Transition Metals Enhance the Adsorption of Nucleotides onto Clays

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Transition Metals Enhance the Adsorption of Nucleotides onto Clays: Implications for the Origin of Life Jihua Hao, Marwane Mokhtari, Ulysse Tom Pedreira Segade, Laurent J. Michot, and Isabelle Daniel ACS Earth Space Chem., Just Accepted Manuscript • DOI: 10.1021/ acsearthspacechem.8b00145 • Publication Date (Web): 21 Nov 2018 Downloaded from http://pubs.acs.org on November 22, 2018

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is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

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ACS Earth and Space Chemistry

Transition metals enhance the adsorption of nucleotides onto clays: implications for the origin of life

Jihua Hao*a, Marwane Mokhtaria, Ulysse Pedreira-Segadea,b, Laurent J. Michotc, and Isabelle Daniel*a

* Corresponding author: [email protected]; [email protected]

Address: aUniv Lyon, Université Lyon 1, Ens de Lyon, CNRS, UMR 5276 LGL-TPE, F69622, Villeurbanne, France bcurrently

at Department of Earth and Environmental Sciences, Rensselaer Polytechnic Institute, 110 8th Street, Troy, NY, USA

cSorbonne

Universite´s, UPMC Univ Paris 06, CNRS, Laboratoire PHENIX, Case 51, 4 Place Jussieu, F-75005 Paris, France

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ACS Paragon Plus Environment

ACS Earth and Space Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Abstract: The chemical evolution of early life requires the concentration of monomers to polymerize from the diluted primordial ocean. Transition metals such as Fe, Mn, and Zn, could have reached considerable levels in the early seawater and/or hydrothermal fluid, but their influences on the adsorption of biomolecules have not been clearly addressed yet. In this study, we conducted batch adsorption experiments to explore effects of various metal cations (Li, Mg, Ca, Zn, Ni, and Mn) on the adsorption of selected nucleotides (dGMP, dAMP, and AMP) and adenosine onto nontronite and montmorillonite. We also varied the concentration of the cations and pH of the solutions to evaluate their effects. Our results show that Zn and to some extent, Ni increase the adsorption of nucleotides and adenosine, compared with Na, Mg, and Ca which are major salts in modern seawater. This increased adsorption is primarily attributed to the mediating role of transition metals between the clays and nucleotides and adenosine. The enhancing effect depends little on salt concentration, but strongly varies as the pH of the solution changes. Presence of transition metals reverses the declining trend of the adsorption of dGMP as the elevation of pH and strongly favors adsorption of dGMP at alkaline pH presumably through precipitation of metal-hydroxides on the clay surface. Enhanced adsorption amount of biomolecules mediated by transition metals would potentially ease the origin of life in two aspects: concentration of simple organics for polymerization and protection of early biomolecules against UV radiation and heating in early seawater.

Keywords: transition metals; adsorption; condensation of nucleotides; clay minerals; polymerization; origin of life

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1. Introduction Life probably originated in the late Hadean or early Archean Earth1. The chemical evolution of life probably initiated from accumulation of organic compounds by endogenous synthesis2 and/or delivery of exogenous material via meteorites, interplanetary dust particles etc3. Even assuming substantial efficiency of these sources, the primitive seawater was likely very dilute in terms of organics4. Violent UV-radiation penetrating through the anoxic atmosphere could destroy surface organics5, undermining further accumulation and chemical evolution of biomolecules. Adsorption of biomolecules onto various mineral surfaces has been increasingly studied these years and shown to effectively concentrate and protect biomolecules, therefore favoring their polymerization3,6–8. Clay minerals are common mineral products from water-rock interactions under both ambient and hydrothermal conditions. Considering large surface area and cation exchange capacity of clay minerals, their adsorption performance toward biomolecules has been extensively investigated both experimentally and theoretically9– 14.

Previous studies have mainly simulated origin of life processes under conditions mimicking

the modern Earth. However, the primitive Earth is thought to have distinctive environment conditions, including mineral composition, pH, salinity, and temperature; all of these factors have been shown to affect adsorption behaviors of biomolecules. One obviously important question therefore is how distinctive environments on the primitive Earth could have affected the adsorption of biomolecules onto minerals. To address all of these parameters simultaneously is, of course, impractical in one study. Here, we focus on one parameter, i.e., salinity. Salinity of modern seawater is mainly composed of NaCl plus minor amount of MgSO4. It has been suggested that the primitive seawater was rich in MgSO4 instead of NaCl based on leaching experiments of meteorites15. However, the primitive atmosphere and ocean were mildly reducing with moderate levels of H2,g16, hindering long persistence of SO42- in the early

