Spontaneous Polymerization of Glycine under Hydrothermal

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Spontaneous polymerization of glycine under hydrothermal conditions Ulysse Pedreira-Segade, Jihua Hao, Gilles Montagnac, Hervé Cardon, and Isabelle Daniel ACS Earth Space Chem., Just Accepted Manuscript • DOI: 10.1021/ acsearthspacechem.9b00043 • Publication Date (Web): 12 Jul 2019 Downloaded from pubs.acs.org on July 22, 2019

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ACS Earth and Space Chemistry

Title: Spontaneous polymerization of glycine under hydrothermal conditions Authors: Ulysse Pedreira-Segade1*†, Jihua Hao1, Gilles Montagnac1, Hervé Cardon1, Isabelle Daniel1 Author affiliation:

1

Univ Lyon, Ens de Lyon, Université Lyon 1, CNRS, UMR 5276 LGL-

TPE, F-69342, Lyon, France *Corresponding author: [email protected] †

Now at Department of Earth and Environmental Sciences, Rensselaer Polytechnic Institute,

110 8th Street, Troy, NY, USA. Keywords: Origins of life, glycine polymerization, in situ Raman spectroscopy, diamond anvil cell, hydrothermal conditions.

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Abstract (189/250 words) The abiotic polymerization of nucleotides and amino acids is a prerequisite for the emergence of life. It has been proposed that hydrothermal conditions might favor the polymerization of amino acids. In the present study, we analyzed by in situ Raman spectroscopy in a diamond anvil cell the fate of the simplest and most abundant amino acid, glycine, under hydrothermal conditions at 200°C and pressures ranging between 50 and 3,500 MPa. We also tested the effect of magnetite on the reactivity of glycine. The polymerization of glycine is highly favored under pressure and in the presence of magnetite. Linear dimers are more abundant than the cyclic ones up to a threshold pressure of 500 MPa. Above 800 MPa, amino acids stop reacting and the system is ‘frozen’. Our findings suggest that pressure and mineral-water interface strongly favor the formation of linear peptides. The optimum conditions for polymerization obtained in the present study suggest that the prebiotic chemical evolution of amino acids was not restricted to hydrothermal vents at oceanic ridges but might also occur much deeper in the first 15-30 km of the crust, widely expanding the prebiotic reactive zone.

1. Introduction The abiotic polymerization of amino acids is surely a mandatory stage in the chemical evolution leading to the emergence of life. Whether proteins or genetic information were first is still a matter of debate. Nevertheless, the formation of oligopeptide is among the first steps towards increased chemical complexity, emergence of enzymatic activity and first metabolic pathways. The availability and low concentration of amino acids in natural environment is often presented as a major impediment to their subsequent polymerization

1,2.

Yet, amino

acids were very likely present in the primitive environment. They are abundant in meteorites and the coma of small icy bodies

3,4.

Their synthesis was observed in interstellar ice analogs 2

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5,

shock experiments reproducing extra-terrestrial impacts

9–12.

6–8,

and hydrothermal experiments

Their abiotic hydrothermal production was recently confirmed in natural systems

13.

Hence, amino acids could have been dissolved in the primitive ocean through extraterrestrial delivery, shock chemistry and hydrothermal abiotic formation. The large volume of the primitive ocean however precluded high concentration of amino acids and their polymerization would have been thermodynamically unfavorable due to the hydrolysis of the peptide bond. The polymerization reaction is intrinsically a dehydration reaction. Therefore, several authors proposed polymerization mechanisms under a variety of conditions including high temperature, closed dry systems, dry-wet cycles or impregnated minerals yielding high amounts of oligomers and in some cases long chains of peptides

14–28.

Such experimental

conditions refer to lakes, lagoons or tidal flats as potential natural environments for the emergence of life. Nonetheless, the relevance of such environments is still a matter of debate. The Hadean and early Archean Earth was certainly a wet world, with less than 5% dry land

29,30,

on which the photolysis induced by UV radiations and the large scale

sterilization due to the meteoritic bombardment would have greatly limited the survivability of oligomers and more generally prebiotic building blocks 31. First proposed by Corliss et al., hydrothermal systems have often been considered as plausible geochemical environments for the abiotic formation and concentration of complex molecules, and ultimately the origin of life

32.

Temperatures higher than 100°C favor the

formation of peptide bond and activate the molecules, in both dry and aqueous conditions 11,33.

