Introduction
According to the hypothesis proposed in 1951 by the Irish scientist John Desmond Bernal on primitive Earth minerals was important in the pre-concentration and polymerization of organic molecules, in the protection of these molecules against hydrolysis and ultraviolet (UV) radiation and even as a primitive genetic code (Bernal, Reference Bernal1951). Several studies show that at least the first four roles could have occurred (Lahav and Chang, Reference Lahav and Chang1976; Mosqueira et al., Reference Mosqueira, Albarran and Negrón-Mendoza1996; Zaia, Reference Zaia2004; Lambert, Reference Lambert2008; Marshall-Bowman et al., Reference Marshall-Bowman, Ohara, Sverjensky, Hazen and Cleaves2010; Baú et al., Reference Baú, Villafañe-Barajas, da Costa, Negrón-Mendoza, Colín-García and Zaia2020).
Nowadays on the Earth, there are more than 5000 minerals. However, 3.5–3.8 Gy (Gy = billion years ago), before the appearance of the first living beings, ~500 types of minerals existed on Earth (Westall, Reference Westall2004; Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008; Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018). According to Hazen et al. (Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008), the main minerals found in this period were Mg-olivines, pyroxene, Fe–Ni metal, FeS, phyllosilicates, carbonates, sulphates and hydroxides. Among the clay minerals, montmorillonite existed on the primitive Earth (Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008) and since montmorillonite has a high surface area and adsorbs organic molecules, it is one of the most widely studied minerals in prebiotic chemistry (Zaia, Reference Zaia2012; Theng, Reference Theng2018). Montmorillonite was identified in 1896, and is a phyllosilicate from the smectite group ((Si7.74Al0.26)(Al3.06Fe3+0.03Fe2+0.03Mg0.48)O20(OH)4Na0.77), with a crystalline arrangement of tetrahedral/octahedral sheets type 2:1 (Paineau et al., Reference Paineau, Michot, Bihannic and Baravian2011; Savic, 2014; Uddin, Reference Uddin, Mansoor and ZoveidavianpoorIntech2018). Montmorillonite is negatively charged, due to the substitution of cations in the tetrahedral and mainly in the octahedral sheets of the clay, providing a negative charge between 0.2 and 0.5 eV. The charge of the layer is compensated by the introduction of interchangeable intercalary cations, usually in its hydrated form (Krupskaya et al., Reference Krupskaya, Zakusin, Tyupina, Dorzhieva, Zhukhlistov, Belousov and Timofeeva2017).
Montmorillonite adsorbs several metals, which could modify its properties (Savic et al., Reference Savic, Stojiljkovic, Savic, Gajic and Wesley2014; Theng, Reference Theng2018; Uddin, Reference Uddin, Mansoor and ZoveidavianpoorIntech2018). Among these, Cu2+ and Fe3+ ions should be highlighted, because they have great affinity to form complexes with biomolecules (Briner, Reference Briner1958; Perrin, Reference Perrin1959, Reference Perrin1960; Hallman et al., Reference Hallman, Perrin and Watt1971; Bryantsev et al., Reference Bryantsev, Diallo and Goddard2009; Masoud et al., Reference Masoud, El-Kaway, Hinddawy and Soayed2012), this has great implications in prebiotic chemistry (Lailach et al., Reference Lailach, Thompson and Brindley1968b; Schwendinger and Rode, Reference Schwendinger and Rode1989; Rode and Schwendinger, Reference Rode and Schwendinger1990; Rode and Suwannachot, Reference Rode and Suwannachot1999; Rode et al., Reference Rode, Son, Suwannachot and Budjdak1999; Remko and Rode, Reference Remko and Rode2001; Fitz et al., Reference Fitz, Reiner and Rode2007; Rimola et al., Reference Rimola, Rodríguez-Santiago, Ugliengo and Sodupe2007; Feuillie et al., Reference Feuillie, Daniel, Michot and Pedreira-Segade2013; Kim and Switzer, Reference Kim and Switzer2014; Pedreira-Segade et al., Reference Pedreira-Segade, Feuillie, Pelletier, Michot and Daniel2016, Reference Pedreira-Segade, Hao, Razafitianamaharavo, Pelletier, Marry, Le Crom, Michot and Daniel2018; Zaia and Zaia, Reference Zaia and Zaia2021).
Iron is the fourth most abundant element in the Earth's crust (Cornell and Schwertmann, Reference Cornell and Schwertmann2003; Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008). Most of the iron on the prebiotic Earth was in the form of Fe°, Fe in alloys and Fe2+ in several different minerals such as olivine, pyroxene, iron-oxide, iron-sulfides, iron-carbonates, iron-phosphates and Fe2+ in the prebiotic Earth oceans (Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008; Cleaves et al., Reference Cleaves, Scott, Hill, Leszczynski, Sahai and Hazen2012; Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018). Although the prebiotic atmosphere was considerably anoxic (Catling and Claire, Reference Catling and Claire2005), Fe3+ ions could be derived from the oxidation of Fe2+ by UV radiation or hydrogen peroxide formed in ice (Braterman et al., Reference Braterman, Cairns-Smith and Sloper1983; Liang et al., Reference Liang, Hartman, Kopp, Kirschvink and Yung2006). In addition, temperature conditions, ranging from 300 to 350°C; pressures (from 10 to 25 MPa), with alkaline pH (from 9.5 to 14), could also have oxidized Fe2+ to Fe3+ (Bassez, Reference Bassez2018). Thus, we cannot rule out the existence of minerals containing Fe3+ such as clay minerals (berthierine, chamosite, cronstedtite, greenalite, nontronite and vermiculite), oxides and hydroxides (akageneite, ferrihydrite, goethite, hematite, lepidocrocite and magnesioferrite), garnets (andradite and schorlomite), pyroxenes (aegirine and aegirine-augite), amphiboles (arfvdsonite, hastingsite, katophorite, magnesio-arfvedsonite and magnesiohornblende), carbonates (pyroaurite) and micas (celadonite) (Cleaves et al., Reference Cleaves, Scott, Hill, Leszczynski, Sahai and Hazen2012; Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018). In addition, we cannot rule out the existence of Fe3+ in the prebiotic Earth oceans.