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waters even though it might have been transported by meteorites. In the meantime, widespread serpentinization reactions should result in Ca- and Fe(II)-rich fluids due to the alteration of ultramafic rocks (including seafloor basalt and meteorites) and formation of Mg-rich smectites17; similar processes are still ongoing in modern hydrothermal environments. Compared with the modern Earth, early Earth had a vast ocean with virtually no land emerged above sea level until the middle Archean18,19. Therefore, in the late Hadean and early Archean, when life might have originated, the seawater should have been heavily buffered by seafloor weathering and hydrothermal fluids, which are enriched in Ca and divalent Fe (see below) but depleted of Mg. In the meantime, no/little emergence of land also indicates no seashore areas for the formation of evaporite, leading to accumulation of sea salt such as NaCl in the seawater. Recently, a large dataset of fluid inclusions in Archean quartz from different localities supported a NaCl-rich early seawater with the salinity comparable to modern seawater20. Transition metals are one group of elements at trace levels in modern surface waters while of vital importance in biological functions. However, considering reducing (due to moderate levels of H2,g) and acidic (high levels of CO2,g) surface environments on the primitive Earth, the surface waters were rich in divalent Fe and probably also Mn leached from waterultramafic rock interactions at least at millimolar levels21, which are comparable to the major components like Ca and Mg. Owing to high silica in the early seawater, the concentration of divalent Fe was experimentally revealed to be controlled by deposition of amorphous greenalite Fe3Si2O5(OH)4 as the precursor of iron(II)-silicate in banded iron formations22. Due to acidity of the seawater with pH around 6.5 in the early Archean and late Hadean23,24, the Fe concentration set by solubility of amorphous greenalite could have reached about 10 mM in the early Archean seawater22. Moreover, transition metals are found to be enriched in hydrothermal fluids interacting with ultramafic rocks, especially divalent Fe, Mn, and Zn which can reach several to tens millimolar levels25,26. A hydrothermal vent environment is

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proposed as a promising cradle for the emergence of life on the Earth and other water-rich planets27–29, despite challenges arising from thermal instability of biomolecules30. In summary, transition metals like divalent Fe could have reached considerable levels in the primitive waters (summarized in Table 1), which might potentially affect adsorption behaviors of biomolecules onto mineral surfaces.

Table1. Aqueous geochemistry of seawater in the present-day and Hadean or early Archean Earth and modern hydrothermal fluid. Element

Modern seawater a Hadean or early Archean seawater a

Hydrothermal fluid a

Ca

10.3 b

40 c

10 – 110 d

Mg

53.2 b

10 c

0d

Fe

10-6 b

10 e

0.2 – 24 f

Mn

5 * 10-7 b

10-6 g

0.2 – 7.1 f

Zn

6 * 10-6 b

Na

468 b

Li

2.5 * 10-2 b

aAll

0.04 – 3 f 500 – 1500 h

319 – 683 f 0.1 – 2.4 f

in mM; bMillero (2013)31; cJones et al. (2015)17; dVon Damm (1995)26; eReported

solubility of divalent Fe based on precipitation experiment of amorphous greenalite22 at pH = 6.5, simulating the early Archean marine environment23; fShock & Canovas (2010)25; gSaito et al. (2003)32; hMarty (2018)20; Pedreira-Segade et al. (2018)12.

Effects of transition metals on the surface adsorption of biomolecules have been proposed and examined, but previous studies mainly have mainly focused on cation-modified clays. For example, previous experiments revealed that montmorillonite fully exchanged with high concentrations of divalent Zn, Cu, Mn, Co, Ni, or trivalent Fe, displays significantly

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higher adsorption of nucleotides than Na-montmorillonite33,34. However, such modified minerals are clearly irrelevant to natural sedimentary settings because transition metals in surface waters cannot reach levels high enough to fully modify the exchangeable cations in clay minerals. In another theoretical study, Liebman et al.35 applied quantum mechanics tools to simulate the relative complexation affinity of Zn and Mg with nucleotides and bentonite clay surface respectively; they found higher affinities of Zn versus Mg complexing with both nucleotides and clay surface. Although the focus of Liebman’s study was on the bridging roles of transition metals on the surface of cation-modified clays, same corollary might be also true for transition metals in aqueous solutions. Few studies explored effect of trace metals in solution on adsorption of biomolecules. For example, Tessis and Vieyra36 studied adsorption of 5’-AMP onto precipitated calcium phosphate (CaPi) and revealed that the adsorption required the presence of Ca in the solution whereas divalent Mn and Mg were less effective and could even inhibit the adsorption when mixed with Ca. Bebié and Schoonen37 reported experimentally both enhancing and hindering adsorption of 5’-AMP onto pyrite by adding trace amounts of divalent Cu and Fe respectively, although these results were complicated by higher concentration of SO32- than that of the trace metals in their experiment. In their following study, Bebié and Schoonen38 found that the presence of divalent Fe and Cu could promote adsorption of acetate onto pyrite surface, but the result again was complicated by the presence of high SO32-. Moreover, in biophysical research, drying deposition of DNA and RNA polynucleotide strands on mica has been shown to be significantly stabilized in the presence of multivalent cations, such as Mg, Ca, Zn, Ni, and their complexes in solution39–42. Adsorption of multivalent metals could indeed modify surface charge of minerals37,38 and enhance binding of organics by the so-called ‘bridging’ effect11. Compared with modern seawater salinity dominated by Na, Ca, Mg, and Cl, transition metals could adsorb more strongly on mineral surfaces and easily form complex with biomolecules considering their higher hydrolysis and complexation

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constants (Table 2 and Sec. 3.4). Therefore, it is necessary and important to study effects of geologically abundant transition metals in early seawater and hydrothermal fluid, such as divalent Fe, Mn, and Zn, on adsorption of small biomolecules onto mineral surfaces.