Consequently, many studies investigated hydrothermal conditions suitable for the

polymerization of the simplest and most abundant amino acid, i.e. glycine, though unsuccessfully

34–49.

They used a wide variety of methods to reach hydrothermal conditions

ranging from static closed systems to dynamic flow-through experiments. The hydrothermal conditions explored spanned over a large range of temperatures (150 to 400°C) and pressures (0.1 to 100 MPa), with highly variable heating times of a few seconds to >20 days, 3 ACS Paragon Plus Environment


with or without heating/quenching cycles, and in the presence or absence of minerals. None of these studies reported high yields of oligomers, and the major reaction product was systematically the cyclic dimer 2,5-diketopiperazine (DKP). DKP is a very stable molecule and a dead-end product of polymerization

50.

In addition, thermal degradation of monomers

was found to be a major drawback for the accumulation of oligomers under hydrothermal conditions. Finally, possible catalytic effects of the materials used for the reactors, concerns on reaching steady state conditions and the need of quenching for ex situ analyses lead several authors to question the validity of the results 35,43–45. Some limitations might be overcome using in situ analytical methods. To the best of our knowledge, only one study was carried out in situ under restricted hydrothermal conditions at 150°C and 2 MPa

44.

In the present study, we analyzed in situ the fate of glycine and its

polymers under hydrothermal conditions at 200°C and for pressures between 50 and 3,500 MPa, using Raman spectroscopy coupled to a diamond anvil cell. We also evaluated the effect of magnetite, which is a common accessory mineral in oceanic hydrothermal systems, on the reactivity of glycine. Our study is the first of its kind focusing on the effects of pressure and minerals on the chemical evolution of glycine under hydrothermal conditions. We measured the ratio of linear over cyclic dimers formed as a function of time and pressure and could assess favorable conditions for the formation of longer peptides.

2. Materials and methods 2.1. Chemicals. Glycine (Gly, C2H5NO2 >99%), diglycine (Gly2, C4H8N2O3 >99%) and glycine anhydride (DKP, C4H6N2O2 99%) were purchased from Sigma Aldrich® and dissolved in pure water (18 MΩ cm) without additional treatment (see Figure S1 for the chemical structures of these compounds). 2.2. Magnetite was purchased from Sigma Aldrich® as an iron(II,III) oxide. It was hydrothermally aged to remove surface oxidation in a stainless steel reactor with Ar-bubbled 4 ACS Paragon Plus Environment

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pure water at 150°C for 3 days. Purity, chemistry, structure and specific surface areas were checked before and after the treatment. Textural analysis was carried out by Micromeritics Analytical Services (Norcross, GA, USA) on a TriStar II 3030 with low pressure N2 adsorption at 77K. Specific surface area of unaged and aged magnetite were calculated using the MicroActive for TriStar II Plus v 2.02, with the multi-point BET method. Aged magnetite exhibits a specific surface area of 5.8 m²/g. XRD powder diffraction (Bruker D2 Phaser), SEM imaging coupled with EDS (JEOL 8500F) and TEM analysis coupled with EELS (Philips EM 420 TEM) revealed that aged magnetite was pure and free of surface oxidation layers. The grains are mainly needle, cubic and sheet-like particles of an average size of 100 nm. 2.3. Raman spectra were collected on a confocal LabRam HR800 micro-Raman spectrometer (Horiba Jobin-YvonTM) of 800 mm focal length. A holographic grating of 1800 tr.mm-1 was used to reach a spectral resolution of 0.3 cm-1 on a Peltier-cooled front illuminated CCD detector (1024x256 pixels). The excitation line at 532.5 nm was produced by a Quantum TorusTM 400 laser, with a power of 20 mW at the sample. The laser and backscattered Raman signal were focused through a MitutoyoTM 50x long working distance objective (0.42 N.A.). This optical configuration ensured a spatial resolution close to the micrometer. Raman spectra were visualized and selected using FitykTM (v0.9.8,

51).

On

selected spectra, the baseline was subtracted and Voigt profiles least-square fitting procedure was used on PeakfitTM (v4.12). 2.4. Hydrothermal conditions were reached using membrane-type low (LP) and high pressure (HP) diamond anvil cells

52,53.