Even though average crustal abundance of copper (50 ppm) is much lower than the iron (41 000 ppm) (Hazen, Reference Hazen2013), its importance for the molecular evolution and formation of polymers, makes it an important element to use in prebiotic chemistry experiments (Schwendinger and Rode, Reference Schwendinger and Rode1989; Rode and Schwendinger, Reference Rode and Schwendinger1990; Rode and Suwannachot, Reference Rode and Suwannachot1999; Rode et al., Reference Rode, Son, Suwannachot and Budjdak1999; Remko and Rode, Reference Remko and Rode2001; Fitz et al., Reference Fitz, Reiner and Rode2007; Rimola et al., Reference Rimola, Rodríguez-Santiago, Ugliengo and Sodupe2007; Kim and Switzer, Reference Kim and Switzer2014; Zaia and Zaia, Reference Zaia and Zaia2021). As reported above for the iron, copper could also be found on the prebiotic Earth as Cu° metal, Cu in (Cu, Ni, Zn) alloys and Cu+ in several minerals such as copper-sulfides, copper-oxides and copper-sulfosalts, as well as Cu+ in the seas of the prebiotic Earth (Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008; Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018). Although the oxygen concentration in Earth's atmosphere was very low (Catling and Claire, Reference Catling and Claire2005), it was sufficient to oxidize Cu+ to Cu2+ (Ochiai, Reference Ochiai1978). Thus, we could expect to have minerals containing Cu2+ on the prebiotic Earth, such as copper-carbonates (azurite and malachite) and copper-sulphates (brochanthite and chalcanthite) and Cu2+ in the prebiotic Earth oceans (Morrison et al., Reference Morrison, Runyon and Hazen2018).
It should be noted that the minerals described above that contain Cu2+ and Fe3+ are volumetrically significant enough to be considered important in prebiotic chemistry experiments (Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018).
Nowadays, iron and copper play important roles in the physiological processes of living beings (Murad and Fischer, Reference Murad, Fischer, Stucki, Goodman and Schwertmann1988; Williams, Reference Williams2007; Curi and Procopio, Reference Curi and Procopio2017). Probably due to high affinity for amino acids, several metalloenzymes contain iron and copper (Ochiai, Reference Ochiai1978, Reference Ochiai1983; Williams, Reference Williams1985; Andreini et al., Reference Andreini, Bertini, Cavallaro, Holliday and Thornton2008). Thus, it could be expected that iron and copper were important for the origin of life.
According to Knauth (Reference Knauth1998), the primitive oceans were approximately twice as saline as those of today, which present high concentrations of Na+ and Cl− ions. With this in mind, Zaia (Reference Zaia2012) suggested a seawater composition, using the information from the work of Izawa et al. (Reference Izawa, Nesbitt, Macrae and Hoffman2010), in which the main ions are Mg2+, Ca2+ and SO42−. The high concentrations of these ions were determined based on the concentration of ions present in the Tagish Lake meteorite, found in Tagish Lake (Yucon, Canada). The meteorite is a carbonaceous chondrite that provides important information on the composition and evolution of primitive oceans (Brown et al., Reference Brown, Hildebrand, Zolensky, Grady, Clayton, Mayeda, Tagliaferri, Spalding, MacRae, Hoffman, Mittlefehldt, Wacker, Bird, Campbel, Carpenter, Gingerich, Glatiotis, Greiner, Mazur, McCausland, Plotkin and Mazur2000). This seawater better represents the saline composition of the prebiotic Earth compared with current seawater and is denominated seawater 4.0 Ga.
There are several studies describing the synthesis of adenine under prebiotic chemical conditions (Basile et al., Reference Basile, Lazcano and Oró1984; Orgel, Reference Orgel2004; Borquez et al., Reference Borquez, Cleaves, Lazcano and Miller2005; Larowe and Regnier, Reference Larowe and Regnier2008; Cleaves et al., Reference Cleaves, Scott, Hill, Leszczynski, Sahai and Hazen2012; Iqubal et al., Reference Iqubal, Sharma, Kamaluddin and Jheeta2019; Yadav et al., Reference Yadav, Kumar and Krishnamurthy2020), as well as its detection in meteorites (Hua et al., Reference Hua, Kobayashi, Ochiai, Gehrke, Gerhardt and Ponnamperuma1986). Therefore, adenine and montmorillonite were most likely present in the primitive Earth and it is probable that they could have interacted.
