Article Cite This: ACS Earth Space Chem. XXXX, XXX, XXX−XXX
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Selective Adsorption of Aspartate Facilitated by Calcium on Brucite [Mg(OH)2] Charlene F. Estrada,*,†,‡,§ Dimitri A. Sverjensky,‡ and Robert M. Hazen§ ‡
ACS Earth Space Chem. Downloaded from pubs.acs.org by UNIV OF RHODE ISLAND on 12/05/18. For personal use only.
Department of Earth and Planetary Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, Maryland 21218, United States § Geophysical Laboratory, Carnegie Institution for Science, 5251 Broad Branch Road Northwest, Washington, District of Columbia 20015, United States S Supporting Information *
ABSTRACT: Dissolved ions present in an aqueous environment may significantly improve biomolecule attachment at mineral surfaces through the formation of cooperative surface complexes. To test whether this phenomenon results in the selective adsorption of an organic species, we conducted batch adsorption experiments with an equimolar mixture of the amino acids aspartate, glycine, lysine, leucine, and phenylalanine onto powdered brucite [Mg(OH)2] at pH 10.2. We performed the batch experiments in triplicate both without and with 4.1 mM CaCl2. In experiments without CaCl2, we observed that up to 0.7 μmol m−2 of aspartate and about 0.4 μmol m−2 each of the remaining four amino acids adsorbed onto brucite. When we added CaCl2, we found that up to 1.6 μmol m−2 of aspartate selectively adsorbed onto the brucite surface relative to between 0.2 and 0.3 μmol m−2 of the other amino acids. We measured the brucite particle surface charge to be slightly positive without added CaCl2, but the surface charge becomes significantly more positive in the presence of CaCl2. Our results suggest that negatively charged molecules selectively and cooperatively adsorb onto brucite when CaCl2 is added to the system. This study emphasizes the importance of the dissolved ionic profile of a geochemical environment when evaluating the role of mineral surfaces in the evolution of prebiotic chemistry. The presence of dissolved ions at a mineral−water interface can selectively enhance the adsorption and concentration of specific molecules, which may serve as a key process in molecular self-organization and the assembly of proteins that are composed of metal−ligand complexes. KEYWORDS: amino acids, brucite, cooperative adsorption, competitive adsorption, prebiotic chemistry
1. INTRODUCTION Calcium is ubiquitous in all living organisms and performs a wide variety of essential biochemical processes, including glycolysis, cell signaling, ion transport, and apoptosis.1 Calcium-binding proteins (CaBPs) play a fundamental role in these processes and occur in eukarya, prokarya, and archaea.2−4 The complexation of calcium to amino acid carboxylate groups has been observed in aqueous systems and may potentially occur in natural systems with elevated dissolved Ca2+ concentrations.5−7 The selection and concentration of such metal−ligand complexes at the mineral−water interfaces present within these environments could have led to the polymerization of primordial CaBPs as a crucial process in the emergence of complex biochemistry in early life. The formation of macromolecules, such as CaBPs, on early Earth could have occurred contemporaneously with the synthesis of constituent amino acids, which have been demonstrated to form abiotically within natural environments as well as under laboratory settings simulating prebiotic conditions that include hydrothermal systems.8−11 In these systems, amino acids have been characterized among a © XXXX American Chemical Society
complex suite of other biomolecules, and the process of concentrating any one species of amino acid in a mixture of organic species within a diluting aqueous environment is challenging. One possible scenario involves the attachment of amino acids at the surfaces of minerals in a geochemical environment, where the amino acids might concentrate and polymerize at the mineral−water interface.12−14 The mineral surface undergoes protonation or deprotonation reactions, depending upon the pH of the aqueous environment relative to the point of zero charge (PZC) of the mineral or the pH at which the mineral surface is net-neutral.14−18 The extent of amino acid adsorption onto mineral surfaces generally correlates with the difference between the PZC and a corresponding property for amino acids, the isoelectric point (pI). For instance, the mineral calcite (PZC = 9.5) adsorbs aspartate (pI = 2.98) to a greater extent than lysine (pI = 9.74) Received: Revised: Accepted: Published: A
June 14, 2018 November 15, 2018 November 19, 2018 November 19, 2018 DOI: 10.1021/acsearthspacechem.8b00081 ACS Earth Space Chem. XXXX, XXX, XXX−XXX
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ACS Earth and Space Chemistry
might have in promoting selection and greater complexity among prebiotic molecules.