The reaction chamber was drilled in nickel (LP) or

stainless steel (HP) gaskets and covered with gold or platinum to prevent reaction with the sample. For the LP cell, a 380 µm hole was pierced in the 300-µm-thick inerted gasket (volume of the reaction chamber of 107 nl). For the HP one, the hole was 150 µm in diameter for a thickness of 100 µm (volume of the reaction chamber of 1.7 nl). The gaskets were sonicated in a H2O2 solution to prevent organic contamination. The amino acid solution was loaded in the reaction chamber using a sterile 1 ml syringe. The small volume of the reaction 5 ACS Paragon Plus Environment


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chamber makes it practically impossible to buffer the oxygen fugacity of the system. One to three ruby microspheres were added to monitor the sample pressure during the experiment 54.

Pressure was thus measured using the shift of the R1 fluorescence peak of ruby

55.

The

temperature dependence of this shift has been previously calibrated for the batch used for these experiments

56.

The internal pressure was increased and stabilized by pumping helium

gas into the membrane of the cell using an automatic pressure regulator (Sanchez technologies). The experimental apparatus was heated externally using a resistance-heating coil adjusted on the diamond anvil cell. The temperature was measured through a K-type thermocouple inserted in the cell and close to the sample. The cell was thermally isolated using ceramic covers in order to keep the automatically-controlled temperature stability at ± 0.5°C during the experiment. The experimental apparatus is depicted in Figure S2. 2.5. Reference spectra and calibrations. We prepared reference solutions of 1.5 M glycine, 1.5 M diglycine and 0.125 M DKP in pure water. Reference spectra of these compounds were acquired in sterile 2 ml glass vials at 25°C and ambient pressure at low (300-1800 cm-1) and high (2750-3100 cm-1) frequencies. These spectra could then be compared with reference spectra from the literature for vibrational assignment and purity (see Table S1; 64).

57–

Raman spectra for degradation products, gases and carbonates were also retrieved from

the literature (see Table S2 for a comparison between Raman bands of decomposition products and the glycine molecules;

65–69).

From the reference solutions we prepared

Gly:Gly2 mixed solutions with a 10 mol% step in Gly2 concentration (from 0 to 100 mol% Gly2). For Gly:DKP mixtures, we started with a step of 1 mol% from 0 to 10 mol% DKP, and used the same 10 mol% steps up to 100 mol% DKP. Calibration spectra (Figure S3) were acquired at 25°C and ambient pressure in the same 2 ml glass vials. Laser power, acquisition time, spectral range and spectral resolution were identical for every spectrum. Calibration spectra were processed on PeakfitTM software (v4.12). We selected a reduced range of 750 to 950 cm-1 and subtracted a linear baseline. Voigt profiles were used for the least-square fitting procedure. A total of four peaks were used to model the data: one peak


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was used for Gly, two for Gly2 and one for DKP, centered at 897 cm-1, 882 and 918 cm-1, and 797 cm-1, respectively. Plots and polynomial curve fittings (see Supplementary text) of the molar fractions of Gly2 and DKP as a function of the characteristic intensity ratios were then obtained using Kaleidagraph software (v3.6).

3. Results and discussion 3.1. In situ Raman analysis under hydrothermal conditions. We carried out fifteen hydrothermal experiments in which a solution of glycine (C2H5NO2, 2 mol/kg) was loaded in a diamond anvil cell

52,53

for experimental durations ranging between 6 and 65 hours. We used

either platinum or gold liners to prevent reaction between the fluid and the nickel or stainlesssteel gasket during hydrothermal treatment. The pressure range under consideration spans the conditions of primitive oceanic hydrothermal systems at a few kilometers below sea level up to more than 100 kilometers depth in cold subducting slabs

70.

To the best of our

knowledge, it is the first study to explore such a wide range of pressure conditions (see Figure S4). As presented in Figure 1A, Raman spectra measured throughout the experiment – before, during high temperature treatment, and after quenching – allowed us to evaluate the effects of pressure on the polymerization of glycine, the thermal stability of glycine and its reaction products for degradation, the stability of quenched products and the effect of a mineral surface. We focused on the dimerization step of the glycine polymerization (see Figure S1, and Supplementary text), as the concentration of longer oligomers would certainly be below detection limit of Raman spectroscopy. Dimerization is a fundamental step for the complexification of the system since it forms either the linear diglycine (Gly2) or the cyclic 2,5diketopiperazine (DKP). The ratio of linear over cyclic dimer (Gly2/DKP) is used to identify conditions favorable to linear polymerization.



