29) Lane, N. J. Cosmol. 2010, 10, 3286–3304. (30) Mathews, C. K.; van Holde, K. E. Biochemistry, 2nd ed.; The Benjamin/Cummings Publishing Company: Menlo Park, CA, 1996; Chapter 15. (31) Huber, C.; W€achtersh€auser, G. Science 1997, 276, 245–247. (32) Huber, C.; W€achtersh€auser, G. Tetrahedron Lett. 2003, 44, 1695–1697. (33) Ludwig, K. A.; Shen, C.-C.; Kelley, D. S.; Cheng, H.; Edwards, R. L. Geochim. Cosmochim. Acta 2011, 75, 1869–1888. (34) Macleod, G.; Mckeown, C.; Hall, A. J.; Russell, M. J. Origins Life Evol. Biospheres 1994, 24, 19–41.
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dx.doi.org/10.1021/la203727g |Langmuir 2012, 28, 3714–3721