Table 2. Chemical properties of divalent cations used in this study. Cation Ionic radius log OHK1 b

log SKM c

log (M-

log (M-

HPO42-) d

CH3OPO4) e

log (M-AMP) f

(M)

(Å) a

Na+

1.02

-13.5

0.60

Li+

0.76

-14.0

0.72

Mg2+

0.72

-11.7

-4.7

2.91

1.57

1.60

Ca2+

1.00

-12.8

-5.5

2.74

1.49

1.46

Zn2+

0.74

-8.96

1.6

2.4

2.16

2.38

Ni2+

0.69

-9.86

-0.6

2.08

1.91

2.49

Mn2+

0.83

-10.6

-0.6

2.19

2.23

Fe2+

0.61

-9.1

1.9

aIonic

3.6

radii in crystals (6-coordinated)43; bFirst hydrolysis constant for the reaction: Mx+ + H2O

 MOH(x-1)+ + H+

44,45; cSurface

complexation constants on strong sites for cations on Na-

montmorillonites44,46,47; dStability constants of metal-HPO42- complexes48; eStability constants of metal-CH3OPO4 complexes from Massoud & Sigel (1988)49; fStability constants of metalAMP complexes from Kazakov & Hecht (2011)50

Here, we designed an experimental study to investigate the effects of transition metals on adsorption of several selected nucleotides namely, dGMP, dAMP, AMP, and adenosine, onto nontronite and montmorillonite. Nucleotides are building blocks of genetic material, as well as potential catalysts for bio-reactions. Prebiotic sources of nucleotides include abiotic

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synthesis in the early Earth environments and extraterrestrial transport by comets and meteorites, as recently reviewed by Cleaves (2018)51. Concentration of nucleobases like adenine has been estimated to reach approximately 35 M in the primitive seawater, but is still too low for further chemical evolution and therefore needs a concentration pathway4. We conducted a series of batch adsorption experiments with various combinations of salts (Table S1). Adsorption of nucleotides and adenosine in the presence of divalent transition metals (Zn, Ni, and Mn) were compared with traditionally used salt environment, i.e., Na, Ca, and Mg. As a comparison with Na as the dominant monovalent metal, Li was also tested. Working on divalent Fe requires strictly anoxic facilities, which we are not yet equipped with, but previous studies have shown that surface complexation properties of divalent Fe are similar to those of Zn44,47,52 (Table 2 and detailed discussions in Sec. 4.1) and therefore Zn was studied as a model divalent cation analogue to divalent Fe here.

2. Materials and methods 2.1 Clay minerals The montmorillonite SAz1 (from Arizona) and nontronite NAu2 (from Australia) were used in the present work. These minerals were purchased from the Source Clays Minerals Repository of the Clay Mineral Society (Purdue University, USA) and have been well characterized previously, e.g. surface area and cation exchange capacity (Table S2). Prior to use, they were purified from accessory impurities and sorted by size, following the protocol by Michot et al.53,54. The clay particles were prepared and stored as homogeneous mineral suspensions in deionized water before used in adsorption experiments.

2.2 Chemical reagents

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All organics and inorganic salts were purchased from Sigma AldrichTM with high purity (>99%). We investigated three nucleotides, i.e. dGMP, dAMP, AMP, and adenosine. Their chemical properties were already reported in a previous study55 and also provided here in Table S3. The reagents were dissolved in deionized water to reach the targeted concentrations.

2.3 Batch adsorption experiments Batch adsorption experiments were conducted under ambient conditions of pressure and temperature. 50 µg/mL nucleotides or adenosine were dissolved into 0.5 M NaCl solution, mimicking the salinity of early seawater. Other salts were introduced into the system with concentrations much lower than NaCl (Table S1): LiCl, CaCl2, MgCl2, ZnCl2, NiCl2, and MnCl2. The concentration of nucleotides and adenosine used in the present study is close to the previously estimated level of adenosine in the prebiotic seawater, i.e., 35 M4. Among the salts, Ca and Mg are major components in seawater and/or hydrothermal fluids (Table 1); Zn and divalent Mn can reach considerable levels (mM) in hydrothermal fluids (Table 1) and Zn is also used here as an analogue to divalent Fe; Ni was included to explore possible patterns of effects of divalent cations on adsorption of nucleotides and adenosine; Li was examined here as a comparison with Na. All divalent cations except Mn were used in the same concentration (50 mM) during the experiment for easy comparison. In order to maintain similar ionic strength to those experiments with divalent cations, Li was used at 100 mM. Lower concentrations of MnCl2 (10 mM and 5 mM) were used in the experiment because divalent Mn might be oxidized and easily formed precipitate at higher concentrations. Moreover, concentrations of trace metals (Li, Zn, Ni) were varied (40 mM and 10 mM for Li; 20 mM and 5 mM for Zn and Ni) to explore the influence of metal concentration. These experiments were carried out at natural pH close to 7. In addition, the effect of pH on adsorption was examined by adding 0.1 M HCl or NaOH to reach target pH values (3 and 11) with negligible changes of volume. Ionic strength