After a custom calibration of the relative amount of dimers in solution, we used Raman intensities to calculate the molar fractions of Gly dimers, DKP and diglycine Gly2. As shown in Figure 1B, this in situ Raman analysis relies only on the accurate measurement of the Raman intensities of the characteristic vibrations of glycine, diglycine and DKP, at 897 cm-1, 918 cm-1 and 797 cm-1, respectively, carefully described in reference solutions. Figure S5 shows selected experimental data fitted with this three-component calibration and illustrates the method that was used to quantify the molar fractions of dimers DKP and Gly2 produced in all experiments (see Table S1, Figures S3, S5 and Supplementary text for more details).

3.2. Dimerization of glycine under hydrothermal conditions as a function of pressure and mineral presence. In all experiments leading to the dimerization of glycine, the characteristic Raman features of Gly2 and DKP readily appeared while increasing temperature between 150 and 200°C (Figure 1). Analysis of the evolution of the molar fraction of polymers with time showed that DKP and Gly2, once formed, remained stable throughout the experiment, even after quenching. The formation of polymers always happened in the first hour after reaching 200°C and remained stable after an initial oscillation, probably correlated with the thermal equilibration of the experimental apparatus. This oscillation was reduced in time and amplitude with increased initial pressure. Steady state was reached in one to six hours under hydrothermal conditions depending on pressure. More importantly, the quantity of products formed did not change with quenching, independently of the experimental duration. To achieve a better evaluation of the reaction yield, we used the Raman intensities measured after quenching, i.e. at ambient temperature but high pressure, to measure the molar fraction of DKP and Gly2 in experimental products. The molar fraction of dimers formed at 200°C during experiments is reported as a function of pressure in Figure 2 (see also Tables S3, S4 and Supplementary text for more details). The effect of the addition of magnetite to the solution is also displayed. We observed significant differences in the relative amount of products, solely depending on pressure 8 ACS Paragon Plus Environment

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(Figure 2 and Table S3). Dimers formed only below ca. 500 to 800 MPa. Above this critical pressure, glycine was stable; Raman spectra showed virtually neither thermal degradation nor polymerization whether magnetite was present or not in the system. Below 500 MPa, where the dimers formed, the hydrothermal conditions systematically favored the linear dimer Gly2. Up to 16 mol% of Gly2 formed at 380 MPa without magnetite. Not only did pressure favor the formation of linear polymer, it also decreased the production of DKP. The Gly2/DKP ratio was as high as 34.4 at 450 MPa in the absence of magnetite. The addition of magnetite favored even more linear dimerization and decreased its optimal pressure, with up to 16 mol% of dimer Gly2 at pressure as low as 140 MPa, and a Gly2/DKP ratio as high as 35.9 at 300 MPa only. After decades of efforts, the present experimental results are the first ones to reach such a high reaction yield, at least one order of magnitude higher than previous ones limited to lower pressure 28,36,37,41,46,49.

3.3. Stability of glycine and polymers under hydrothermal conditions. As many authors did, we again stress the importance of using inert materials in contact with the sample for the reactor as some metals enhanced the decomposition of glycine (e.g. stainless steel or nickel). Our carefully designed experimental set-up allowed to observe for the first time highly stable monomers and oligomers of glycine at 200°C, independently of experimental duration. It is likely due to the higher pressures investigated here compared to previous studies. Previous ex situ experiments have shown that, at peak temperatures above 200°C, the duration of the hydrothermal treatment directly impacted the survivability of organic molecules and thermal degradation continually depleted the system in glycine leading to the hydrolysis of polymers

36,43,49.

Only fast temperature-quenching cycles produced longer

polymers that could be preserved upon quenching

45,46.

This led some authors to claim the

need for highly dynamical natural environments as the cradle of life in order to cycle its building blocks through the hot regions of hydrothermal systems and the cold open ocean, thereby limiting or inhibiting thermal degradation of the oligomers. Yet, in the latter 9 ACS Paragon Plus Environment


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experiments, pressure was limited to seafloor or sub-seafloor conditions. In the present experiments, the higher pressure investigated clearly stabilized the amino acid and its dimers during hydrothermal treatment. Decarboxylation and deamination of glycine were definitely below the detection limit of our method. We never observed the characteristic intense Raman peaks of methylammonium, acetate, glycolate or formate (Figure S1, Table S2)

65–67.

