PREBIOTIC CHEMISTRY

Adsorption of Adenine and Thymine on Zeolites:FT-IR and EPR Spectroscopy and X-RayDiffractometry and SEM Studies

João Paulo T. Baú & Cristine E. A. Carneiro & Ivan G. de Souza Junior &

Cláudio M. D. de Souza & Antonio C. S. da Costa & Eduardo di Mauro &

Cássia T. B. V. Zaia & Joaquin Coronas & Clara Casado & Henrique de Santana &

Dimas A. M. Zaia

Received: 10 July 2011 /Accepted: 27 September 2011 /Published online: 20 October 2011# Springer Science+Business Media B.V. 2011

Abstract The interactions of adenine and thymine with and adsorption on zeoliteswere studied using different techniques. There were two main findings. First, asshown by X-ray diffractometry, thymine increased the decomposition of the zeolites(Y, ZSM-5) while adenine prevented it. Second, zeolite Y adsorbed almost the sameamount of adenine and thymine, thus both nucleic acid bases could be protected fromhydrolysis and UV radiation and could be available for molecular evolution. The X-ray diffractometry and SEM showed that artificial seawater almost dissolved zeolite A.The adsorption of adenine on ZSM-5 zeolite was higher than that of thymine(Student-Newman-Keuls test-SNK p<0.05). Adenine was also more greatly adsorbed onZSM-5 zeolite, when compared to other zeolites (SNK p<0.05). However the adsorptionof thymine on different zeolites was not statistically different (SNK p>0.05). Theadsorption of adenine and thymine on zeolites did not depend on pore size or Si/Al ratio

Orig Life Evol Biosph (2012) 42:19–29DOI 10.1007/s11084-011-9246-1

J. P. T. Baú : C. E. A. Carneiro : C. M. D. de Souza : H. de Santana :D. A. M. Zaia (*)Laboratório de Química Prebiótica, Departamento de Química-CCE,Universidade Estadual de Londrina, 86051-990 Londrina, PR, Brazile-mail: damzaia@uel.br

I. G. de Souza Junior :A. C. S. da CostaDepartamento de Agronomia-CCA, Universidade Estadual de Maringá, 87020-900 Maringá, PR, Brazil

E. di MauroLaboratório de Fluorescência e Ressonância Paramagnética Eletrônica (LAFLURPE)-CCE,Universidade Estadual de Londrina, 86051-990 Londrina, PR, Brazil

C. T. B. V. ZaiaDepartamento de Ciências Fisiológicas-CCB, Universidade Estadual de Londrina, 86051-990 Londrina,PR, Brazil

J. Coronas : C. CasadoChemical and Environmental Engineering Department and Instituto de Nanociencia de Aragón,Universidad de Zaragoza, 50018 Zaragoza, Spain

and it was not explained only by electrostatic forces; rather van der Waals interactionsshould also be considered.

Keywords Zeolites . Adenine . Thymine . Adsorption . Prebiotic chemistry

Introduction

Bernal (1951) was the first to suggest that minerals could have played an important role inthe pre concentration and polymerization of molecules on the prebiotic Earth, and severalpapers have explored how this may have occurred (Lahav and Chang 1976; Zaia 2004;Lambert 2008).

Zeolites are crystalline microporous aluminosilicates with periodic arrangements ofcages and channels that are synthesized in hydrothermal environments and can be found inseveral places on Earth as well as on Mars (Shock 1992; Smith 1998; Spray et al. 2010).Zeolites could have played an important role on the origin of life on Earth in theconcentration of biomolecules and the formation of biopolymers and primitive cells (Smith1998; Parsons et al. 1998). The Si/Al ratio in a zeolite is a property of paramountimportance that determines its main properties of catalysis, adsorption and ion exchange.Natural zeolites, with low Si/Al rations, are in general hydrophilic materials that upon lossof aluminum (through natural leaching) may experience a trend to become organophilicmaterials. Thus these materials could be used to concentrate organic molecules (Lethbridgeet al. 2005).

Nucleic acid bases have been synthesized in several experiments simulating theenvironments of the prebiotic Earth and have been found in meteorites (Basile et al.1984; Hua et al. 1995; Borquez et al. 2005; LaRowe and Regnier 2008). Thus, nucleic acidbases and zeolites could have been present on the prebiotic Earth and interactions amongthem could have occurred.