There are several works showing that the adsorption of adenine and adenine nucleotides onto clays depends on the pH and the exchangeable cations (Lailach et al., Reference Lailach, Thompson and Brindley1968a, Reference Lailach, Thompson and Brindley1968b; Lailach and Brindley, Reference Lailach and Brindley1969; Winter and Zubay, Reference Winter and Zubay1995; Benetoli et al., Reference Benetoli, de Santana, Zaia and Zaia2008; Carneiro et al., Reference Carneiro, Berndt, de Souza Junior, de Souza, Paesano, da Costa, di Mauro, de Santana, Zaia and Zaia2011; Cleaves et al., Reference Cleaves, Scott, Hill, Leszczynski, Sahai and Hazen2012; Feuillie et al., Reference Feuillie, Daniel, Michot and Pedreira-Segade2013, Reference Feuillie, Sverjensky and Hazen2015; Pedreira-Segade et al., Reference Pedreira-Segade, Feuillie, Pelletier, Michot and Daniel2016; Villafañe-Barajas et al., Reference Villafañe-Barajas, Baú, Colín-García, Negrón-Mendoza, Heredia-Barbero, Pi-Puig and Zaia2018; Baú et al., Reference Baú, Villafañe-Barajas, da Costa, Negrón-Mendoza, Colín-García and Zaia2020). The interaction of biomolecules with mineral surfaces could have contributed to chemical evolution. In addition, the adsorption of adenine and adenine nucleotides has been studied in several other minerals such as silica (Basiuk et al., Reference Basiuk, Gromovoy and Khil'Chevskaya1995; Cohn et al., Reference Cohn, Hansson, Larsson, Sowerby and Holm2001; Cleaves et al., Reference Cleaves, Scott, Hill, Leszczynski, Sahai and Hazen2012), iron-sulfides (Cohn et al., Reference Cohn, Hansson, Larsson, Sowerby and Holm2001), forsterite (Cohn et al., Reference Cohn, Hansson, Larsson, Sowerby and Holm2001), graphite (Sowerby et al., Reference Sowerby, Mörth and Holm2001), rutile (Cleaves et al., Reference Cleaves, Jonsson, Jonsson, Sverjensky and Hazen2010), apatite (Winter and Zubay, Reference Winter and Zubay1995; Hammami et al., Reference Hammami, El-Feki, Marsan and Drouet2015), iron oxides (Cohn et al., Reference Cohn, Hansson, Larsson, Sowerby and Holm2001; Canhisares-Filho et al., Reference Canhisares-Filho, Carneiro, de Santana, Urbano, da Costa, Zaia and Zaia2015) and zeolites (Baú et al., Reference Baú, Carneiro, de Souza Junior, de Souza, da Costa, di Mauro, Zaia, Coronas, Casado, de Santana and Zaia2012; Anizelli et al., Reference Anizelli, Baú, Valezi, Canton, Carneiro, di Mauro, da Costa, Galante, Braga, Rodrigues, Coronas, Casado-Coterillo, Zaia and Zaia2016). Depending on the environment in which a given mineral is found, its surface and physical–chemical properties may be different due to modifications by elements or molecules that could have interacted with it. For clay minerals, the main properties that can be modified are the increase in the interlamellar space and the capacity of ionic exchange capacity. Thus, a biomolecule that would be poorly adsorbed in a mineral under certain conditions may have an increased adsorption if the mineral has been modified (Mortland et al., Reference Mortland, Shaobai and Boyd1986).
Thus, the main goal of this work was to modify the montmorillonite mineral with Cu2+ and Fe3+ ions, in order to determine the adsorption capacity of adenine under prebiotic chemistry conditions on the modified material, and to investigate the interaction of the adenine with the montmorillonite [montmorillonite washed with distilled water (Mont-STD)], Cu2+-montmorillonite [montmorillonite modified with 500 ml of 0.1 mol l−1 of CuCl2 (Cu2+-Mont)] and Fe3+-montmorillonite [montmorillonite modified with 500 ml of 0.1 mol l−1 FeCl3 solution (Fe3+-Mont)] using different adsorption isotherm models, infrared (IR) spectroscopy–Fourier transform-IR (FT-IR) and X-ray diffractometry. Adsorption isotherms were obtained at the temperatures of 30, 45 and 60°C, because they are easily controlled using a water bath. Furthermore, these temperatures are in the range of the primitive oceans of the Earth (Krissansen-Totton et al., Reference Krissansen-Totton, Arney and Catling2018). To better represent the primitive Earth, the prebiotic chemistry experiments were performed in saline solution.
Materials and methods
All the reagents were of analytical grade P.A.
Materials
Montmorillonite
Montmorillonite KSF (CAS 1318-93-0) was purchased from Acros Organics, NJ, USA and was used as received.
Artificial Seawater
Artificial seawater 4.0 Gy was prepared as described by Zaia (Reference Zaia2012). The following salts were dissolved in 1.0 l of ultrapure water: Na2SO4 (0.271 g), MgCl2⋅6H2O (0.500 g), CaCl2⋅2H2O (2.50 g), KBr (0.050 g), K2SO4 (0.400 g) and MgSO4 (15.00 g).