We

also carefully looked for the final-stage degradation products CO2, CH4, NH3 and H2 68. These molecules are soluble at high pressure and high temperature and exsolve upon decompression. The exsolution of a gas phase containing CO2, CH4, NH3 and H2 has only been observed indeed in our lowest pressure experiments at 50 MPa. Overall, the lack of Raman signal typical of the degradation products of glycine together with the intense and stable signal to noise ratio of glycine ensured that degradation was negligible throughout our experiments at high pressure.

3.4. Contrasted effect of pressure. Here we describe a novel effect of pressure on amino acids. Below 500 MPa, polymerization of glycine is favored and thermal degradation is suppressed. In our experiments, Gly2 was produced in large amount with increasing pressure, with an optimal pressure around 450 MPa at 200°C. This favorable effect of pressure on glycine polymerization was intuited by many authors, even if most studies focused on the effect of temperature instead of pressure

14,15,24,34.

Moreover, although some

theoretical studies suggested that pressure might have a detrimental effect on the stability and preservation of amino acids and on the polymerization reaction

35,43,48,49,

our

polymerization achievements below 500 MPa are in good agreement with comprehensive thermodynamic calculations for the reactivity of pure glycine in water (Figure S6, S7)

33,71.

The models predict that pressure favors linear dimerization and minimize cyclization. Above the threshold pressure of 800 MPa, repeated experiments showed that the evolution of glycine is ‘frozen’ and that the amino acid neither reacts nor degrades. This might indicate that either pressure strongly slows down the reaction rate of glycine polymerization, or 10 ACS Paragon Plus Environment

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glycine becomes stable at such high pressures. To the best of our knowledge, neither modeling nor experiments have shown so far that pressure could decrease reaction rates. To test the possibility of kinetic hindering, we carried out two experiments above the threshold pressure, for which we further increased temperature from 200 to 250 and 300°C for one to two hours. No polymerization occurred and the only effect of temperature was to increase thermal degradation, with minor decarboxylation observed. This suggests that the system could be thermodynamically locked, although this is not predicted by the currently available thermodynamic models

33,71

that indicate more linear dimers and less DKP as pressure

increases until 2 GPa at least (Figures S6, S7). The Raman spectroscopic data in this study allowed to calculate the equilibrium constant of the cyclization reaction of dimers using the measured values of Gly2/DKP up to 500 MPa (see Supplementary Text for details). Figure 3 presents log K values of the experimental cyclization reaction in pure water. It shows that they are in excellent agreement with the curve extrapolated from Shock’s data model

71

33

and are one log unit below the curve of the DEW

integrating the experimental results of Lemke et al. at high temperature

49.

This is

consistent with the higher yield for linear dimers obtained in the present study that includes the actual effect of pressure. This good agreement between our results and the original model of Shock

33

suggests that the experiments actually reached equilibrium and behaved

as predicted, up to 500 MPa (see also Figure S8 for the comparison of the experimental and theoretical log K of dimerization of glycine). However, above ca. 500 MPa, our results failed to reproduce thermodynamic equilibrium and glycine appeared stable. In their study of the polymerization of amino acids, Otake et al (2011) showed that pressure tends to stabilize glycine and alanine, and oligomers in their solid phase up to 5.5 GPa for temperatures between 180 and 400°C

15.

Although encouraging, the latter results cannot be directly

applied to aqueous solutions. We proposed that the aqueous solvent may play an extra role in the stabilization of aqueous glycine at high pressure. This hypothesis was tested in an experiment, at ambient temperature, in which pressure was increased step-wise from 1 to



1,066 MPa and the interaction between glycine and water was carefully monitored using the C-H vibrations in glycine and the symmetric stretching vibrations of hydroxyls in water between 2700 and 3800 cm-1 (Figure S9). A sudden, reversible transition of the asymmetric C-H stretching vibration around 3025 cm-1

58

is observed between 830 and 880 MPa. The

asymmetric C-H stretching mode of glycine that is well observed up to 830 MPa suddenly broadens and becomes almost undetectable beyond 860 MPa. This apparent broadening is actually related to a significant change in the low frequency part of the O-H stretching of water, with some increased signal at 3050 cm-1. Although the detailed interpretation of the transition would require theoretical calculation that is beyond the scope of the present contribution, the increased intensity of the O-H stretching at 3050 cm-1 combined with the broadening of the asymmetric C-H band of glycine is consistent with the strengthening of hydrogen bonds between glycine and water. This transition occurs at 855 ±25 MPa at ambient temperature, while the polymerization of glycine stops between 500 and 800 MPa at 200°C. Despite the small effect that temperature may have on the exact transition pressure and might be worth investigating theoretically, we propose that this change of the solvation of glycine might stabilize glycine and damper polymerization.