There are several papers describing the interactions of nucleic acid bases withminerals, most of these studies were carried out with clay minerals (Lailach et al.1968; Lailach and Brindley 1969; StrašáK 1991; Winter and Zubay 1995; Weckhuysen etal. 1999; Perezgasga et al. 2005; Hashizume and Theng 2007; Benetoli et al. 2008;Hashizume et al. 2010; Negrón-Mendoza et al. 2010; Pucci et al. 2010; Carneiro et al.2011a). Other minerals have also been studied such as: apatite (Winter and Zubay 1995),graphite (Sowerby et al., 2001a; b), metal sulfide (Sowerby et al. 1998; Bebié andSchoonen 2000; Plekan et al. 2007; Hatton and Rickard 2008) and rutile (Cleaves et al.2010).

Several of these articles report that minerals adsorb more adenine and/or cytosinethan thymine and/or uracil and usually this higher adsorption is due to electrostaticforces or ion exchange (Lailach and Brindley 1969; Sowerby et al. 2001b; Perezgasgaet al. 2005; Benetoli et al. 2008; Cleaves et al. 2010; Hashizume et al. 2010; Carneiro etal. 2011a). The higher adsorption of adenine when compared to the lower adsorption ofthymine raises some questions about the availability of thymine for the molecularevolution.

In the present work the adsorption of adenine, and thymine (Fig. 1) on zeolites (A, ZSM-5, Y)(Fig. 2) was studied. The nucleic acid bases were dissolved in artificial seawater whosecomposition had the major elements. The amount of nucleic acid bases adsorbed on clays wasmeasured. The interactions between nucleic acid bases and zeolites were studied by FT-IR andEPR spectroscopy, SEM and X-ray diffractometry.

20 J.P.T. Baú et al.

Materials and Methods

Materials

Zeolites

All zeolites were synthetic: zeolite A was provided by Industrias Químicas del Ebro(Zaragoza, Spain), while ZSM-5 and zeolite Y were purchased from Zeolyst InternationalValley Forge, PA, USA (Fig. 2).

Nucleic Acid Bases

All reagents were of analytical grade, all nucleic acids bases (Fig. 1) were purchase fromAcros Organics (USA) and were used as received.

Seawater

The following substances were weighed and dissolved in 1.0 L of distilled water:0.488 mol L−1 sodium chloride, 19.0 10−3 mol L−1 magnesium chloride, 7.2 10−3 mol L−1

magnesium sulfate, 7.6 10−3 mol L−1 calcium sulfate, 4.8 10−3 mol L−1 potassium sulfate,8.6 10−4 mol L−1 potassium bromide, and 4.5 10−4 mol L−1 boric acid.

Sample Preparation

The solutions of adenine and thymine were dissolved in seawater at the concentration of720 μg mL−1 or as a saturated solution. Each zeolite, 25 mg, was placed in a separate

Fig. 2 Zeolite A, viewed from the [100] face (a); ZSM-5, viewed from the [010] face (b) and zeolite Y,viewed from the [111] face (c). Structures of zeolites (2011)

Fig. 1 Molecular structures ofthe nucleic acid bases studied inthis work. The position numbersshown are arbitrary (non IUPAC)labels

Adsorption of Adenine and Thymine on Zeolites 21

Eppendorff tube (1.5 mL) containing either: (a) 1.0 mL of artificial seawater, (b) 1.0 mL ofartificial seawater with 720 μg mL−1 of adenine or thymine, or (c) 1.0 mL of artificial seawaterwith saturated solution of adenine or thymine. To standardize the pH of the solutions they wereadjusted to 1.50 with HCl. The tubes were stirred for 24 h before being centrifuged (“HT”-HB-003-84019-0, rotor 2.0 cm) for 5 min. at 6,000 rpm. The aqueous phase (720 μg mL−1

solution) was used for adenine and thymine analysis, and the solid (saturated solution) waslyophilized and analyzed using FT-IR and EPR spectroscopy, SEM and ray-X diffractometry.

Methods

FT-IR Spectroscopy

The IR spectra were recorded with a Shimadzu 8300 FT-IR spectrophometer. KBr discpellets were prepared and spectra were recorded from 400 to 4000 cm−1 with a resolution of4 cm−1, after 98 scans. FT-IR spectra were analyzed using the Origin program (8.0, 2007).

UV Spectrophotometric Methods

Absorbance was read with a Shimadzu UV–vis spectrophotometer. Adenine and thyminewere determined by reading the absorbance in the UV region (260–265 nm). The followingequation was used for the calculation of the amount of base adsorbed on zeolite.