because negatively charged, aqueous aspartate is electrostatically attracted to the positively charged calcite surface over the pH range of 3.0−9.5.19 The electrostatic environment at the mineral−water interface could, therefore, adsorb and concentrate one charged biomolecule, whereas another is repelled. Divalent cations may substantially change the adsorption behavior of biomolecules at mineral surfaces. Lee and colleagues20 determined that the surface of rutile (TiO2) became more positively charged at alkaline pH conditions as a result of the adsorption of the Ca2+ ion at the mineral surface. As a consequence, the negatively charged amino acid glutamate adsorbed onto the surface of rutile in significant amounts in the presence of the Ca2+ ion at alkaline pH conditions in contrast to experiments in which no calcium was added. Franchi and co-workers21 investigated the interaction of nucleic acids on kaolinite and montmorillonite surfaces and observed that adsorption increased significantly in the presence of the divalent cations Mg2+ and Ca2+. The authors attributed the increase in adsorption to the formation of a cation−ligand complex, where the M2+ cation acted as a bridge between the clay surface and the nucleic acid. Similarly, our previous investigations of brucite [Mg(OH)2] revealed that the surface adsorption of aspartate and ribose was enhanced in the presence of Ca2+.22,23 We used a surface complexation model to predict that a cooperative calcium−aspartate complex adsorbs at the brucite−water interface via a “cation-bridge” configuration.22 In the previous study of the brucite−water interface, we used a surface complexation model to calculate the particle surface charge or ζ potential of the brucite surface with and without the presence of CaCl2. Consequently, we concluded that the surface charge increased in the presence of CaCl2 and predicted that more negative amino acids, such as aspartate, would preferentially adsorb onto brucite in comparison to a positively charged amino acid, such as lysine, when CaCl2 was added to the brucite surface. In this study, we tested this prediction by investigating the adsorption of aqueous solutions of the five amino acids aspartate, glycine, lysine, leucine, and phenylalanine in equimolar mixtures in the presence of brucite with and without CaCl2. These five amino acids were chosen because they have a wide range of pI values (between 2.98 and 9.7419) relative to the estimated PZC of brucite of 10.5.22 Furthermore, we tested the accuracy of the calculations made by the previously established surface complexation model by making electrophoretic mobility measurements of the brucite surface. Brucite is a major alteration product of serpentinization, which occurs at alkaline hydrothermal vent systems.24 It has been hypothesized that the emergence of life may have occurred at alkaline hydrothermal environments.25,26 However, the interaction between prebiotic molecules, such as amino acids, and products of serpentinization are not wellcharacterized. We evaluated the attachment of the amino acids onto brucite with batch adsorption experiments to determine whether selective adsorption of individual amino acids may be amplified with the presence of dissolved calcium, which is abundant in alkaline hydrothermal vent systems.27 It was also possible that competitive adsorption might occur between the amino acids, and the addition of calcium might enhance those effects. We used the batch adsorption experiments to evaluate the possible role that mineral surfaces, in particular, mineral surfaces in hydrothermal vent systems,