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in these systems is constantly controlled by concentration of dominantly abundant NaCl; therefore, its effect on adsorption could be ruled out. Nucleotides or adenosine solutions were mixed with mineral suspensions in 2 mL Eppendorf safe-lock tubes. The closed tubes were vortexed for 10 s to achieve homogenization and then allowed to stand in a dark water bath at 25 °C for 24 h to ensure equilibrium. Afterwards, the suspensions were centrifuged for 25 min at 16,100 g (acceleration of gravity). Finally, the separated supernatant was analyzed to calculate equilibrium concentration of nucleotides or adenosine using UV spectrophotometry at 260 nm. Samples were triplicated and each sample was analyzed four times. Resultant uncertainty was reported as error bar in the figures. The adsorbed amount of nucleotides was calculated from the difference in concentration before and after adsorption normalized by total surface area of mineral particles in each sample. In the experiment at alkaline pH, there was possible precipitation of Ni- or Zn(hydr)oxides on nontronite surface (as discussed below), which potentially modified the surface area. Therefore, we present the results as percentage of nucleotides adsorbed.

3. Results and discussions 3.1 Adsorption of dGMP, dAMP, AMP, and adenosine onto nontronite and montmorillonite

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dGMP onto nontronite

a.

Adsorption enhancement (%) -17 31 51 156 68

Trace element Li Mg Ca Zn Ni

0.12 2

0.1

0.14

Adsorption (µmole/m )

2


0.12


dAMP onto nontronite

b.

0.14

0.08 0.06 0.04 0.02

0.1 0.08 0.06 0.04

0 0.5 M NaCl 100 mM Li 50 mM Mg 50 mM Ca 50 mM Zn 50 mM Ni

0.5 M NaCl 100 mM Li 50 mM Mg 50 mM Ca 50 mM Zn 50 mM Ni

AMP onto nontronite

c.

0.02


0.016 2


2


Adenosine onto nontronite

d.

0.14 0.12


0.02

0


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


0.1 0.08 0.06 0.04


Adsorption enhancement (%) -43 16 -16 84 41

0.012

0.008

0.004

0.02 0

0



Figure 1. Adsorption of (a) dGMP, (b) dAMP, (c) AMP, and (d) adenosine onto nontronite in the presence of different cations. Notice the scale of y axis in (d) is different with others due to little adsorption of adenosine. The adsorption is presented as moles of organic molecules adsorbed per m2 surface area of nontronite. Effects of various cations (Li, Mg, Ca, Zn, or Ni) other than Na on adsorption of nucleotides and adenosine are reported as adsorption enhancement (%) relative to the adsorption amount with only 0.5 M NaCl.

Figure 1 summarizes adsorption results of the three nucleotides and adenosine onto nontronite in the presence of different cations. For the sake of easy comparison, adsorption enhancement (%) was calculated for samples with additional cations relative to the 0.5 M 11



NaCl-only run. The results demonstrated that the addition of divalent cations overall enhances adsorption of the nucleotides and adenosine compared with NaCl-only sample, whereas, the presence of Li has a noticeable detrimental effect on the adsorption. Among the divalent cations investigated, Zn showed the greatest enhancing effect compared with other divalent metals. Ni exhibited stronger enhancing effect than Ca and Mg, but weaker than Zn. Adsorbed amounts of the three nucleotides are relatively close to each other. Still, for all the salt combinations used, a systematic order is observed, i.e. dAMP > AMP > dGMP. In contrast, adsorption of adenosine on nontronite is one order of magnitude lower, which suggests that the phosphate group plays a crucial role in the adsorption of nucleotides, in line with previous studies56,57. Compared with nontronite, montmorillonite adsorbs slightly less dGMP and dAMP (Figure 2), a tendency that was already observed in earlier studies using the same batch of minerals10. As far as the effect of the nature of salts is concerned, montmorillonite and nontronite exhibit the same behavior, i.e., a significant enhancing effect of transition metals and a slight reduction of adsorption in the presence of Li. These results concur with adsorption experiments carried out on pyrite surface37,38 showing that presence of divalent trace elements, such as Zn, Fe, Cu, Ni etc., promotes biomolecules adsorption. This might be linked to the fact that both sulfide minerals and swelling clay minerals bear a negative surface charge over a wide range of pH.

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dGMP adsorption

a.

dAMP adsorption

b. 0.1

0.1

Nontronite Montmorillonite

Nontronite Montmorillonite

2


0.08

0.08 2


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


0.06

0.04

0.02

0

0.06

0.04

0.02

0



Figure 2. Comparison between nontronite and montmorillonite on adsorption of (a) dGMP and (b) dAMP.