Cadsorbed mg= ¼ Cinitial � Csolutionð Þ; where Csolution ¼ Cinitialð Þ Abssample ¼ Absinitial� �� �

Electron Paramagnetic Resonance (EPR) Spectroscopy

The samples were submitted to EPR experiment at X-band (ca. 9 GHz) with 20 Gmodulation amplitude and magnetic field modulation 100 kHz using a JEOL (JES-PE- 3X)spectrometer at room temperature. Mn2+:MgO was used as a g-marker and standard of lineintensity, using its fourth spectral line (g=1.981).

X-Ray Diffractometry

Zeolites were analyzed by powder X-ray diffraction using a Shimadzu D 6000 diffractometerusing Co Kα radiation (40 kV, 30 mA) and an iron filter in a step-scanning mode (0.02°2θ/0.6 s). All peak positions were analyzed using Grams 8.0 software.

Scanning Electron Microscopy (SEM)

SEM images were taken on a Philips model Quanta 200 (FEI) SEM, in Scanning ElectronMicroscope and Microanalysis laboratory of the UEL (Universidade Estadual de Londrina),equipped with an energy dispersive X-ray (EDX) model INCA 200 at 30 keV. The samples werefixed on ‘stubs’ using carbon adhesive tape and then coated with a 30 nm thick layer of gold.

Statistical Analysis

The ANOVA and Student–Newman–Keuls test (SNK test) were used for the comparisonsbetween means at a significance level of p<0.05.

22 J.P.T. Baú et al.

Results and Discussion

Table 1 shows Si/Al ratio, pore size, net charge of the zeolites (NCZ), pH of theexperiments, net charge of nucleic acid bases (NCNAB) and amount of thymine andadenine adsorbed on zeolites. It should be noticed that zeolites are negatively charged(Table 1) and this charge is independent of the pH of the solution (Lambert 2008). Theadsorption of adenine and thymine on zeolites did not depend on pore size and Si/Al ratios(Table 1). The adsorption of adenine on ZSM-5 zeolite was higher than that of thymine(SNK p<0.05) (Table 1).This higher adsorption of adenine than thymine on ZSM-5 zeolitecould be due to electrostatic forces between the ZSM-5 zeolite (negatively charged) andadenine (positively charged) (Table 1). Other authors also observed a higher adsorption ofadenine than thymine on: graphite (Sowerby et al. 2001a, b) and clays (Lailach et al. 1968;Lailach and Brindley 1969; Benetoli et al. 2008; Carneiro et al. 2011a). However eventhough adenine is positively charged it did not adsorb more than thymine on Y-zeolite(negatively charged) and A-zeolite (negatively charged) (SNK p>0.05) (Table 1). Probablyin this case van der Waals forces are playing the main role in the adsorption. Adenine wasadsorbed more on ZSM-5 zeolite, compared to other zeolites (SNK p<0.05) (Table 1).However the adsorption of thymine on zeolites was not statistically different from eachother (SNK p>0.05) (Table 1).

Table 2 shows adenine/thymine adsorption ratios for zeolites, clays, graphite andadenine/thymine ratios in the living organisms. The adenine/thymine ratios for the Y-zeoliteand A-zeolite were closer to those of living organisms (Table 2). On the other hand claysand graphite adsorbed much more adenine than thymine (Table 2). The almost sameadsorption of adenine and thymine on Y and A-zeolites is an important result for prebioticchemistry since both nucleic acid bases could be protected from hydrolysis or UVdegradation, thus they would be available for molecular evolution. The protection ofbiomolecules by minerals against UV irradiation is well known (Biondi et al. 2007;Kranksith et al. 2010). Carneiro et al. (2011a) observed that when adenine and thyminewere adsorbed on modified montmorillonite with sodium sulfide at pH 7.00 the adenine/thymine ratios were closer to 1.00. This effect was possibly due to the neutralization of thecharges of montmorillonite by sulfide making it more organophilic (like a zeolite). It shouldalso be pointed out that zeolites adsorbed almost the same amount of amino acids with andwithout charged R-groups (Carneiro et al. 2011b). As reviewed by Zaia (2004) minerals

Table 1 Amount of thymine and adenine adsorbed on zeolites

Base Zeolite Si/Al Pore size nm *Range of pH Amount adsorbed μg **NCZ/NCNAB

Adenine ZSM-5 25 0.55 1.49–1.66 685.7±10.7a −/+Zeolite Y 60 0.74 2.46–2.69 251.9±24.0b −/+Zeolite-A 1 0.41 3.32–3.63 229.5±23.7b −/+

Thymine ZSM-5 25 0.55 1.32–1.50 226.6±6.9b −/0Zeolite Y 60 0.74 1.63–2.69 205.2±24.3b −/0Zeolite-A 1 0.41 3.32–3.58 193.0±23.1b −/0