2. MATERIALS AND METHODS 2.1. Batch Adsorption Experiments. We performed batch adsorption experiments with a synthetic brucite powder as described in previous publications.22,23 We determined a total surface area of 17.6 m2/g of brucite with the multipoint Brunauer−Emmett−Teller (BET) N2 method (Micromeritics, Norcross, GA, U.S.A.). We measured the surface area that was specific to the edge surfaces of brucite (1.9 m2/g) with lowpressure Ar adsorption performed at the Laboratoire Interdisciplinaire des Environnements Continentaux (Vandœuvre les Nancy, France) using methods previously published.22 We made equimolar mixtures of aspartate, glycine, lysine, leucine, and phenylalanine at four concentrations of 10, 50, 75, and 150 μM, resulting in total amino acid concentrations of 50, 250, 375, and 750 μM, respectively. Brucite buffered the pH of each sample to approximately 10.2. The corresponding amount of Mg2+ that dissolved from the brucite surface ranged from 0.9 to 1.1 mM according to the dissolution equation Mg(OH)2 + 2H+ = Mg 2 + + 2H 2O
(1)
where the brucite powder is assumed to reach equilibrium with the aqueous solution after 24 h. We determined the equilibrium constant for this batch of synthetic brucite in a previous adsorption study, where log K = 17.30 ± 0.06.22 We conducted the batch adsorption experiments for a second set of experiments with 4.1 mM CaCl2 (Fluka Analytical). We conducted adsorption experiments with equimolar amino acid mixtures in the presence of CaCl2 in triplicate concurrently with the experiments without CaCl2 to ensure the reproducibility of the results. We determined the concentration of the five amino acids, Mg2+ ion dissolved from brucite, and CaCl2 in the supernatant with ion chromatography (IC). We used a Dionex ICS-5000 system described previously22 to determine the amino acid and Mg2+ and Ca2+ ion concentrations. The amount of amino acid or calcium adsorption (Γads, μmol m−2) was calculated with the equation Γads =
[X ]0 − [X ]eq CsA s
(2)
where Cs is the solid loading of the mineral and As is the edge surface area of brucite. We ran the samples in triplicate and determined the mean concentration of aspartate, glycine, lysine, leucine, and phenylalanine remaining in the liquid supernatant within ±1 standard error (σM). It was necessary for us to analyze the samples containing amino acids in triplicate because we initially detected low amounts of adsorption (10%), and we calculated that ±1 standard deviation (σ) was equal to about 8% of the adsorption data. In addition to carrying out the experiments described above, we performed blank adsorption experiments, where equimolar mixtures of 10, 50, 75, and 150 μM aspartate, glycine, lysine, leucine, and phenylalanine were added to Falcon tubes without B
DOI: 10.1021/acsearthspacechem.8b00081 ACS Earth Space Chem. XXXX, XXX, XXX−XXX
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Table 1. Characteristics of Brucitea and Modified ETLM Parameters for Proton and Electrolyte Adsorption onto Brucite reaction type surface equilibria
hypothetical 1.0 m standard state
log K01
>SOH + H+ = >SOH 2+
log
K02
log K, modified
reaction
−
9.7
+
>SO + H = >SOH +
−
+
+
log K0Na+
>SOH + Na = >SO _Na + H
log K0Cl−
>SOH + Cl− + H+ = >SOH 2+_Cl−
log
K0>SOH2+__Ca(OH)2 b
>SOH + Ca
2+
+
+ 2H 2O = >SOH 2 _Ca(OH)2 + H
+
surface equilibria
site-occupancy standard state
log Kθ>SOH2+_Ca(OH)2
>SOH 2+ + Ca 2 + + 2H 2O = >SOH 2+_Ca(OH)2 + 2H+
log K, original22 9.6
11.3
11.4
−8.8
−9.0
11.6
11.8
−6.7
−5.2
−16.4 (±0.3)
−14.5 (±0.3)
Brucite properties are Ns = 38 sites/nm , As = 3.8 m /g, C1 = 190 μF/cm , C2 = 190 μF/cm , pHPZC = 10.5, = 1.28, log Kθ1 = 9.86, log Kθ2 = 11.14, log KθNa+ = −8.64, log KθCl− = 11.76, where Ns is the site density and C1 and C2 are capacitances. bEquilibrium constants relative to siteoccupancy standard states were calculated using the equation: log Kθ>SOH2+_Ca(OH)2 = log K0>SOH2+__Ca(OH)2 + log NsAs/100 − pHPZC + ΔpKθn/2. a
2
2
2
2
ΔpKθn
Figure 1. Average adsorption (μmol m−2) of aspartate (blue diamonds), glycine (green squares), lysine (red circles), leucine (orange triangles), and phenylalanine (inverted purple triangles) onto brucite as a function of the initial concentration of each amino acid in an equimolar mixture following three batch experiments with (a) no CaCl2 and (b) CaCl2 added at pH 10.2. Vertical error bars represent the standard error calculated from all adsorption values.