3.5. Effect of magnetite. Figure 3 shows that the presence of magnetite in the system displaces the equilibrium to lower log K values for the cyclization reaction, by half a log unit. This indicates that magnetite does not act only as a catalyst but changes the thermodynamics of the system. During the hydrothermal treatment of glycine, magnetite greatly enhanced the formation of the linear dimer while decreasing the amount of the cyclic one. Figure S8 also suggests that, whereas pressure seems to have an unpredicted effect on the dimerization equilibrium between glycine and linear diglycine, magnetite mainly plays a role in the cyclization reaction of dimers, as its presence does not displace the equilibrium of glycine dimerization to DKP.


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Raman spectra did not reveal any oxidation of magnetite throughout experiments. Therefore, the strong effect of magnetite cannot be related to redox reactions. Considering the initial slightly acidic pH of the glycine solution, magnetite could weakly dissolve and aqueous iron could favor the formation of stable Fe-Gly or Fe-Gly2 complexes through their free anionic carboxylate groups 72, while DKP would be insensitive to ferric iron. It was recently proposed that magnetite (and hematite) could actually promote the hydrothermal reactions of ketones through their catalytic mineral surface

72.

Accordingly, we

propose that the favored production of Gly2 in our experiments is due to reactions at the surface of magnetite. Glycine could be adsorbed on the positively charged surface of magnetite

73

and therefore have different properties and reactivity compared with free

monomers in solution 74. For instance, the free energy of adsorption of polymers is thought to be lower than that of the free monomers

75–78.

From the theoretical and experimental studies

of adsorption of glycine onto magnetite

28,79,80,

anionic or zwitterionic glycine should adsorb

on the positively charged surface of magnetite via its carboxylate group, under the present experimental conditions. Schwaminger et al.

79

proposed that the amino acids could adsorb

on iron hydroxyl sites through ionic or bidentate coordination. The adsorption of the carboxylate group is then combined with deprotonation of the amine group (see Scheme 1 in ref 65). Adsorption hence induces a similar effect as the one described under alkaline conditions, for which glycine is negatively charged 38, as –NH2 is a more efficient nucleophilic group than –NH3+, the nucleophilic attack of peptide bond formation would be greatly favored when glycine is adsorbed onto magnetite. This mechanism also closely resembles the one proposed by Kitadai et al. in dry heating experiments on iron oxide surfaces (see Figure 5 in ref 28). Given the low concentration of magnetite used in our experiments, a maximum of 0.5% of total glycine could have been adsorbed on magnetite (see Supplementary text for more details). Therefore, this suggests that the adsorption of glycine onto the surface of magnetite was highly reversible, with a dynamic equilibrium allowing for new monomers to adsorb.



4. Implications for the prebiotic environments and conclusions In summary, we presented a first of its kind in situ study of the simplest and most abundant amino acid, i.e. glycine, under hydrothermal conditions simulating primitive environments from seafloor hydrothermal systems to subduction zones. In a diamond anvil cell, the classical limitations of ex situ apparatus could be overcome and our results show that polymerization of amino acids at high pressure is a fast, favorable reaction. The stability and reactivity of amino acids is tightly controlled by pressure and mineral surface. Our multiple discoveries suggest that pressure and interactions with mineral surface, and magnetite in particular, are crucial to the formation of the peptide bond within glycine. This is illustrated in Table 1 by comparing optimal Gly2/DKP ratios found in the literature to the significantly larger ones obtained in the present study. To the best of our knowledge, the high Gly2/DKP ratios measured at equilibrium in this study are one order of magnitude higher than those obtained under moderate hydrothermal conditions and comparable to the highest values previously obtained under dry conditions

19.