Results are presented as mean±standard error of mean. The number of sets was five or four with two sampleseach set. *Ranges of pHs after the samples were mixed 24 h, the pHs were adjusted at time t=0, pH=1.50.**NCZ=net charge zeolite as described by Lambert 2008, NCNAB=net charge of nucleic acid base asdescribed by Carneiro et al. 2011. ANOVA test F=69.97and p=0.000, SNK test (p<0.05) a/b

Adsorption of Adenine and Thymine on Zeolites 23

adsorb more amino acids with positively/negatively charged R-groups (Asp, Glu, Arg,Lys, His) than amino acids with uncharged R-groups. Klapper (1977) studied theaverage occurrence of amino acids in over 200 proteins and showed that proteins have thefollowing composition: 40.1% amino acids with non-polar aliphatic R groups; 8.1%amino acids with aromatic R groups; 25.9% amino acids with polar uncharged R groups;11.7% amino acids with negatively charged R groups; and 13.8% amino acids withpositively R charged groups. Then about 75% of the amino acids of the proteins haveuncharged R-group. Thus, we should look for mechanisms that concentrate these aminoacids and the adsorption of amino acids on zeolites could be a solution for this problem.These results are expected since zeolites can be, in general, organophilic materials(Lethbridge et al. 2005).

Table 2 Adenine/Thymine ratios

*A/T **A/T ***A/T-organism

3,03-ZSM-5 From 3.26 to 114.5, montmorillonite 1.05-homo sapiens

(Lailach et al., 1969)

1,23-Y 3.1 graphite 1.03-sheep

(Sowerby et al. 2001b)

1,04-A From 4.68 to 25.1, clays 1.02-chicken

(Benetoli et al. 2008)

From 0.79 to 3.87, Clays 1.05-turtle

(Carneiro et al., 2011)

1.02-salmon

1.02-sea urchin

1.00-grasshopper

0.95-yeast

1.04-E. coli

1.05-Staphylococcus aureus

A adenine, T thymine.*A/T ratios of the present paper. **A/T ratios obtained by several authors. ***A/Tratios of several organisms (Lehninger 1984)

1500 1550 1600 1650 1700 1750 18000

1

2

3

0,0

0,5

1,0

1,5

1636

1683

1722

1677

1741

b

wavenumber (cm-1)

a

1604

1636

1673

1696

Ab

sorb

ance

(a.

u.)

Fig. 3 FT-IR spectra, A: ZSM-5solid ( ); adenine solid( ); ZSM-5 mixed withartificial seawater ( );adenine adsorbed on ZSM-5( ). B: ZSM-5 solid( ); thymine solid ( );ZSM-5 mixed with artificialseawater ( ); thymineadsorbed on ZSM-5 ( )

24 J.P.T. Baú et al.

Figure 3 shows the FT-IR spectra of ZSM-5 solid, ZSM-5 after mixing withartificial seawater, adenine and thymine solids and adenine and thymine adsorbed onZSM-5. The FT-IR spectra of the zeolites with and without artificial seawater are thesame (Figure not shown). The FT-IR spectrum of adenine solid shows bands at1604 cm−1 and 1673 cm−1 attributable to C=N stretching and NH2 deformation,respectively (Colthup et al. 1964). ZSM-5 zeolite solid or mixed with artificial seawatershowed a band in the region of 1636 cm−1 attributable to water O-H bending. Whenadenine was adsorbed on ZSM-5 the band at 1673 cm−1 shifted to 1696 cm−1 while theband at 1604 cm−1 shifted to the same region of the 1636 cm−1 O-H bending band of thezeolite (Fig. 3a). Because of the shift the band at 1673 cm−1 to 1696 cm−1, the interactionbetween adenine and ZSM-5 was through 5NH2 (Fig. 1). Chen et al. (2002), Yamada et al.(2004) and Furukawa et al. (2007) studied the adsorption of adenine on Cu (110) and alsoobserved the interaction was through 5NH2 of adenine. According to Benetoli et al.(2008) and Carneiro et al. (2011a) the interaction between adenine and clays was through5NH2

+ group the adsorption of adenine on clays was studied. They proposed that thisgroup was positively charged since clays are very acidic substances. On the other hand,McNutt et al. (2003) proposed that interaction between adenine and Cu (110) was through2N and 3NH (Fig. 1).

