Ultraviolet Irradiation on a Pyrite Surface Improves Triglycine Adsorption

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Article Ultraviolet Irradiation on a Pyrite Surface Improves Triglycine Adsorption

Santos Galvez-Martinez and Eva Mateo-Marti *

Centro de Astrobiología (CSIC-INTA), Ctra. Ajalvir, Km. 4, 28850 Torrejón de Ardoz, Spain; [email protected] * Correspondence: [email protected]; Tel.: + 34-915-872-973

Received: 27 July 2018; Accepted: 9 October 2018; Published: 25 October 2018

Abstract: We characterized the adsorption of triglycine molecules on a pyrite surface under several simulated environmental conditions by X-ray photoemission spectroscopy. The triglycine molecular adsorption on a pyrite surface under vacuum conditions (absence of oxygen) shows the presence of + two different states for the amine functional group (NH2 and NH3 ), therefore two chemical species (anionic and zwitterionic). On the other hand, molecular adsorption from a solution discriminates the NH2 as a unique molecular adsorption form, however, the amount adsorbed in this case is higher than under vacuum conditions. Furthermore, molecular adsorption on the mineral surface is even favored if the pyrite surface has been irradiated before the molecular adsorption occurs. Pyrite surface chemistry is highly sensitive to the chemical changes induced by UV irradiation, as XPS analysis shows the presence of Fe2O3 and Fe2SO4—like environments on the surface. Surface chemical changes induced by UV help to increase the probability of adsorption of molecular species and their subsequent concentration on the pyrite surface.

Keywords: pyrite; triglycine; XPS; peptide; sulfide mineral; UV; surface; adsorption; prebiotic chemistry

1. Introduction Minerals can be very promising surfaces for studying biomolecule surface processes, which are of principal relevance in the origin of life and a source of chemical complexity [1,2]. Bernal proposed that mineral surface adsorption could help to overcome the problem of the extremely dilute concentration of amino acids in prebiotic oceans [3]. Minerals such as silicates, oxides and sulfides were probably present on early Earth in several environments [4,5], and among them, pyrite (FeS2) is one of the most important and abundant sulfide minerals on Earth. Indeed, many redox-based geochemical and biogeochemical processes, such as the cycling of S, Fe, and other elements in the environment or in deposit formation, occur on the surface of pyrite [6]. Additionally, due to its catalytic activity, the pyrite surface plays an important role in heterogeneous catalysis [7,8] and a role in the origin of life and prebiotic chemistry [9,10]. Huber and Wächtershäuser proposed the theory of an “iron–sulfur world” [11] in that the first reactions that led to the formation of amino acids occurred on the surface of minerals (such as pyrite) because such surfaces may adsorb and concentrate these biomolecules and catalyse the reactions. It has been proposed that the first reactions that led to the formation of amino acids did not occur in a bulk solution in oceans but on the surface of minerals because such surfaces have the potential to facilitate prebiotic polymerization [12–14]. The presence of iron-sulfur cores in several modern proteins, such as ferredoxins, has been offered as additional evidence for the “iron-sulfur” world hypothesis.

Life 2018, 8, 50; doi:10.3390/life8040050 www.mdpi.com/journal/life Life 2018, 8, 50 2 of 12