equimolar solutions of the five amino acids with and without 4 mM CaCl2. We calculated ζ potentials from electrophoretic mobility using the Smoluchowski equation. We determined a total of eight ζ-potential measurements for each sample and calculated an averaged value from these measurements with a corresponding standard deviation value. 2.3. Surface Complexation Modeling. In a previous study, we characterized the surface of our synthetic brucite powder and the attachment of aspartate to its surface with batch adsorption experiments and a predictive model that uses Born solvation and crystal chemical theory known as the extended triple-layer model (ETLM).22,28−30 The ETLM predicts the electrical work resulting from the release of water dipoles during the adsorption of a species directly at the mineral surface. In this study, we investigated the ability of the previously published model to predict amino acid adsorption behavior and new measurements of ζ potential at the brucite surface. In the course of making these comparisons, we also created a modified ETLM of the brucite surface that better fit the available data. We used the software GEOSURF31 to iteratively predict calcium surface adsorption and brucite ζ potential using the parameters in Table 1. These parameters
brucite powder. We increased the initial pH of the amino acid mixtures to approximately 10.2 with small volumes of 0.1 M NaOH. We conducted the experiments without CaCl2 and with approximately 4 mM CaCl2. The purpose of these experiments was to evaluate whether or not a difference could be detected between the initial concentration and the concentration after 24 h as a result of either polymerization at alkaline conditions or the formation of complexes between the multiple amino acid species. We analyzed the solutions with IC after they had mixed over 24 h, and we found that the concentrations in the solutions were equal to the initial concentrations for each amino acid (see Table S-1 of the Supporting Information). 2.2. ζ-Potential Measurements. We determined ζ potential (mV) of the brucite−water interface by measuring electrophoretic mobility of the surface with a NanoBrook ZetaPALS ζ-potential analyzer (Brookhaven Instruments Corporation). This ζ-potential analyzer determined electrophoretic mobility using phase analysis light scattering, and as a sample requirement, brucite suspensions needed to transmit light. Therefore, we prepared brucite suspensions containing loadings of brucite of 1 g/L with between 10 and 150 μM C
DOI: 10.1021/acsearthspacechem.8b00081 ACS Earth Space Chem. XXXX, XXX, XXX−XXX
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where “>SOH” denotes the brucite surface and the calcium complex interacts at the outer sphere of the brucite−water interface. Although calcium hydrolysis likely does not occur to any significant extent in the aqueous phase alone, we have predicted that the hydrated calcium species is the predominant adsorbing species at the brucite surface. After iteratively fitting the calcium adsorption data with other potential calcium surface species (e.g., >SO−_Ca2+), we determined that the adsorption data predicted by the reaction stoichiometry in eq 3 best fit the experimental data. Moreover, previously published experimental studies involving the adsorption of CaCl2 on the same batch of synthetic brucite powder have determined the same adsorption reaction.22,23 Hydrated calcium species, such as Ca(OH)+, have been previously predicted to form at the surfaces of minerals at a wide range of pH conditions.20,32 Indeed, previous works have predicted species that form at the mineral−water interface might not otherwise exist in significant concentrations in the aqueous phase.15,17,23 The formation of such species may be a unique property of the mineral surface environment. Previous observations of biomolecule attachment at the solid−water interface have found that electrostatic attraction plays a significant role.17,19,20 Thus, we determined the ζ potential of the brucite−water interface in the presence of the five amino acids both with and without CaCl 2 with electrophoretic mobility measurements. We observed that, at a pH of 10.2, the brucite surface has a slightly positive charge at all amino acid concentrations when no CaCl2 is added to the system (Figure 2). This result indicates that the PZC of brucite
include the equilibrium constants for surface protonation and deprotonation, electrolyte adsorption, and calcium adsorption reactions, and a further discussion of how these values were altered from those in the previously published ETLM is provided below.