FT-IR spectrum of thymine solid shows bands at 1677 cm−1 and 1741 cm−1 thatcould be attributed to C=C and C=O stretching, respectively (Fig. 3b) (Aroca andBujalski 1999). FT-IR spectrum of thymine adsorbed on ZSM-5 showed three bands at1636 cm−1, 1683 cm−1 and 1722 cm−1. The band at 1636 cm−1 could be due to ZSM-5mixed with artificial seawater, the bands at 1683 cm−1 and 1722 cm−1 were shifted due toC=C and C=O stretchings, respectively (Fig. 3b). Similar results were obtained byBenetoli et al. (2008) and Carneiro et al. (2011a) when thymine was adsorbed on clays.The weakening of the C=C and C=O bonds could be an indication that the interactionbetween thymine and ZSM-5 was through 2NH group (Fig. 1). On the other hand,Yamada et al. (2004) proposed that interaction between thymine and Cu (110) wasthrough 1NH.

FT-IR spectra (Figure not shown) of thymine adsorbed on zeolites A and Y and adenineadsorbed on zeolite A exhibited a broad band in 1643 cm−1 that could be due to zeolitesmixed with artificial seawater. However, for adenine adsorbed zeolite Y (Figure not shown)besides the broad band at 1643 cm−1 a band at 1700 cm−1 due to the shift of the band at1674 cm−1 was also observed.

Table 3 shows EPR intensity lines of the samples of pure zeolites. These resonance linesare due to hydroxides and oxides of Fe3+ (g≈2), Fe3+ with rhombic symmetry (g≈3.7) andFe3+ rhombohedral distorted symmetry (g≈6.9) (Guskos et al. 2002; Carbone et al. 2005;Budziak et al. 2007; Mota et al. 2009). The intensity of these lines were almost at thedetection limit of the equipment. This was expected since the industrial zeolites may havetraces of Fe remaining from the crystallization reagents (Nichols et al. 2006). Theseamounts of Fe likely do not have a large effect on the adsorption of adenine or thymine onthe zeolites.

Zeolite g≈2 g≈3.7 g≈6.9

ZSM-5 0.26 0.21 0.13

Y 0.10 0.14 0.10

A 0.09 0.17 0.11

Table 3 Resonance line intensitiesof Fe3+ of pure zeolites

Adsorption of Adenine and Thymine on Zeolites 25

X-ray diffraction (XRD) data for the zeolites after the adsorption experimentsshowed significant differences among the porous solids (Fig. 2). After the sampleswere mixed with artificial seawater and centrifuged and lyophilized, halite diffractionpattern was observed (Fig. 4). In the presence of both nucleobases, gypsum alsoprecipitated from solution due to high sulphate concentration in the seawater and theincrease of the solution ionic strength with the dissolution of the zeolite (Fig. 4)(Barcelona et al. 1976). Zeolite A was almost dissolved completely by the artificialseawater and only small intensity diffraction peaks were observed joint to intense (Fig. 4).The instability of zeolite A at low pH has been reported many times (de la Iglesia et al.2007). The dissolution of zeolite A was also confirmed by SEM (Figure not shown).However, it should be noticed that FT-IR spectrum of this zeolite did not indicate anydecomposition (Figure not shown).

The presence of thymine or adenine as a discrete solid phase was not observed in any ofthe zeolites demonstrating that adsorption is low at the surface of the zeolites and are notdetected by XRD. Discrete phases would be observed by XRD in concentrations greaterthan 3% (30,000 ppm) (Cullity 1978).

Zeolites Y and ZSM-5 were not dissolved at acidic pH but their crystallinity wasaffected. Diffraction peaks presenting lower intensities and larger width at half height (FullWidth Half Maximum-FWHM). For zeolite Y, this was more intense in presence of thyminethan in the presence of adenine (Fig. 4). An excess of negative charge on thymine surfacedue to carbonyl complexing groups, not present on the adenine, might enhance thecomplexation of hydroxyls from the silanol groups, destabilizing the solid structures andthus promoting their dissolution (Sposito 1989; Huang and Longo 1992) In the presence ofboth nucleobases adenine protects the zeolite surfaces against the dissolution induced bythymine (Fig. 4).

Conclusion

In conclusion this paper shows that adenine and thymine are adsorbed on zeolites at lowpH. Adenine was more adsorbed on ZSM-5 zeolite than thymine and electrostatic forces arelikely involved. However the adsorption of adenine and thymine on zeolites Y and A wereprobably due to van der Waals forces and other interactions.

The adenine/thymine adsorption ratio for zeolite Y was about 1.00. Both nucleic acidbases could be protected from hydrolysis and UV radiation and consequently could beavailable for molecular evolution.

As shown by infrared spectroscopy the interaction of adenine and thymine with ZSM-5zeolite was likely via 5NH2 and

2NH, respectively. However, the adsorption of thymine onzeolites A and Y and adenine on zeolite A did not show any characteristic bands of thisinteraction.