Hence, we show that high pressure could

stabilize amino acids for extended durations and together with mineral-water interactions could favor their linear polymerization, up to 500 MPa at 200°C. In modern environments, such conditions are widely distributed. Hydrothermal circulation is not limited to localized flows in seafloor hydrothermal vent fields but also occurs deeper in the porous crust, at an average temperature of ca. 150°C, which could be suitable for the chemical evolution of prebiotic systems 9. Under such circumstances, the major limit for prebiotic reactivity would often be pressure rather than temperature. This would hold particularly true in geochemical settings where the temperature gradient is low, such as in subduction zones or convergent margins more generally. Assuming a threshold pressure of 500 MPa as a limit for prebiotic reactivity, as observed for polymerization of glycine in the present study, the prebiotic reactive zone would not only be limited to hydrothermal vents but


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could well extend to the global ubiquitous hydrothermal circulation in the crust and the sediment below seafloor. The maximum depth of the prebiotic reactive zone would then be either limited by high temperatures at mid oceanic ridges, or by high pressure in cold subduction zones, at ca. 25 km depth. A growing body of work suggests that during the Hadean, the crust likely interacted with the primitive ocean favoring the onset of tectonics and subduction 81,82. As dry lands were limited, plate tectonics might have commonly produced intra-oceanic arcs fueled alkaline mud volcanoes develop at present day

83–85.

83,

where serpentinization-

The analysis of 20-km-deep

serpentinite clasts expelled from the South Chamorro mud volcano showed that serpentinization, inclusive of the formation of magnetite occurred below 300°C and that the rocks harbored microbial communities

85.

Building upon this modern example, we could

argue that the source fluid in the deep subsurface of primitive intraoceanic forearc environments would not reach detrimental temperatures and that the depth of the prebiotic reactive zone would be mostly limited by pressure, down to ca. 25-km depth in such settings 70,85.

Last but not least, chemical evolution in the sub-seafloor and below would also be favored by the elevated porosity of serpentinites in such hydrothermal systems. The high porosity allows for large reactive surface areas and high water-rock ratios, hence favoring the adsorption and subsequent polymerization of amino acids. A recurrent limitation opposed to this model is the low concentration in amino acids in the primitive ocean that was probably limited to 106-10-7

M 1, that would render experimental studies irrelevant since they report results

obtained with concentrations hundred to a million time those of the primitive ocean

35,43.

Interestingly enough, Baaske et al. showed that a small temperature gradient in porous networks could tremendously increase the concentration of organic molecules, by a factor of 106 to 108

86.

As a consequence, such deep subsurface geochemical environments,

potentially with molar concentrations of amino acids in high reactive surface area pores in serpentinites, could then represent a large-scale prebiotic reactor on the early Earth. 15 ACS Paragon Plus Environment


Therefore, we propose that high pressures, mild temperatures, high pH conditions and high reactive surface areas in porous networks are highly favorable to the emergence of prebiotic peptides.

Supporting information The data that support the findings of this study are available within the paper and its Supplementary Information Files. Raw data such as pictures taken during hydrothermal experiments or Raman spectra are available from the corresponding author on reasonable request. Supplementary Text: Glycine reactions and Raman quantification. Adsorption of glycine on magnetite. Figure S1: Schematic reaction pathways of glycine. Figure S2: Experimental apparatus: Diamond anvil cell coupled with Raman spectroscopy. Figure S3: Raman spectra of reference solutions for calibration of dimerization quantification. Figure S4: Experimental pressure-temperature conditions in this study and in the literature. Figure S5: Illustration of Raman spectrum fitting and glycine dimerization quantification. Output of the DEW model for the dimerization of glycine and the cyclization of diglycine. Figure S6: Output of Shock (1992) for the dimerization of glycine and the cyclization of diglycine. Figure S7: Output of the updated DEW model for the dimerization of glycine and the cyclization of diglycine. Figure S8: Comparison between both thermodynamic models and experimental data at 200°C and in the presence or absence of magnetite. 16 ACS Paragon Plus Environment

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Figure S9: Raman spectra of the reversible transition in solvent-glycine interactions at high pressure. Table S1: Characteristic Raman bands of glycine and its dimers in solution. Table S2: Characteristic Raman bands of potential decomposition products of glycine. Table S3: Data plotted in Figure 2. Table S4: Details of the quantification procedure.

Acknowledgements This work was supported by the ANR grant ANR2015-CE31-0010 PREBIOM. The authors thank Dimitri Sverjensky for discussion and Marie Cros for her contribution to preliminary experiments. The authors also would like to acknowledge Tim Strobel for the XRD analysis at Geophysical Laboratory (CIW), John Armstrong for the SEM analysis at Geophysical Laboratory (CIW), Kenn Livi for the TEM analysis at Johns Hopkins University and Cécile Feuillie for the help to treat the magnetite.