Modification of montmorillonite
Mont-STD was prepared by making a suspension of 5 g of montmorillonite KSF in 500 ml of distilled water under constant stirring for 24 h. The suspension was filtered and washed with 3.0 l of distilled water and then it was lyophilized.
To prepare the montmorillonite modified with Cu2+ (Cu2+-Mont) and Fe3+ (Fe3+-Mont), the clay was saturated with Cu2+ or Fe3+ by stirring 5 g of montmorillonite with 500 ml of 0.1 mol l−1 of CuCl2 or FeCl3 solution for 24 h. The suspension was filtered and washed with distilled water until it was free of Cl− ions and then lyophilized.
Methods
Adsorption isotherms
To obtain the adsorption isotherms, 10 m Lof adenine dissolved in distilled water or in artificial seawater 4.0 Gy with concentrations ranging from 0 to 800 mg L−1 were mixed with 50 mg of Mont-STD, Cu2+-Mont, or Fe3+-Mont (all experiments were performed by triplicate) in 15 mL Falcon tubes. The samples were stirred for 1 h at three different temperatures (30, 45 and 60°C), at a pH range of 5.00–6.00. The temperatures were controlled (±0.2°C) using a thermostatic water bath. Next, the samples were centrifuged at 6000 rpm, the supernatant was collected and the adenine was quantified using a spectrophotometer UV–Vis Spectrum SP-2000UV at 260 nm.
The results of adenine adsorption on different montmorillonites were fitted to non-linear isotherm models: Langmuir, Freundlich and Sips models (Limousin et al., Reference Limousin, Gaudet, Charlet, Szenknect, Barthès and Krimissa2007; Foo and Hameed, Reference Foo and Hameed2010).
Non-linear Langmuir isotherm model
where C (mg L−1) is the concentration of adenine in the solution after the equilibrium; qe (mg g−1) is the concentration of adenine adsorbed onto montmorillonite (difference between initial adenine concentration and the concentration after the equilibrium) by mass unity; Q max (mg g−1) is the theoretical limit of adsorbed adenine onto montmorillonite; and k eq (L mg−1) is the equilibrium constant (adsorbate–adsorbent).
Non-linear Freundlich isotherm model
where K f is the adsorption capacity of Freundlich and n is the index of heterogeneity.
Non-linear Sips isotherm model
where K (L mg−1) is the affinity constant for adsorption and n is the index of heterogeneity.
N2 isotherm
Determination of surface area, volume and pore size was performed on a High Speed Gas Sorption Analyzer, Version 11.02. The samples were previously treated at 120°C under vacuum for 3 h. Measurements were performed at liquid N2 temperature (77.3 K). Data were analysed with NovaWin 11.0 software. The Brunauer, Emmett and Teller (BET) method was used to calculate the surface area by plotting P/ν(P 0−P) versus P/P 0 (equation (4)).
where P 0 is the equilibrium pressure, P is the saturation pressure, ν is the adsorbed gas volume, νm is the adsorbed gas monolayer volume and C is the BET constant. The Barret–Joyner–Halenda (BJH) and Dollimore and Heal (DH) methods were used to calculate pore size and volume.
FT-IR spectroscopy
FT-IR spectra were obtained using a Bruker FT-IR spectrophotometer, model Vertex 70, with Platinum ATR reflectance accessory. The spectra from 400 to 4000 cm−1 were obtained from 16 scans at a resolution of 4 cm−1.
Results and discussion
Specific surface area
The surface area and pore volume of montmorillonites modified with Fe3+ and Cu2+ decreased compared with Mont-STD (Table 1). The decrease in surface area and pore volume could be attributed to the sorption of metals onto montmorillonite. The pore size was not changed after modification with the ions.
Table 1. Parameters obtained from N2 adsorption/desorption isotherm
BET, Brunauer, Emmett and Teller method used for superficial area determination; BJH: Barret–Joyner–Halenda; DH: Dollimore and Heal methods used for pore volume and pore size determinations. Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol l−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol l−1). Each result is the mean of two experiments.