3.2 Effects of concentrations of trace metals Since concentration of trace metals would normally not reach levels as high as 50 mM in surface waters even under the Hadean-Archean anoxic and acidic conditions, it is necessary to examine the effects of lower concentrations of the trace metals on the adsorption results. Figure 3 displays the evolution of the adsorbed amounts of dGMP on nontronite with various concentrations of the trace elements, namely Li, Zn, Ni, and Mn. The detrimental effect of Li on the adsorption of dGMP was found to languish at lower Li concentrations. Similarly, the enhancing effects of Zn, Ni, and Mn, appeared to slightly diminish at lower metal concentrations. Nevertheless, it must be emphasized that even at a low concentration such as 5 mM, Zn could still induce more adsorption than the runs with Ca and Mg. In other words, concentration of Zn is not the primary factor to control its enhancing effect on adsorption of nucleotides, at least when the concentration is beyond 5 mM, and Zn is much more effective to enhance the adsorption of nucleotides onto clay minerals than Ca and Mg. This discovery is particularly relevant to primitive environments as the estimated levels of transition metals in

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prebiotic seawater and ultramafic hydrothermal fluids (Table 1) fall within the concentration range studied here. Therefore, transition metals like Fe(II), Zn, and Ni, could substantially promote the adsorption of nucleotides and adenosine onto mineral surfaces in ancient waters and might favor their stability and polymerization (see Sec. 4). b.

0.1

0.1

0.08

0.08 2


2


a.

0.06

0.04

0.02

0.06

0.04

0.02

0

0 NaCl only

100 mM Li

40 mM Li

10 mM Li

c.

NaCl only

50 mM Zn

20 mM Zn

5 mM Zn

d. 0.1

0.08

0.08 2


0.1

2


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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0.06

0.04

0.02

0 NaCl only

50 mM Ni

20 mM Ni

0.06

0.04

0.02

0

5 mM Ni

NaCl only

10 mM Mn

5 mM Mn

Figure 3. Adsorption of dGMP onto nontronite under various levels of trace elements (a: Li; b: Zn; c: Ni; d: Mn).

3.3 Effects of pH Although primitive seawater was nearly neutral23, hydrothermal fluids could be either acidic or alkaline depending on the tectonic setting58,59. We therefore varied the pH of solutions

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to evaluate its effect on the adsorption of nucleotides and adenosine in presence of trace metals (Figure 4). The results demonstrated a pronounced influence of pH on the adsorption. At pH = 3, adsorption of dGMP onto nontronite is overall much higher than at pH = 7, a result that is consistent with previous studies10,55. The samples with Zn and Ni, however, do not follow the same trend as for these two cations, adsorbed amounts at pH = 3 are slightly lower than at higher pH. Interestingly, at acidic pH, the addition of divalent cations does not significantly affect the adsorption of dGMP onto nontronite whereas the detrimental effect associated to Li persists. At pH = 11, samples with NaCl-only, Li, Mg, and Ca exhibited a dramatic decrease of nucleotide adsorption while experiments with Zn and Ni showed an inverse behavior with strongly enhanced adsorption. However, at such alkaline pH, considering the low solubility of both Ni(OH)2,s and Zn(OH)2,s with pKsp of 15.3 and 16.5

43,

respectively, such an increase

could be partly due to the precipitation of metal hydroxides (see discussion below and Supporting Information). A compelling evidence for the precipitation of Ni(OH)2,s and Zn(OH)2,s is the significant loss of dGMP in the blank controls of Zn and Ni experiments without adding clay mineral, in comparison with no loss in the blanks with other metals. The loss is due to the adsorption of dGMP onto newly formed metal-hydroxides. We then subtracted the loss of dGMP in blank controls from the total retained adsorption amount (apparent adsorption) of samples with clay particles, thus yielding the calibrated adsorption results presented in Figure 4. These calibrated adsorption values remain significantly higher than those obtained for samples with alkali and alkaline cations at pH = 11. This result could be tentatively attributed to a surface precipitation of metal hydroxides that could then in turn increase nucleotide adsorption onto the clay surface. The proposed surface precipitation of metal hydroxides is in line with a recent experimental study that observed formation of surface Fe(II)-hydroxide during divalent Fe sorption onto clay surface under neutral and alkaline

15



conditions60. In summary, the adsorption of nucleotides on swelling clays increases as pH declines but the presence of transition metals could reverse such a trend, leading to a significant nucleotide adsorption in alkaline conditions.

dGMP onto nontronite 100 pH = 3 pH = 7 pH = 11 (apparent) pH = 11 (calibrated)

80

Adsorption (%)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

60

40

20

0 0.5 M NaCl 100 mM Li 50 mM Mg 50 mM Ca 50 mM Zn 50 mM Ni

Figure 4. Adsorption amount of dGMP onto nontronite under various pH conditions, in % of starting concentration. For the adsorption experiments at pH = 11, results are presented in two ways: apparent adsorption representing total adsorption after experiment; calibrated adsorption representing net adsorption after deducting the amount of adsorption observed in the blank controls of Zn and Ni runs, presumably by the precipitated metal (Zn/Ni)-hydroxide.