3. RESULTS AND DISCUSSION The average amount of surface adsorption following three batch adsorption experiments for aspartate, glycine, lysine, leucine, and phenylalanine onto brucite as a function of the amino acid initial concentration without CaCl2 and an average of 0.9 mM Mg2+ that dissolved from the brucite surface is displayed in Figure 1a. Amino acid adsorption is illustrated as an adsorption isotherm. Glycine, lysine, leucine, and phenylalanine adsorbed onto brucite in comparable amounts at all of the investigated initial amino acid concentrations. At initial concentrations of 10 μM, between 0.014 and 0.021 μmol m−2 of the four amino acids attached onto brucite. This amount increased with the amino acid concentration, and when 150 μM of each amino acid was added, we observed between 0.37 and 0.42 μmol m−2 adsorption. In contrast, aspartate adsorbed in amounts ranging between 0.028 and 0.71 μmol m−2 when 10 and 150 μM were added to the brucite surface, respectively. All adsorption data are reported in Table S-2 of the Supporting Information. In the presence of CaCl2 and an average of 1.1 mM Mg2+, the amount of aspartate adsorption was between 0.20 and 1.63 μmol m−2 when the initial aspartate concentration was between 10 and 150 μM, respectively (Figure 1b). This amount of aspartate adsorption was between 2 and 7 times higher than that observed in the experiments without calcium added. The amount of glycine, lysine, leucine, and phenylalanine adsorption in the presence of CaCl2 was approximately 0.015 μmol m−2 when 10 μM of each amino acid was added to brucite. We observed between 0.17 and 0.28 μmol m−2 of the four amino acids attached onto brucite when initial concentrations of 150 μM were added with calcium. This amount of adsorption is lower than the amount that we observed in experiments without calcium added. More significantly, as demonstrated by Figure 1, the contrast between aspartate adsorption and the adsorption of the other four amino acids is significantly more pronounced in experiments with calcium. When calcium is added to a mixture of amino acids and the brucite surface, aspartate adsorption is between 6 and 12 times greater than the other amino acids in the mixture. In addition to amino acids, we observed that up to 15.9% of the initial 4.1 mM calcium adsorbed onto the brucite surface. This amount did not vary more than 0.6% with the initial amino acid concentration. In contrast to amino acid adsorption, which occurred in amounts of up to 2.58 μmol m−2, we calculated that an average of 34.31 ± 1.24 μmol m−2 calcium adsorbed onto the brucite surface. We previously observed comparable amounts of calcium adsorption (i.e., 29.6 ± 2.3 μmol m−2) with 4.0 mM CaCl2 added to brucite.22 In that study, we fitted calcium adsorption data with the ETLM, which indicated that calcium adsorbed onto brucite with the reaction stoichiometry
Figure 2. ζ potential (mV) measured as a function of the total amino acid concentration with and without CaCl2 at pH 10.2. Dotted lines represent ETLM-modeled fits to the observed data. Vertical error bars represent standard deviations taken from ζ-potential measurement runs.