Adsorption isotherms
The adsorbed adenine, dissolved in distilled water or artificial seawater 4.0 Gy, onto Mont-STD and Cu2+-Mont decreased as temperature increased (Fig. 1). However, we observed an opposite trend for adenine adsorbed onto Fe3+-Mont (Fig. 1). Thus, an exothermic process occurred for adenine adsorbed onto Mont-STD or Cu2+-Mont, while an endothermic process occurred for adenine adsorbed onto Fe3+-Mont. The highest adenine adsorption occurred when adenine was dissolved in artificial seawater 4.0 Gy onto Fe3+-Mont at 60°C (Fig. 1). The lowest adenine adsorption occurred when adenine was dissolved in distilled water or artificial seawater 4.0 Gy onto Mont-STD (Fig. 1). Adenine dissolved in artificial seawater 4.0 Gy adsorbed little less on montmorillonite than adenine dissolved in distilled water (Fig. 1, Table 2), however, depending on the pH (3.9–4.6) this effect was higher (Villafañe-Barajas et al., Reference Villafañe-Barajas, Baú, Colín-García, Negrón-Mendoza, Heredia-Barbero, Pi-Puig and Zaia2018) and at very acidic pH (2.20–2.74) there was no difference between them (Baú et al., Reference Baú, Villafañe-Barajas, da Costa, Negrón-Mendoza, Colín-García and Zaia2020). The adenine adsorption, at several pH ranges, onto ferrihydrite decreased in all seawaters (seawater 4.0 Gy, today's seawater) when compared with distilled water (Canhisares-Filho et al., Reference Canhisares-Filho, Carneiro, de Santana, Urbano, da Costa, Zaia and Zaia2015). Furthermore, the adsorption of uridine-5′-monophosphate onto brucite decreased in NaCl solution when compared with distilled water (Fornaro et al., Reference Fornaro, Brucato, Feuillie, Sverjensky, Hazen, Brunetto, D'Amore and Barone2018). However, artificial seawater 4.0 Gy did not decrease the adsorption of adenine onto several Fe–ZSM-5 zeolites (Anizelli et al., Reference Anizelli, Baú, Valezi, Canton, Carneiro, di Mauro, da Costa, Galante, Braga, Rodrigues, Coronas, Casado-Coterillo, Zaia and Zaia2016). Although the modification of montmorillonite with Fe3+ and Cu2+ decreased its surface area (Table 1), the adsorption of adenine onto these clays, in general, was higher than on Mont-STD (Fig. 1). It should be noted that, in general, transition metals enhanced the adsorption of nucleic acid bases and nucleotides onto clay minerals (Lailach et al., Reference Lailach, Thompson and Brindley1968a; Pedreira-Segade et al., Reference Pedreira-Segade, Feuillie, Pelletier, Michot and Daniel2016, Reference Pedreira-Segade, Hao, Razafitianamaharavo, Pelletier, Marry, Le Crom, Michot and Daniel2018; Hao et al., Reference Hao, Mokhtari, Pedreira-Segade, Michot and Daniel2019). In addition, the effect of an increase in adsorption of adenine onto modified montmorillonites was higher at higher temperatures (Fig. 1(c)). The adsorption of adenine onto montmorillonites was not due to electrostatic interaction, since in the pH range used (5.0–6.0), adenine is uncharged (Christensen et al., Reference Christensen, Rytting and Izatt1970). Cu2+-Mont or Fe3+-Mont adsorbed the same amount of positively or uncharged adenine (Lailach et al., Reference Lailach, Thompson and Brindley1968b). Thus, it is probable that adenine interacts with the adsorbed metals on montmorillonite.
Fig. 1. Adsorption isotherms of adenine onto different montmorillonites in distilled water and artificial seawater 4.0 Gy at (a) 30°C; (b) 45°C and (c) 60°C. C (mg L−1) is the concentration of adenine in solution after the equilibrium, θ (mg g−1) is the amount of adenine adsorbed onto montmorillonites. Mont-STD: adenine dissolved in distilled water adsorbed onto Mont-STD; Mont-STD (SW): adenine dissolved in artificial seawater 4.0 Gy adsorbed onto Mont-STD; Cu2+-Mont: adenine dissolved in distilled water adsorbed onto Cu2+-Mont; Cu2+-Mont (SW): adenine dissolved in artificial seawater 4.0 Gy adsorbed onto Cu2+-Mont; Fe3+-Mont: adenine dissolved in distilled water adsorbed onto Fe3+-Mont; Fe3+-Mont (SW): adenine dissolved in artificial seawater 4.0 Gy adsorbed onto Fe3+-Mont. Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol L−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol L−1). Each result was a mean of three experiments. The solutions were stirred for 1 h at 30, 45 and 60°C, with 50 mg of montmorillonite, at pH range 5.0–6.0. Artificial seawater 4.0 Gy was prepared as described by Zaia (Reference Zaia2012).
Table 2. Sips parameters obtained for non-linear model adjustment of adenine adsorption onto different montmorillonites in distilled water or artificial seawater 4.0 Gy
Each result is a mean of three experiments. The solutions were stirred for 1 h at 30, 45 and 60°C, with 50 mg of montmorillonite, at pH range 5.00–6.00. Q max: maximum adsorption capacity (mg g−1); K: adsorbate–adsorbent affinities (L mg−1); n: empiric constant. Artificial seawater 4.0 Gy was prepared as described by Zaia (Reference Zaia2012). Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol L−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol L−1).
Among the isotherm models studied, for all samples with one exception, the Sips model showed the best coefficient of determination-R 2 (Table 3). Thus, this model was used to obtain maximum adsorption capacity (Q max), adsorbate–adsorbent affinities (k) and empiric constant (n) (Table 2).
Table 3. R 2 parameters for isothermal modelling of adenine adsorption onto different montmorillonites in distilled water or artificial seawater 4.0 Gy
Each result is a mean of three experiments. Artificial seawater 4.0 Gy was prepared as described by Zaia (Reference Zaia2012). Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol L−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol L−1).