3.4 Proposed mechanisms

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In a solution where minerals, metal cations, and nucleotides or adenosine are present, three types of interaction must be considered: organic-mineral, organic-cation, and cationmineral. As mentioned above, basal surface charge of nontronite and montmorillonite is insensitive to pH and remains negative over a wide range of pH. Consequently, at pH ≥ 7, both the nucleobase and phosphate group of nucleotides are negatively charged55. Adsorption is expected to be rather unfavorable in these conditions due to electrostatic repulsion between the mineral basal surface and adsorbents. However, experimental results from the present work (see 0.5 NaCl-only samples) and previous studies have revealed considerable adsorption of nucleotides onto clay minerals10,12,55. This adsorption is mainly assigned to the binding of phosphate group to metal sites located on the edge surface of clay minerals55. The assignment is further confirmed by our experimental results showing that the adsorption of adenosine is much lower than that of dAMP and AMP. Below we examine evolution of adsorption features as a function of pH. At pH = 3, the phosphate group of nucleotides is still negatively charged but with lower charge (-1 instead of -2 at pH = 7 or 11) whereas the nucleosides become either positively (AMP, dAMP) or neutrally charged (dGMP) (Table S3). The electrostatic repulsion between nucleotides and the basal surface of clay is expected to be weaker, which leads to an increase in adsorbed amount. This phenomenon has been previously observed10,55 and is confirmed in the present study where the adsorption of dGMP at pH = 3 is overall higher than at neutral and alkaline pH (Figure 4). Under acidic condition, presence of divalent cations in the solution has very little influence on adsorption features. At low pH, divalent cations mainly present as free cations and can interact with the clay surface either through non-electrostatic surface complexation with OH-groups on the edge or ionic exchange on the basal surface44. The latter interaction could lead to a partial neutralization of the negatively charged basal surface by adsorption of positively charged cations, which in turn could potentially induce surface-charge

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inversion at high salt concentrations61. However, the concentrations of divalent cations are relatively low in the present study. In addition, adsorption of divalent cations decreases heavily as pH declines and becomes negligible at pH = 3 62. Collectively, adsorption of divalent cations might have little, if any, effects on charge properties of the clay at pH = 3. Consequently, both phosphate binding and electrostatically favorable adsorption of positively charged nucleotides are little influenced by the presence of divalent species at pH = 3. In contrast, the presence of Li appears to hinder nucleotide adsorption. This detrimental effect may be tentatively ascribed to the stronger affinity of Li compared to Na towards the clay surface, which has been shown to be true on muscovite surface63. At pH = 7, dominant adsorption mechanism occurs on the edge surface of clay where the phosphate group of nucleotides binds to the surface hydroxyls of clay in NaCl-only solution12. Under this circumstance, our experiment showed that addition of divalent cations enhances nucleotides adsorption, particularly transition metals being more efficient than Ca or Mg. This enhancing effect could be due to various factors. Divalent cations could either favor phosphate complexation on the edge surfaces or could form complexes with nucleotides to mediate the adsorption of nucleotides onto the mineral surface, a phenomenon that is widely referred to as ‘bridging’ effect 11,64. As far as the former possibility is concerned, experiments carried out on non-swelling uncharged clay minerals such as pyrophyllite showed that the presence of Ca and Mg in solution at neutral pH slightly decreased dGMP adsorption55. This result suggests that the presence of divalent cations does not enhance adsorption of nucleotides on the edge surfaces of clay minerals. Further evidence can be also obtained by analyzing the strength of complexation between metal cations and OH-groups of edge surface, i.e., log K for reaction (1), that is known to strongly vary among different cations65. >SiOH + M2+ + H2O  >SiOM+ + H3O+

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Table 2 summarizes the available surface complexation constants on Na-montmorillonite. It appears that Zn and divalent Fe have significantly stronger complexation affinity with silanol groups on the edge surface of montmorillonite than the other divalent cations. In this case, the presence of Zn should imply a stronger detrimental effect than that of the other cations, which is contradictory to our observation here. As previously suggested12, enhanced adsorption in the presence of divalent cationic species might be caused by the formation of positively charged dGMP-M2+ complexes, that adsorb on the basal surfaces through the formation of cationic bridges. The distinct effect of the nature of cation on the enhancement of nucleotide adsorption, as observed here, suggests that it is worthwhile examining possible interactions between divalent cations and nucleotides in solution. Two mechanisms can be invoked, either electrostatic attraction or chemical complexation. Electrostatic attraction between divalent cations and nucleotides phosphate groups likely occurs but should not be cation specific. With regards to complexation, two potential complexing sites are present in nucleotides: terminal phosphate oxygens and endocyclic atoms in guanosine (N-7) and adenosine (N-7 or N-1)50. Complexation between nucleic acids and multivalent (including divalent) cations is known to be significantly stronger than that with monovalent cation50. Table 2 compiles available literature data on complexation constants for divalent cation-nucleic acid complexes. It shows that the transition metals hold significantly higher constants than the alkaline earth metals such as Ca and Mg. Under the conditions of this study, mass-balance calculations suggested that at least 50% of AMP would occur as AMP-M2+ complex in solutions containing the transition metals, assuming that the complexation reactions reach equilibrium (details described in Supporting Information). As previously suggested12, the presence of such complexes can be inferred from residual analyses of UV absorbance spectra. Indeed, our analysis shows that the presence of transition metals could lead to strong modifications of UV absorbance spectra indicating the formation of complexes in solution, whereas alkaline earth elements such as Ca