is slightly above 10.2 and the presence of more positively charged functional groups at the experimental pH would adsorb negatively charged aspartate in greater amounts compared to less polar and less negative amino acids, such as glycine and lysine. The adsorption of the amino acids at the brucite surface is also pH-dependent because the charge of the mineral surface is related to the pH of the aqueous phase and the PZC of the brucite surface. The pI of aspartate is 2.98,19 whereas the PZC of brucite is slightly above 10.2. Therefore, in
>SOH + Ca 2 + + 2H 2O = >SOH 2+_Ca(OH)2 + H+ (3) D
DOI: 10.1021/acsearthspacechem.8b00081 ACS Earth Space Chem. XXXX, XXX, XXX−XXX
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surface area is available than previously measured or calculated by both the low-pressure Ar adsorption and BET methods. The increase in ζ potential with CaCl2 was previously attributed to the formation of the positively charged calcium complex at the brucite surface, which was predicted to favor the adsorption of negatively charged molecules over positively charged molecules. The results of the adsorption study with the five amino acids demonstrate that this prediction was correct. Aspartate (pI = 2.98) adsorbs significantly more than lysine (pI = 9.74) but also more than glycine (pI = 6.06), leucine (pI = 5.98), and phenylalanine (pI = 5.48) when CaCl2 is present at the brucite surface.19,33 The general correspondence between the previously modeled predictions and observations of amino acid adsorption indicates that surface complexation models, such as the ETLM,28 can successfully describe the adsorption behavior of organic molecules on mineral surfaces. The significant adsorption of aspartate in comparison to the other four amino acids illustrates that amino acid speciation plays a fundamental role in surface adsorption. The amino acids glycine, leucine, and phenylalanine each have similar pI values but significantly different functional groups. Nonetheless, there was no observable difference in the extent of surface adsorption of these three amino acids both with and without CaCl2 added to brucite, which could be attributed to the configuration of the amino acid relative to the brucite surface. In contrast, at the investigated pH of 10.2, aspartate was the most negatively charged among the five amino acids that we added to brucite. It has been previously predicted that aspartate forms a strong electrostatic bond with the Ca2+ ion, which results in a metal−ligand complex at the brucite surface.22 Aspartate−calcium complexes can be both neutral (CaAsp0) and positively charged (CaHAsp+) in water. In contrast, calcium complexes with the other four amino acids can only be positively charged, which might limit their adsorption onto brucite. For instance, an experiment by Yang and co-workers determined that the Ca2+ ion competitively adsorbed in the presence of lysine and, furthermore, caused the desorption of the amino acid from the montmorillonite surface.34 Moreover, both calcium and aspartate adsorbed in significant amounts, resulting in decreased availability of surface sites for the attachment of other amino acids. This competitive effect might account for the limited adsorption of glycine, lysine, leucine, and phenylalanine onto brucite with added CaCl2.
the pH range between 2.98 and 10.2, we would expect negatively charged aspartate to be electrostatically attracted to the positively charged brucite surface. Moreover, this electrostatic attraction should be stronger than that of the other four amino acids, which have higher pI values. The observation of positively charged ζ potential at the brucite surface contrasts with a prediction made by the previously published model of brucite that the measurements would be slightly negatively charged.22 We modified the parameters of the existing ETLM such that the model could better fit the ζ-potential measurements. As a consequence, we found that it was necessary to decrease the point of zero salt effect (PZSE), which is largely affected by the hypothetical input of 0.001 M NaCl and is defined as the equilibrium constant of the reaction >SOH 2+_Cl− + Na + = >SO−_Na + + Cl− + 2H+
(4)
The PZSE was previously 10.4 and was shifted downward to 10.2. We also made small alterations to the equilibrium constants affecting brucite surface protonation and deprotonation, and as a result, ΔpKn, which is determined from the equilibrium constant of the reaction >SO− + >SOH 2+ = 2>SOH
(5)