The EPR spectra showed that the amount of Fe present likely did not contribute to theadsorption of the bases, since the concentration of Fe is very low.

X-ray diffraction data and SEM showed that zeolite A was almost entirely dissolved byartificial seawater while the crystallinity of zeolite Y and ZSM-5 decreased. Thymineenhanced the dissolution of zeolites, but adenine protected them.

�Fig. 4 X-ray diffraction spectra of pure zeolites, zeolites after mixed with artificial seawater and nucleic acidabases adsorbed on zeolites. Z: zeolite ZSM-5; Y: zeolite-Y; A: zeolite-A; H: halite (NaCl)lita; G: gypsum(CaSO42.H2O)

26 J.P.T. Baú et al.

ZSM + adenine + thymine

Hd 20

0Z

d 533

Zd 6

22

Zd 05

3

Zd 60

2

Zd 45

1

Zd 50

2

Zd 43

2

Zd 13

3

Zd 03

3

Zd 50

1

Zd 3

22

Zd 01

3

Zd 40

1

Zd 04

0

Zd 0

22

Zd 31

1

Zd 11

2

Zd 10

2

Zd 0

02

Zd 20

1

Zd 21

1

Zd 2

00

Zd 10

1

ZSM pH 2

ZSM

ZSM + adenine

ZSM + thymine

Y + adenine + thymine

Yd 84

0

Yd 66

4

Yd

753

Hd 20

0

Yd 55

5

Yd 66

0

Yd 73

3

Yd 73

1

Yd 64

2

Yd 55

1

Yd 44

4

Yd 53

3

Yd 62

0

Yd 4

40

Yd 3

33

Yd 33

1

Yd 31

1

Yd 22

0

Yd 1

11

Y pH 2

Y

Y + adenine

Y + thymine

5 10 15 20 25 30 35 40

A + adenine + thymine

Gd 22

0

Gd 2

20

Gd 02

0 Hd 11

1

Hd 2

00

Ad 6

44

Ad 84

0 Ad 84

2

Ad 6

44

Ad 64

2

Ad 6

40

Ad 6

22

Ad 6

20

Ad 60

0

Ad 44

0

Ad 42

0

Ad 22

2

Ad 22

0

CoK , º2

A pH 2

A

A + adenine

A + thymine

Ad 20

0

Adsorption of Adenine and Thymine on Zeolites 27

Acknowledgments JPTB and CMDS and CEAC acknowledge the fellowships from PIBIC/CNPq andCapes, respectively. The authors are grateful to Dr. Alan W. Schwartz for the reviewing the text. The authorsalso are grateful to one anonymous reviewer for the suggestions. This research was supported by grants fromCNPq (474985/2010-5) and Fundação Araucária (15279/2009).

References

Aroca R, Bujalski R (1999) Surface enhanced vibrational spectra of thymine. Vib Spectrosc 19:11–21Barcelona MJ, Tosteson TT, Atwood DK (1976) Study PF organic-calcium interactions: gypsum

precipitation in tropical surface waters. Marine Chem 4:89–92Basile B, Lazcano A, Oró J (1984) Prebiotic syntheses of purines and pyrimidines. Adv Space Res 4:125–131Bebié J, Schoonen MAA (2000) Pyrite surface interaction with selected organic aqueous species under

anoxic conditions. Geochem Trans. doi:10.1039/b005581fBenetoli LOB, de Santana H, Zaia CTBV, Zaia DAM (2008) Adsorption of nucleic acid bases on clays: an

investigation using Langmuir and Freundlich isotherms and FT-IR spectroscopy. Monatsh Chem 139:753–761Bernal JD (1951) The physical basis of life. Routledge and Kegan Paul, LondonBiondi E, Branciamore S, Maurel MC, Gallori E (2007) Montmorillonite protection of an UV-irradiated

hairpin ribozyme:evolution of the RNA world in a mineral environment. BMC Evol Bio 7(Suppl 2):s2.doi:10.1186/1471-2148-7-S2-S2

Borquez E, Cleaves HJ, Lazcano A, Miller SL (2005) An investigation of prebiotic purine synthesis from thehydrolysis of HCN polymers. Orig Life Evol Biosph 35:79–90

Budziak CRF, Wypych F, Mangrich AS (2007) Use of Fe3+ ion probe to study the stability of urea-intercalated kaolinite by electron paramagnetic resonance. J Coll Inter Sci 313:537–541

Carbone C, di Benedetto F, Marescotti P, Sangregorio C, Sorace L, Lima N, Romanelli M, Luchetti G,Cipriani C (2005) Natural Fe-oxide and -oxyhydroxide nanoparticles: an EPR and SQUID investigation.Mineral Petrol 85:19–32

Carneiro CEA, Berndt G, de Souza Junior IG, de Souza CMD, Paesano Jr. A. da Costa ACS, di Mauro E, deSantana H, Zaia CTBV, Zaia DAM (2011a). Adsorption of adenine, cytosine, thymine and uracil onsulfide-modified montmorillonite: FT-IR, Mössbauer and EPR Spectroscopy and X-ray diffractometrystudies. Orig. Life Evol. Biosph. In press.