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or Mg do not provoke any such changes (Figure 5 & Supporting Information). An inevitable corollary is that adsorption of dGMP-M2+ complexes on basal surfaces through the formation of cationic bridges is more efficient in the case of transition metals due to the stronger complexation. However, such a mechanism does not explain why the enhancing effect of Zn is more pronounced than that of Ni and Mn at similar concentration (Table 2). This dilemma could be partly ascribed to the stronger complexation affinity of Zn with the clay surface than Ni and Mn, as well as the alkaline and alkali metals (Table 2), in line with previous suggestion35. Additional reason may involve the possible precipitation of Zn(OH)2,s on the clay surface considering the lower solubility of Zn(OH)2,s (Ksp = 3 × 10-17)43 compared to Ni(OH)2,s (Ksp = 5.48 × 10-16)43 or Mn(OH)2,s (Ksp = 9 × 10-14)66. Indeed, adsorption has been shown to favor surface precipitation of hydroxides of transition metals even though the suspension might be still undersaturated with respect to corresponding metal hydroxides67,68. If Zn(OH)2 can presumably precipitate onto the clay surface, it could offer more transition metal sites for surface complexation, whereas the other cations remain in solution. Collectively, these two factors could lead to a slightly higher retained amount of nucleotide in the case of Zn.

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0.08

Li Mg Ca Zn Na

0.04

Residual (a.u.)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


0

-0.04

-0.08 240

270

300

330

360

390

Wavelength (nm) Figure 5. UV absorbance spectra residues of dGMP in various salt solutions. The reference spectrum (black line) for residue calculation was dGMP in 0.5 M NaCl solution.

At pH = 11, adsorption on the edge surfaces through phosphate complexation becomes very unfavorable as all sites on the edge faces of clay are then negatively charged. As a result, total adsorption of nucleotide in NaCl-only solution is very low at alkaline pH. This minimal adsorption may be due to remaining phosphate complexation on the edges or to the adsorption of weak dGMP-Na+ complexes on the basal surfaces. As we discussed above, addition of multivalent cations in the solution should enhance the adsorption of nucleotides by forming strong complexes of nucleotide-metal and/or precipitating metal-hydroxides on the clay surface, in line with our observation. Our thermodynamic calculations (Supporting Information) suggest that Zn-, Ni-, and Mn-hydroxides reach supersaturation at pH = 11 under our experimental conditions with Zn(OH)2 as the least soluble mineral among the three 21



hydroxides. The difference between Zn and Ni remains similar to the case at pH = 7 and can be explained in the same way, i.e. as resulting from the lower solubility of Zn(OH)2. Fourier-transform infrared spectroscopy (FT-IR) and Raman spectroscopy are, in principle, potentially useful to detect the surface complexation of organics onto mineral surface. However, in practice, the overlap of P-O and Si-O peaks rules out the applicability of FT-IR in detection of clay-phosphate interaction. In our experiment, Raman spectroscopy is found to be not sensitive enough for the nucleotide concentration used here. In addition, organic matter, in particular small molecules including nucleotides, is too delicate for the high energy input, which would readily burn out the signals. Moreover, swelling clays have a high fluorescence that greatly degrades the quality of the Raman signal. Other analytical techniques, e.g. XANES, STXM, and XRF, have also been applied in parallel studies but none of them so far works with the low concentrations of nucleotides, i.e. M to mM. Compared with the dilemma of analytical techniques, theoretical simulations are promising to decipher the adsorption mechanism, as preliminarily investigated in Liebmann et al.35. In the future, more complicated models involving clay surfaces, nucleotides, and transition metals in the aqueous solution, might be helpful to nail down the relative roles of lateral versus basal surfaces in our system. Our observation of transition metal-enhanced adsorption opens more opportunities for future investigation about organic-mineral interaction with special attentions on roles of geologically abundant transition metals.

4. Implications 4.1 Concentration of nucleotides onto mineral surfaces The prebiotic ocean has been proposed to be very diluted in biomolecules and therefore further chemical evolution necessarily requires concentration processes. Our study suggested that the presence of geologically relevant levels of transition metals, i.e. Zn and Ni, in the early

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ocean could significantly enhance the surface adsorption of nucleotides onto clays, in a much more efficient way than modern seawater divalent salts, i.e. Ca and Mg. Zn studied in this experiment can be considered as an analogue to divalent Fe based on the following considerations: (i) previous investigations on adsorption of divalent Fe and Zn onto nontronite have revealed similar complexation characteristics47,52; (ii) limited available data indicated that Zn and divalent Fe share similar complexation constants for various metal-organic complexes69; (iii) solubility behavior of Fe(OH)2,s is close to that of Zn(OH)2,s 43. The results obtained in the case of Zn, can then likely be extended to divalent Fe, and therefore, geologically relevant levels of divalent Fe in early seawater and hydrothermal fluids should also significantly favor nucleotides adsorption onto mineral surfaces. This hypothesis is further supported by experimental results which showed enhanced adsorption of organics onto pyrite surface (FeS2) in the presence of divalent Fe in solution37,38. In addition to the above-mentioned mineral-cation surface complexation, divalent transition metals could exchange with Ca and Mg to form solid solution of minerals such as carbonate, oxide, and hydroxide70, or get incorporated into interlayer structure of clay minerals71 during water-rock interaction. In this way, structurally coordinated trace metals could modify chemical properties of mineral surfaces72 and potentially promote adsorption of biomolecules. Indeed, previous studies revealed enhancing adsorption of nucleotides onto montmorillonite homo-ionized by transition metals, such as divalent Zn, Cu, Mn, and trivalent Fe33–35. It has also been suggested that in early Earth surface environments, water-rock interactions could have led to the formation of carbonate and clay minerals containing Fe(II)end members73,74. This statement is supported by both theoretical simulations and field observations that revealed the presence of Fe(II)-rich clay minerals, such as saponite, in hydrothermal vents75,76. These types of minerals may then have been more important in early