shifted from 2.08 in the previous model to 1.28. Additionally, we made predictions with the presence of the five amino acids, the properties of which are given in Table S-3 of the Supporting Information. These alterations to the existing ETLM made it possible for the model to predict slightly positive ζ-potential values at pH 10.2, which reflect the observed data. We determined that brucite ζ potential increased to more positive values at all initial amino acid concentrations with the addition of CaCl2 (Figure 2). Although, in comparison to the measured ζ-potential values, those predicted by the previously published ETLM in the presence of CaCl2 were higher,22 both the predicted and measured values determined that the ζ potential of brucite increased with CaCl2. After iteratively fitting the model with the measured data using different parameters, we determined that the ETLM could better correspond to both the calcium adsorption data and the ζpotential values measured with CaCl2 only if we considered a larger value for surface area. We measured an edge surface area of 1.9 m2/g and calculated a basal surface area of 15.7 m2/g but considered only the edge surface area in our calculations as a result of the protonation of the basal surface sites.22 However, we did not consider the surface area that might be made available from brucite dissolution in water (eq 1) as well as the number of basal surface sites that may be able to participate in reactions as a result of surface defects. If we considered an active surface area of 3.8 m2/g, it was possible to predict 15.6% calcium adsorption (in comparison to a measured 15.9%) and fit the measured ζ-potential values (Figure 2). In contrast, the original ETLM calculated 12.6% calcium adsorption and overpredicted the ζ potential in the presence of CaCl2 by 30 mV. These predictions with the higher active surface area were also made with a lower equilibrium constant for eq 3 than has been previously established (see Table 1). The increase in active surface area by a factor of 2 relative to the previous model may reflect the uncertainty in broadly categorizing the basal brucite surface as unreactive. It is also possible that, once exposed to water, the surface dissolves and a greater amount of
4. CONCLUSION Our observation of competitive and cooperative adsorption effects demonstrates that the dissolved ion composition of the aqueous environment combined with mineral surfaces can influence the availability of biomolecules. The preferential adsorption of aspartate from a mixture onto a mineral−water interface in the presence of dissolved Ca2+ could be significant for the evolution of CaBPs, which notably contain negatively charged amino acids bound to calcium.6,35 Hazen and Sverjensky18 suggest that, to evaluate the emergence of complex molecules, such as CaBPs, it is necessary to conduct experiments that attempt to reproduce prebiotic complexities (e.g., multiple organic species, ligand concentrations, and electrolytes). We focused on the addition of CaCl2 as a first step in approaching complex geochemical conditions while assessing molecular interactions at the mineral surface. Molecular self-organization may emerge within a system as E
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(4) Barnwal, R. P.; Jobby, M. K.; Devi, K. M.; Sharma, Y.; Chary, K. V. Solution Structure and Calcium-Binding Properties of MCrystallin, a Primordial βγ-Crystallin From Archaea. J. Mol. Biol. 2009, 386 (3), 675−689. (5) De Robertis, A.; De Stefano, C.; Gianguzza, A. Salt Effects on the Protonation of L-Histidine and L-Aspartic Acid: A Complex Formation Model. Thermochim. Acta 1991, 177, 39−57. (6) Fox, S.; Büsching, I.; Barklage, W.; Strasdeit, H. Coordination of Biologically Important α-Amino Acids to Calcium(II) at High pH: Insights From Crystal Structures of Calcium α-Aminocarboxylates. Inorg. Chem. 2007, 46 (3), 818−824. (7) Kurochkin, V. Y.; Chernikov, V. V.; Orlova, T. D. The Thermodynamic Characteristics of Complex Formation Between Calcium Ions and L-Leucine in Aqueous Solution. Russ. J. Phys. Chem. 2011, 85 (4), 598−602. (8) Miller, S. L. A Production of Amino Acids Under Possible Primitive Earth Conditions. Science 1953, 117 (3046), 528−529. (9) Cleaves, H. J., II; Chalmers, J. H.; Lazcano, A.; Miller, S. L.; Bada, J. L. A Reassessment of Prebiotic Organic Synthesis in Neutral Planetary Atmospheres. Origins Life Evol. Biospheres 2008, 38 (2), 105−115. (10) Hennet, R.; Holm, N. G.; Engel, M. H. Abiotic Synthesis of Amino-Acids Under Hydrothermal Conditions and the Origin of Life: A Perpetual Phenomenon. Naturwissenschaften 1992, 79 (8), 361− 365. (11) Ménez, B.; Pisapia, C.; Andreani, M.; Jamme, F.; Vanbellingen, Q. P.; Brunelle, A.; Richard, L.; Dumas, P.; Réfrégiers, M. Abiotic Synthesis of Amino Acids in the Recesses of the Oceanic Lithosphere. Nature 2018, DOI: 10.1038/s41586-018-0684-z. (12) Goldschmidt, V. M. Geochemical Aspects of the Origin of Complex Organic Molecules on the Earth, as Precursors to Organic Life. New Biol. 1952, 12, 97−105. (13) Hazen, R. M. Presidential Address to the Mineralogical Society of America, Salt Lake City, October 18, 2005: Mineral Surfaces and the Prebiotic Selection and Organization of Biomolecules. Am. Mineral. 