Carneiro CEA, de Santana H, Casado C, Coronas J, Zaia DAM (2011b) Adsorption of amino acids (Ala,Cys, His, Met) on zeolites: FT-IR and Raman spectroscopy investigations. Astrobiology 11:409–418

Chen Q, Frankel DJ, Richardson NV (2002) Self assembly of adenine on Cu (100) surfaces. Langmuir18:3219–3225

Cleaves HJ, Jonsson CM, Jonsson CL, Sverjensky DA, Hazen RM (2010) Adsorption of nucleic acidcomponents on rutile (TiO2) surfaces. Astrobiology 10:311–323

Colthup NB, Daly LH, Wiberly SE (1964) Introduction to Infrared and Raman Spectroscopy. Academic,New York

Cullity BD (1978) Elements of X-ray Diffraction. Addison-Wesley, Reading, Massde la Iglesia O, Mallada R, Menéndez M, Coronas J (2007) Continuous zeolite membrane reactor for

esterification of ethanol and acetic acid. Chem Engin J 131:35–39Furukawa M, Yamada T, Katano S, Kawai M, Ogasawara H, Nilsson A (2007) Geometrical characterization

of adenine and guanine on Cu (110) by NEXAFS, XPS and DFT calculation. Surf Sci 601:5433–5440Guskos N, Papadopoulos GJ, Likodimos V, Patapis S, Yarmis D, Przepiera A, Przepiera K, Majszczyk J, Typek J,

Wabia M, Aidinis K, Drazek Z (2002) Photoacoustic, EPR and electrical conductivity investigations of threesynthetic mineral pigments: hematite, goethite and magnetite. Mater Res Bull 37:1051–1061

Hashizume H, Theng BKG (2007) Adenine, adenosine, ribose and 5’-AMP adsorption to allophane. ClaysClay Miner 55:599–605

Hashizume H, Van der Gaast S, Theng BKG (2010) Adsorption of adenine, cytosine, uracil, ribose, andphosphate by Mg-exchanged montmorillonite. Clays Clay Miner 45:469–475

Hatton B, Rickard D (2008) Nucleic acid binds to nanoparticulate iron (II) monosulphide in aqueoussolutions. Orig Life Evol Biosph 38:257–270

Hua LL, Kobayashi K, Ochiai EI, Gehrke CW, Gerhardt KO, Ponnamperuma C (1995) Identification andquantification of nucleic acid bases in carbonaceous chondrites. Orig Life Evol Biosph 16:226–227

Huang WL, Longo JM (1992) The effect of organics on feldspar dissolution and the development ofsecondary porosity. Chem Geol 98:271–292

Klapper MH (1977) Independent distribution of amino acids near neighbor pairs into polypeptides. BiochemBiophys Res Comm 78:1018–1024

28 J.P.T. Baú et al.

Kranksith LLE, Negrón-Mendoza A, Mosqueira FG, Ramos-Bernal S (2010) Radiation-induced reactions ofamino acids adsorbed on solid surfaces. Nucl Instrum Meth Phys Res A 619:51–54

Lahav N, Chang S (1976) The possible role of solid surface area in condensation reactions during chemicalevolution. J Mol Evol 8:357–380

Lailach GE, Brindley GW (1969) Specific co-absorption of purines and pyrimidines by montmorillonite(Clay-organic studies XV). Clays Clay Miner 17:95–100

Lailach GE, Thompson TD, Brindley GW (1968) Adsorption of pyrimidines, purines and nucleosides by Co,Ni, Cu, and Fe (III)-montmorillonite (Clay-organic studies XIII). Clays Clay Miner 16:295–301

Lambert JF (2008) Adsorption and polymerization of amino acids on minerals surfaces: a review. Orig LifeEvol Biosph 38:211–242

LaRowe DE, Regnier P (2008) Thermodynamic potential for the abiotic synthesis of adenine, cytosine, guanine,thymine, uracil, ribose and deoxyribose in hydrothermal sytems. Orig Life Evol Biosph 38:383–397