For experiments carried out in distilled water, the maximum adsorption capacity (Q max) values of adenine adsorbed onto Mont-STD and Cu2+-Mont did not demonstrate large differences at 30 and 45°C; however, there was a considerable decrease at 60°C (Table 2). In addition, Mont-STD and Cu2+-Mont presented almost the same Q max values (Table 2), meaning that Cu2+ did not have an effect on adenine adsorption when it was dissolved in distilled water (Table 2). In addition, artificial seawater 4.0 Gy did not have an effect on the adsorption of adenine onto Mont-STD. However, at 30 and 45°C, artificial seawater 4.0 Gy had a large effect on the adsorption of adenine onto Cu2+-Mont (Table 2). For all these experiments, the adsorption of adenine decreased at 60°C (Fig. 1, Table 2). This decrease in adsorption with increasing temperature indicates that adenine adsorption on these montmorillonites is an exothermic process. In addition, the adsorption of adenine onto graphite is an exothermic process (Sowerby et al., Reference Sowerby, Mörth and Holm2001). The Q max values for the adsorption of adenine onto Fe3+-Mont at 30 and 45°C did not show a large variation in distilled water or artificial seawater (Table 2). Furthermore, these Q max values were almost the same as those obtained when adenine was dissolved in distilled water and artificial seawater 4.0 Gy and adsorbed onto Mont-STD or Cu2+-Mont and Mont-STD, respectively (Table 2). However, when adenine was dissolved in artificial seawater 4.0 Gy and adsorbed onto Fe3+-Mont at 60°C, the highest Q max value was obtained (Table 2). Thus, in this case, the adsorption is an endothermic process. These results suggest that the adsorption of adenine onto Cu2+-Mont or Fe3+-Mont involves a complex interaction among adenine, salts in seawater and Cu2+/Fe3+. A possible explanation for these data would be that the salts of the artificial seawater decreased the activity of the water, thereby reducing the hydration sphere of adenine, as well as of the metals, facilitating its interaction with Cu2+/Fe3+-Mont (Do Nascimento Vieira et al., Reference Do Nascimento Vieira, Kleinermanns, Martin and Preiner2020).
The n parameter of the Sips isotherm model could be related to the heterogeneity of the system (Do, Reference Do1998). The adsorption is heterogeneous when montmorillonites have several different adsorption sites and adenine interacts differently with them. For the Sips isotherm model, if the n values are >1, this means that the system is more heterogeneous (Do, Reference Do1998). For all experiments, the n values were <1, which means that the adenine adsorption process on the montmorillonites is homogeneous (Table 2).
Thermodynamic functions (ΔG, ΔH, ΔS)
For better understanding of the adsorption process, the thermodynamic parameters, namely Gibbs free energy (ΔG), enthalpy (ΔH) and entropy (ΔS), were determined from equations (5) and (6):
where R is the thermodynamic gas constant (8.314 J mol−1 K−1), T is the temperature (K) and K d is the distribution coefficient (Lg−1) that can be obtained by plotting q e/C versus q e and extrapolating q e to zero.
For all experiments, ΔG presented negative values, indicating that adenine adsorption on different montmorillonites is a spontaneous and favourable process (Table 4). Furthermore, the adsorption of adenine, adenosine-5′-monophosphate and nucleosides (adenosine, inosine)/nucleotides (adenosine triphosphate and uridine-5′-triphosphate) onto graphite, apatite and silica presented negative values for ΔG, respectively (Basiuk et al., Reference Basiuk, Gromovoy and Khil'Chevskaya1995; Sowerby et al., Reference Sowerby, Mörth and Holm2001; Hammami et al., Reference Hammami, El-Feki, Marsan and Drouet2015). The adsorption of adenine dissolved in distilled water or artificial seawater 4.0 Gy onto Fe3+-Mont was ruled by entropy (Table 4). However, from the point of view of enthalpy, the process is endothermic (Table 4). The adsorption of adenine, dissolved in distilled water or artificial seawater 4.0 Gy onto Mont-STD, is thermodynamically favourable from the point of view of enthalpy (ΔH < 0) and entropy (ΔS > 0) (Table 4). The same can be said for the system of adenine adsorbed on Cu2+-Mont. However, the major contribution for ΔG comes from enthalpy (Table 4). For all experiments, ΔS values were positive (Table 4), indicating that adenine adsorption onto montmorillonites increased the system disorder. It should be noted that for the samples with artificial seawater the variation in entropy was larger than the values calculated for the samples without artificial seawater (Table 4). In addition, the highest ΔS values were obtained for the samples of adenine dissolved in distilled water or artificial seawater adsorbed onto Fe3+-Mont (Table 4). Usually in the adsorption process, when the solute in the liquid phase is adsorbed by the solid, there is a reduction in the system disorder at the solid–liquid interface, as the solute loses some degree of freedom (including translation and rotation), so the entropy process is reduced (Mortland, Reference Mortland1970). In these experiments, the increase in entropy could be linked to the release of water from the hydration sphere of adenine or metals, or even by the adsorbed water on the clay (Mortland, Reference Mortland1970). This explanation is reinforced by the fact that the Fe3+-Mont samples showed the highest entropy variation. The ionic radius of Fe3+ (coordination number 6, 0.55 Å) is lower than that of Cu2+ (coordination number 6, 0.73 Å) and the charge of Fe3+is higher than that of Cu2+ (Haynes, Reference Haynes2017). Thus, Fe3+ has higher charge density. As a consequence, the hydration sphere of Fe3+ is larger than that of Cu2+. Therefore, the interaction of adenine with Fe3+ releases more water than the interaction of adenine with Cu2+.