2006, 91 (11−12), 1715−1729. (14) Cleaves, H. J., II; Michalkova Scott, A.; Hill, F. C.; Leszczynski, J.; Sahai, N.; Hazen, R. M. Mineral−Organic Interfacial Processes: Potential Roles in the Origins of Life. Chem. Soc. Rev. 2012, 41 (16), 5502−5525. (15) Jonsson, C. M.; Jonsson, C. L.; Sverjensky, D. A.; Cleaves, H. J., II; Hazen, R. M. Attachment of L-Glutamate to Rutile (α TiO2): A Potentiometric, Adsorption, and Surface Complexation Study. Langmuir 2009, 25 (20), 12127−12135. (16) Sverjensky, D. A.; Sahai, N. Theoretical Prediction of SingleSite Surface-Protonation Equilibrium Constants for Oxides and Silicates in Water. Geochim. Cosmochim. Acta 1996, 60 (20), 3773− 3797. (17) Jonsson, C. M.; Jonsson, C. L.; Estrada, C. F.; Sverjensky, D. A.; Cleaves, H. J., II; Hazen, R. M. Adsorption of L-Aspartate to Rutile (α-TiO2): Experimental and Theoretical Surface Complexation Studies. Geochim. Cosmochim. Acta 2010, 74 (8), 2356−2367. (18) Hazen, R. M.; Sverjensky, D. A. Mineral Surfaces, Geochemical Complexities, and the Origins of Life. Cold Spring Harbor Perspect. Biol. 2010, 2 (5), a002162. (19) Churchill, H.; Teng, H.; Hazen, R. M. Correlation of pHDependent Surface Interaction Forces to Amino Acid Adsorption: Implications for the Origin of Life. Am. Mineral. 2004, 89 (7), 1048− 1055. (20) Lee, N.; Sverjensky, D. A.; Hazen, R. M. Cooperative and Competitive Adsorption of Amino Acids with Ca2+ on Rutile (αTiO2). Environ. Sci. Technol. 2014, 48 (16), 9358−9365. (21) Franchi, M.; Ferris, J. P.; Gallori, E. Cations as Mediators of the Adsorption of Nucleic Acids on Clay Surfaces in Prebiotic Environments. Origins Life Evol. Biospheres 2003, 33 (1), 1−16. (22) Estrada, C. F.; Sverjensky, D. A.; Pelletier, M.; Razafitianamaharavo, A.; Hazen, R. M. Interaction Between LAspartate and the Brucite [Mg(OH)2]−Water Interface. Geochim. Cosmochim. Acta 2015, 155, 172−186.
biomolecules are selectively adsorbed and concentrated at the mineral−water interface, whereas other organic species remain dilute within bulk water.18 An alkaline hydrothermal system may play a role in this process because we have observed dissolved calcium promoting the adsorption of negatively charged amino acids among a mixture of other amino acids onto the brucite−water interface. The selective pressure exerted by the brucite surface during the addition of CaCl2 may hold implications for the transition between a dilute, unorganized “prebiotic soup” to a concentrated, systematic suite preceding molecular evolution.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsearthspacechem.8b00081.
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Amino acid control experimental data (Table S-1), amino acid adsorption data (Table S-2), and aqueous amino acid properties (Table S-3) (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Charlene F. Estrada: 0000-0002-4824-8940 Present Address †
Charlene F. Estrada: School of Earth and Space Exploration, Arizona State University, 781 East Terrace Mall, Tempe, Arizona 85287, United States. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank Cécile Feuillie, Namhey Lee, Alyssa K. Adcock, Jihua Hao, Manuel Pelletier, Angélina Razafitianamaharavo, Timothy Strobel, Dionysis Foustoukos, George Cody, Paul Goldey, John Armstrong, Adrian Villegas-Jimenez, Stephen Hodge, Steven Coley, Paul Westeroff, and Xiangyu Bi for their invaluable expertise and advice throughout this project. The authors also thank the three anonymous reviewers for their comments in significantly improving this manuscript. This research was supported by the Deep Carbon Observatory, Johns Hopkins University, and the Carnegie Institution for Science and funded by grants from the National Science Foundation (EAR-1023865 to Dimitri A. Sverjensky and EAR1023889 to Robert M. Hazen) and the U.S. Department of Energy (DE-FG02-96ER-14616).
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