Lehninger AL (1984) Princípios de Bioquímica. Sarvier Editora de Livro Técnicos Ltda, São Paulo-SP, 574Lethbridge ZAD, Williams JJ, Walton RI, Evans KE, Smith CW (2005) Methods for the synthesis of large

crystals of silicate zeolites Micropor. Mesopor Mater 79:339–352McNutt A, Haq S, Raval R (2003) RAIRS investigations on the orientation and intermolecular interactions of

adenine on Cu (110). Surf Sci 531:131–144Mota L, Toledo R, Faria RTJr, da Silva EC, Vargas H, Deladillo-Hotfort I (2009) Thermally treated soli clays

as ceramic raw materials: characterization by x-ray diffraction, photoacoustic spectroscopy and electronspin resonance. Appl Clay Sci 43:243–247

Negrón-Mendoza A, Ramos-Bernal S, de Buen IG (2010) A thermoluminescence study of bio-organiccompounds adsorbed in a clay mineral. IEEE Trans Nucl Sci 57:1223–1227

Nichols WT, Kodaira T, Sasaki Y, Shimizu Y, Sasaki T, Koshizaki N (2006) Zeolite LTA NanoparticlesPrepared by Laser-Induced Fracture of Zeolite Microcrystals. J Phys Chem B 110:83–89

Parsons I, Lee MR, Smith JV (1998) Biochemical evolution II: Origin of life in tubular microstructures onweathered feldspar surfaces Proc. Natl Acad Sci USA 95:15173–15176

Perezgasga L, Serrato-Díaz A, Negrón-Mendonza A, de Pablo GL, Mosqueira FG (2005) Sites of adsorptionof adenine, uracil, and their corresponding derivatives on sodium montmorillonite. Orig Life EvolBiosph 35:91–110

Plekan O, Feyer V, Šutara F, Skála T, Švec M, Cháb V, Matolín V, Prince KC (2007) The adsorption ofadenine on mineral surfaces: iron pyrite and silicon dioxide. Surf Sci 601:1973–1980

Pucci A, Branciamore S, Casarosa M, D’Acqui LP, Gallori E (2010) Implications for an RNA-clay world:interaction of cytosine with clays minerals. J Cosmol 10:3398–3407

Shock EL (1992) Chemical environments of submarine hydrothermal systems. Orig Life and Evol Biosph22:67–102

Smith JV (1998) Biochemical evolution I. Polymerization on internal, organophilic silica surfaces ofdealuminated zeolites and feldspars. Proc Natl Acad Sci USA 95:3370–3375

Sowerby SJ, Edelwirth M, Reiter M, Heckl WM (1998) Scanning tunneling microscopy image contrast as afunction of scan angle in hydrogen bonded self assembled monolayers. Langmuir 14:5195–5202

Sowerby SJ, Mörth CM, Holm NG (2001a) Effect of temperature on the adsorption of adenine. Astrobiology1:481–487

Sowerby SJ, Cohn CA, Heckl WM, Holm NG (2001b) Differential adsorption of nucleic acid bases:relevance to the origin of life. Proc Natl Acad Sci USA 98:820–822

Sposito G (1989) The chemistry of soil. Oxford University Press, New York, p 277Spray JG, Thompson LM, Biren MB, O’Connell-Cooper C (2010) The Manicouagan impact structure as

terrestrial analogue site for lunar and martian planetary science. Plan Space Sci 58:538–551StrašáK M (1991) An unsual reaction of adenine and adenosine on montmorillonite. Naturwissenschaften

78:121–122Structures of zeolites (2011). The structures of ZSM-5, A and Y were taken from the International Zeolite

Association Database (Baerlocher and McCusker). Color images available online at http://www.iza-structure.org/databases.

Weckhuysen BM, Leeman H, Schoonheydt RA (1999) Synthesis and spectroscopy of clay intercalated Cu(II) bio-monomer complexes: coordination of Cu (II) with purines and nucleotides. Phys Chem ChemPhys 1:2875–2880

Winter D, Zubay G (1995) Binding of adenine and adenine related compounds to the clay montmorilloniteand the mineral hydroylapatite. Orig Life Evol Biosph 25:61–81

Yamada T, Shirasaka K, Takano A, Kawai M (2004) Adsorption of cytosine, thymine, guanine and adenineon Cu (110) studied by infrared reflection absorption spectroscopy. Surf Sci 561:233–247

Zaia DAM (2004) A review of adsorption of amino acids on minerals: was it important for origin of life?Amino acids 27:113–118

Adsorption of Adenine and Thymine on Zeolites 29