Table 4. Thermodynamic parameters found for adenine adsorption onto different montmorillonites at distilled water or seawater 4.0 Gy
Each result is a mean of three experiments. Gibbs free energy (ΔG), enthalpy (ΔH), entropy (ΔS). Artificial seawater 4.0 Gy was prepared as described by Zaia (Reference Zaia2012). Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol l−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol l−1).
IR spectroscopy (FT-IR)
Figure 2 shows FT-IR spectra of the standard montmorillonite, washed with distilled water (Mont-STD), montmorillonite modified with FeCl3 solution (0.1 mol L−1) (Fe3+-Mont) and montmorillonite modified with CuCl2 solution (0.1 mol L−1) (Cu2+-Mont). The FT-IR spectrum of Mont-STD was very similar to the FT-IR spectrum of Cu2+-Mont and Fe3+-Mont (Fig. 2, Table 5). The FT-IR spectra showed four regions with bands at 520, 1012, 1630, 3388 and 3621 cm−1 (Fig. 2, Table 5). The band at 520 cm−1 could be attributed to the angular deformation of the Si–O bond of the clay (Tyagi et al., Reference Tyagi, Chudasama and Jasra2006). The broad band at 1012 cm−1 is due to the sum of several frequencies such as: Si–O deformation, O–H deformation of hydroxyl linked to Fe3+ and Al3+, Si–O–Si stretching and Si–O stretching (Bukka et al., Reference Bukka, Miller and Shabtai1992). The band at 1630 cm−1 could be attributed to hydration of clay or H–O–H bending (Bukka et al., Reference Bukka, Miller and Shabtai1992; Tyagi et al., Reference Tyagi, Chudasama and Jasra2006). The broad band at 3388 cm−1 and the band at 3621 cm−1 could be attributed to OH stretching, due to the hydration of clay, with both water and coordinated hydroxyl groups with mineral cations, e.g. Al3+, Mg2+, Fe3+, respectively (Bukka et al., Reference Bukka, Miller and Shabtai1992; Madejová, Reference Madejová2003; Tyagi et al., Reference Tyagi, Chudasama and Jasra2006).
Fig. 2. FT-IR spectra of different montmorillonites. Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol l−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol l−1).
Table 5. Assignments of frequencies (cm−1) in FT-IR spectra of Mont-STD, Mont-STD, Cu2+-Mont, Fe3+-Mont, adenine and adenine adsorbed onto Mont-STD, Cu2+-Mont and Fe3+-Mont
a Monts = Mont-STD, Cu2+-Mont and Fe3+-Mont showed the same bands.
b Tyagi et al. (Reference Tyagi, Chudasama and Jasra2006).
c Bukka et al. (Reference Bukka, Miller and Shabtai1992).
d Colthup et al. (Reference Colthup, Daly and Wiberly1964).
e Baú et al. (Reference Baú, Carneiro, de Souza Junior, de Souza, da Costa, di Mauro, Zaia, Coronas, Casado, de Santana and Zaia2012).
f Madejová (Reference Madejová2003).
Adenine has two characteristic bands at 1599 and 1671 cm−1 (Fig. 3) that can be attributed to the C=C stretch and NH2 bending, respectively (Colthup et al., Reference Colthup, Daly and Wiberly1964). After adenine adsorption on different montmorillonites, in both distilled water and 4.0 Ga seawater, the band at 1599 cm−1 shifted to the region of 1622–1626 cm−1; the band at 1671 cm−1 shifted to the region of 1697–1699 cm−1 (Fig. 3, Table 5). The displacement of the NH2 deformation band indicates that the interaction of adenine with mineral may occur through this functional group. However, StrašáK (Reference StrašáK1991) attributed the band in the region 1697–1699 cm−1 to the C=O stretching, after the adenine was adsorbed onto Cu2+-Mont reacted with Cu2+ forming hypoxanthine. Nevertheless, StrašáK (Reference StrašáK1991) assumed that this unique band could be due to hypoxanthine. It should be noted that Baú et al. (Reference Baú, Carneiro, de Souza Junior, de Souza, da Costa, di Mauro, Zaia, Coronas, Casado, de Santana and Zaia2012) studied the adsorption of adenine onto several synthetic zeolites, which do not contain Cu2+ and observed the same shift of the band 1671 cm−1. Carneiro et al. (Reference Carneiro, Berndt, de Souza Junior, de Souza, Paesano, da Costa, di Mauro, de Santana, Zaia and Zaia2011) using FT-IR spectroscopy observed the same shift in the adenine bands when several nucleic acid bases adsorbed onto sulfide modified montmorillonite. However, Mössbauer spectroscopy showed a decrease in the amount of Fe2+. Thus, further investigation of the adsorption of nucleic acid bases onto minerals bearing transition metals should be carried out to verify a possible reaction among them. The displacement of the C=C stretch band for the region of 1622–1626 cm−1 could not be attributed to an interaction of C=C with the mineral, since montmorillonite has a band at 1630 cm−1 attributed to clay hydration with water (Fig. 3, Table 5).