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Graphics

Figure 1. Dimerization of glycine at 216 MPa, 200°C. A) Selected Raman spectra from a hydrothermal experiment carried out at ca. 216 MPa, 200°C for 8 hours. The starting molecule is pure aqueous glycine (Gly) 2 mol.kg-1. As soon as the sample reaches 200°C, the characteristic bands of diglycine (Gly2) and diketopiperazine (DKP) are present. The relative intensities of these bands remain stable throughout the experiment and after quenching. B) Reference Raman spectra of Gly, Gly2 and DKP at atmospheric pressure and 25°C. The bands highlighted with an asterisk have been used to detect and quantify the presence of the dimers relative to the monomer concentration.



Figure 2. Molar fraction of dimers as a function of pressure, in presence or absence of magnetite. A) Molar fraction of linear diglycine. B) Molar fraction of DKP. Note that the scale of the plots are different to see the evolution of the low amount of DKP.


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Figure 3. Log K of the reaction of cyclization of diglycine as a function of pressure at 200°C. Data from this study are plotted along the curves calculated from Shock

33

and the latest

version of the Deep Earth Water (DEW) Model including results by Lemke et al. 49,71.



Table 1 Optimal ratios of linear over cyclic dimer obtained after hydrothermal treatment of glycine in the literature along with minimal and maximal ratio measured this study. Initial glycine concentration, mineral surfaces, pressure and temperature are also listed. Note that in most previous studies, the optimal ratio is obtained before steady state is reached and generally at very short experimental durations. Mt = montmorillonite; Mgt = magnetite.

Sample Gly 1 M Gly 6.5x10-2 M Gly 2x10-2 M Gly 0.1x10-1 M Gly 0.1x10-1 M Gly 1x10-1 M Gly 5x10-4 M Gly 0.1x10-1 M Gly 0.1x10-1 M Gly 5x10-2 M Gly 2 M Gly 2 M Gly + Mt (Dry/Wet) Gly + Goethite (Dry) Gly + Akaganeite (Dry) Gly + Hematite (Dry) Gly + TiO2 (Dry) Gly + ZnO (Dry) Gly + Mgt (aqueous) Gly + Mgt (aqueous)

P (MPa) 0.1 22.2 0.2 24 25 16.5 20 24 24 20 ~ 50 452 0.1 0.1 0.1 0.1 0.1 0.1 137 300

T (°C) 150 300 120 250 250 200 151 250 225 160 200 200 150 50 50 50 90 90 200 200

Gly2/DKP 0.75 2.00 2.95 0.17 0.096 2.00 2.00 5.20 0.20 0.75 4.02 34.41 0.75 3.60 5.70 0.10 40.00 7.00 19.43 35.90

reference 22 34 36 40 41 43 44 45 46 49 This study This study 22 26 26 26 26 26 This study This study


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Abstract Graphic – For Table of Content Only



Figure 1. Dimerization of glycine at 216 MPa, 200°C. A) Selected Raman spectra from a hydrothermal experiment carried out at ca. 216 MPa, 200°C for 8 hours. The starting molecule is pure aqueous glycine (Gly) 2 mol.kg-1. As soon as the sample reaches 200°C, the characteristic bands of diglycine (Gly2) and diketopiperazine (DKP) are present. The relative intensities of these bands remain stable throughout the experiment and after quenching. B) Reference Raman spectra of Gly, Gly2 and DKP at atmospheric pressure and 25°C. The bands highlighted with an asterisk have been used to detect and quantify the presence of the dimers relative to the monomer concentration. 177x148mm (300 x 300 DPI)


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Figure 2. Molar fraction of dimers as a function of pressure, in presence or absence of magnetite. A) Molar fraction of linear diglycine. B) Molar fraction of DKP. Note that the scale of the plots are different to see the evolution of the low amount of DKP. 139x216mm (300 x 300 DPI)



Figure 3. Log K of the reaction of cyclization of diglycine as a function of pressure at 200°C. Data from this study are plotted along the curves calculated from Shock 33 and the latest version of the Deep Earth Water (DEW) Model including results by Lemke et al. 49,71. 264x256mm (300 x 300 DPI)


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Abstract graphic / For table of content only 81x43mm (300 x 300 DPI)


Spontaneous Polymerization of Glycine under Hydrothermal

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