23



anoxic Earth and clearly deserve further investigation even though they require rather demanding experimental conditions.

4.2 Preservation of biomolecules in planetary environments of early Earth and Mars The primitive Earth was a harsh environment for delicate early life. On one hand, the atmosphere was anoxic with moderate levels of H2,g and thus no ozone layer77. As a result, UV radiation could easily penetrate the atmosphere and reach the surface of early Earth. Under such conditions, UV radiation could readily destroy biomolecules in the surface waters5. On the other hand, although many investigators have suggested hydrothermal vents as the cradle for life on the early Earth and other planets, one has to confront a stability problem of biomolecules at elevated temperatures and pressures. For instance, an experimental study has reported that at T = 100 °C in water, half-lives for decomposition of the nucleotides (A, G, U, and C) in water range from days to years30, much shorter than geological timescale for biological origination and evolution. Therefore, the thermal instability of biomolecules might limit the emergence of life at elevated temperatures78. Previous studies have proposed that adsorption of biomolecules onto mineral surface could shelter them from UV radiation79–86 and heating8. As the early seawater and hydrothermal fluid would be enriched in Fe(II), adsorption of nucleotides should be significantly enhanced in this aspect. Furthermore, complexation between transition metals including Fe(II) and organics is generally stronger at elevated temperatures and pressures69 and adsorption of divalent cations was shown to be promoted with increasing temperature87–89. These lines of evidence concurrently support enhanced surface complexation of nucleotides with minerals in the presence of transition metals, which in turn, could have helped in stabilizing biomolecules on the primitive Earth and other habitable planets. In that context, it is worth mentioning that the Mars Science Laboratory (MSL) mission recently evidenced the presence of several zinc-

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enriched targets at Gale crater on Mars. Such environments might have been formed by highZn reducing fluid activity at low to moderate temperature90 and may then be particularly significant for the potential preservation of Martian biosignatures.

5. Summary This study has investigated the effects of transition metals (Zn, Ni, and Mn) on the adsorption of nucleotides (dGMP, dAMP, AMP) and adenosine onto clay minerals. Our main conclusions are as follows: (1) As compiled by this study (Table 1), transition metals could have reached considerable levels (1 to 10 mM) in surface water (divalent Fe) and hydrothermal fluids (divalent Fe, Mn, and Zn) on the primitive Earth. (2) Zn and Ni significantly increase the adsorption of nucleotides onto the clays compared with traditionally used salts, i.e. Na, Ca, and Mg, favoring the stability and concentration of biomolecules for polymerization. (3) The enhancing effect by transition metals is heavily dependent on pH of the solutions, but less on cation concentrations in the range studied here. High pH favors the enhancing effect whereas lower concentration of cation slightly lessens it. (4) The enhancing effect is primarily attributed to enhanced cation bridging on the basal surfaces of swelling clay minerals. The formation and surface precipitation of metal hydroxide also plays a role in this effect. The second mechanism is particularly important at high pH. (5) Transition metals, either in early waters or minerals on the Earth or Mars, could significantly increase adsorption of biomolecules on the clay surface, therefore favoring surface condensation of monomers for possible subsequent polymerization. Moreover, increased adsorption of nucleotides onto mineral surfaces might help protect them from UV radiation and heating on early Earth and other planetary environments.

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Supporting Information Complexation of AMP with metal cations (S-1); spectra residual analysis (S-2); saturation states of metal-hydroxides (S-3); experimental setup of salts (Table S1); properties of clay minerals used in this study (Table S2); properties of biomolecules used in this study (Table S3).

Acknowledgement This work is financially supported by The French National Research Agency through the PREBIOM (Primitive Earth - Biomolecules Interacting with Hydrothermal Oceanic Minerals) project #ANR-15-CE31-0010. J. H. wants to acknowledge the postdoctoral fellowship from LABEX Lyon Institute of Origins (ANR-10-LABX-0066) of the Université de Lyon within the program "Investissements d'Avenir" (ANR-11-IDEX-0007) of the French government operated by the National Research Agency (ANR). We acknowledge the helpful comments of D.A. Sverjensky (JHU) on the manuscript. We also thank two anonymous reviewers and editor Professor J. Blum for helpful reviews.

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Transition Metals Enhance the Adsorption of Nucleotides onto Clays

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