Fig. 3. FT-IR spectra: (a) adenine; (b) Mont-STD; (c) Mont-STD plus adenine in distilled water; (d) Mont-STD plus adenine in artificial seawater 4.0 Gy; (e) Cu2+-Mont; (f) Cu2+-Mont plus adenine in distilled; (g) Cu2+-Mont plus adenine in artificial seawater 4.0 Gy; (h) Fe3+-Mont; (i) Fe3+-Mont plus adenine in distilled water; (j) Fe3+-Mont plus adenine in artificial seawater 4.0 Gy. Adenine (500 mg l−1) was dissolved in distilled water or artificial seawater 4.0 Gy and adsorbed onto Mont-STD, Cu2+-Mont or Fe3+-Mont. Mont-STD is montmorillonite washed with distilled water. Cu2+-Mont is montmorillonite modified with CuCl2 solution (0.1 mol l−1). Fe3+-Mont is montmorillonite modified with FeCl3 solution (0.1 mol l−1). Artificial seawater 4.0 Gy was prepared as described by Zaia (Reference Zaia2012).
Implications for prebiotic chemistry
First, we should remember that due to exogenous and endogenous sources, prebiotic seas probably contain biomolecules (amino acids, nucleic acid bases, etc.), precursors of biomolecules (CN−, SCN−, NH3, CH2O, etc.), salts of seawater and metals. It is likely that prebiotic seas were a complex solution and all these substances could be adsorbed onto minerals. Thus, due to a large variety of species, this complex solution could lead to more possibilities for the formation of different and more complex molecules. However, this complex solution could not lead to the formation of any important molecule or biopolymer in high concentrations that could be used for the molecular evolution. If the latter occurs it is a dead end for prebiotic chemistry. This problem has been highlighted by Schwartz (Reference Schwartz2007), which he discussed in his article ‘Intractable mixtures and the origin of life’. In summary, to better understand what could have occurred on the Earth 4.0 Gy, prebiotic chemistry experiments should represent, as closely as possible, what happened on Earth. Iron is the fourth most abundant element in the Earth's crust (Cornell and Schwertmann, Reference Cornell and Schwertmann2003; Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008; Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018). In addition, although copper is not as abundant as iron, it could be easily found on prebiotic Earth (Hazen et al., Reference Hazen, Papineau, Bleeker, Downs, Ferry, McCoy, Sverjensky and Yang2008; Hazen, Reference Hazen2013; Morrison et al., Reference Morrison, Runyon and Hazen2018). Thus, it would be expected that minerals, including montmorillonite, contain iron and copper. Furthermore, these experiments were performed with artificial seawater that probably better resembles the major composition of cations and anions of the seas of prebiotic Earth. The most outstanding result of this work was that the adsorption of adenine onto modified montmorillonites depends on a complex interaction among adenine, salts in the seawater and Cu2+/Fe3+.The salts of artificial seawater plus Cu2+ or Fe3+ increased the amount of adenine adsorbed onto modified montmorillonites. For all the experiments ΔG was negative, meaning the adsorption of adenine onto montmorillonites is a spontaneous process. However, there were differences among them, with the adsorption of adenine onto Fe3+-Mont and Mont-STD or Cu2+-Mont ruled out by entropy and enthalpy/entropy, respectively. This difference comes from the higher charge density of Fe3+ compared with Cu2+. Thus, these data better represent what could have happened on the prebiotic Earth.
Conclusions
Montmorillonite modification with Cu2+ and Fe3+ decreased its surface area and pore volume, but pore size did not change. Among the isotherm models, the Sips model presented the best fit of the data. The n parameter of Sips indicated that the adenine adsorption process on the montmorillonites was homogeneous. Adenine dissolved in artificial seawater 4.0 Gy showed the highest adsorption (96.65 mg g−1) onto Fe3+-Mont at 60°C. The lowest adenine adsorption occurred when adenine was dissolved in distilled water (43.15 mg g−1) or artificial seawater 4.0 Gy (43.90 mg g−1) onto Mont-STD at 60°C. When adenine was dissolved in distilled water or artificial seawater 4.0 Gy, its adsorption onto Mont-STD and Cu2+-Mont was an exothermic process. However, for adenine dissolved in distilled water or artificial seawater 4.0 Gy, its adsorption onto Fe3+-Mont was an endothermic process. For all adsorptions ΔG was negative, meaning that adenine adsorption on different montmorillonites is a spontaneous and favourable process. The adsorption of adenine onto Fe3+-Mont was ruled out by entropy. For the other samples, the adsorption of adenine was ruled by enthalpy and entropy, being a major contribution for Gibbs free energy from enthalpy. Since the adsorption of adenine onto modified montmorillonites changed when carried out in artificial seawater, the adsorption of adenine onto modified montmorillonites involves a complex interaction among adenine, salts in seawater and Cu2+/Fe3+. The FT-IR data indicate that the interaction of adenine with mineral may occur through the NH2 functional group.
Acknowledgements
RCP acknowledges fellowship from CNPq. This research was supported by grant from CNPq/Fundação Araucaria (project number: 46824, Agreement: 11/2017, Title: Paranaense Nucleus of Studies in Complex Oxides).
Author contributions
Conceptualization: D.A.M.Z. and A.C.S.C.; writing first draft: R.C.P and B.S.T.; review and editing: D.A.M.Z. and A.C.S.C.; performed experiments: R.C.P and B.S.T. All authors have read and agreed to the published version of the manuscript.
Conflicts of interest
None.