Mineral surfaces could potentially allow for almost any type of general catalysis, with low specificity and efficiency. Understanding the possible contribution of mineral surfaces to peptide oligomerization and how minerals could play a relevant role in concentrating biomolecules at the surface and/or providing catalytic sites on the surface is critical for understanding the origin of life [10–15]. The adsorption of small molecules onto specific mineral surfaces for selective concentration [16], catalytic polymerization [17], protection from UV light [18], etc., is critical for understanding the selective mechanisms for the accumulation of amino acids or nucleotides involved in chemical evolution. The surrounding mineral conditions affect the surface processes and how the molecular and physicochemical inorganic aspects drive the prebiotic chemistry process. In primitive Earth studies, special attention must be paid to inorganics interacting with organics [19] under different environmental conditions. Moreover, on terrestrial planets, such as Mars [20] and primitive Earth, a lack of an ozone layer in the first stages was possible, with a strong ultraviolet (UV) irradiation acting as a potential driving force for chemical activation [21–25]. Therefore, the role of mineral surfaces [26] would be crucial for studies on the origin of life in this context. A detailed study of the pyrite UV oxidation process and reactivity of molecule/pyrite systems at the molecular level is fundamental to understanding the chemistry of this mineral in a wide variety of environments. Oxidation studies have shown that pyrite is reactive under ambient conditions and oxidizes rapidly in air, forming ferric sulfate. Other possible oxidation products including Fe-hydroxide or Fe-oxyhydroxide, monosulfide, disulfide and polysulfide are also formed. The formation of these oxidation products depends on the conditions and duration of the oxidation process. However, little is known about the surface chemistry of pyrite under vacuum conditions (simulated absence of oxygen), and few studies concerning oxidation, hydration and desulfurization reactions on pyrite surfaces have been reported [27,28]. The adsorption of amino acids on the surface of pyrite has been studied experimentally and theoretically [29,30]. The surface of pyrite has a rich chemistry due to the surface defect sites, where either iron or sulfur ions are exposed and can serve as adsorption sites for various ionic species. It has been reported by our group that sulfur enrichment drives molecular adsorption on pyrite, and the pyrite surface structure could dictate its molecular adsorption and reactivity properties, having relevant implications for prebiotic chemistry surface reactions. It is important to explore the role-played by the mineral surfaces related to the prebiotic chemistry processes, such as molecular adsorption and geochemistry, and therefore, we focused our study on investigating the possible role played by mineral surface reactivity. Our recent experiments have suggested that amino acids and small peptides can adsorb onto the mineral surfaces, depending on their structures, which are affected by the surroundings or surface pretreatment conditions. These studies provided some new insights into the adsorption process on surfaces. This strategy is designed to be able to evaluate how diverse environments favour or inhibit molecular adsorption and the crucial role played by mineral surfaces chemically driving amino-acids interactions. Even if amino acids only provide an interesting starting point for studying mineral—biomolecule interactions, small peptides could be a good way to achieve molecular complexity on surfaces. Triglycine (Figure1) is an amino-acid trimer formed by three glycine molecules (Gly-Gly-Gly). The glycine unit is the simplest possible amino acid. Triglycine is used as a model peptide for studies of the physicochemical parameters and molecular associations of small peptides, which can be used as a simple model of more complex molecules such as proteins. Triglycine provides two different functional groups, either or both of which could potentially be involved in bonding to mineral surfaces. In addition, triglycine molecule increases molecular complexity from amino acids to peptides studies, in order to study the role play by the peptide bond and to identify components on surface interaction, which has not been previously described. In this context, we studied the pyrite oxidation resulting from UV irradiation and adsorption of the tripeptide triglycine (Figure1) on pyrite by evaluating the interactions under different environmental conditions. It is crucial to compare experiments performed in the presence of water to others conducted Life 2018, 8, 50 3 of 12 under strictly ultra-high vacuum (UHV) conditions (simulated absence of oxygen and in-situ molecular depositionLife 2018, 8, x FOR by evaporation PEER REVIEW in UHV), allowing for the relevant impact of these different conditions3 of on12 the surface to be examined. Our surface science studies aim at a chemical characterization of the surface, investigatingconditions that the are strategic more favorable binding sites for increasing and the environmental the probability conditions of adsorption that are of moremolecular favorable species for increasingand their subsequent the probability concentration of adsorption on the of molecular surface. Th specieserefore, and we their report subsequent the results concentration of a spectroscopic on the surface.study of Therefore, X-ray photoemission we report the spec resultstroscopy of a spectroscopic (XPS) data, studyobtained of X-ray for pyrite photoemission under UV spectroscopy irradiation (XPS)treatment data, and obtained triglycine for pyrite adsorption under UVon irradiationa natural treatmentpyrite surface and triglycinebefore an adsorptiond after UV on treatment. a natural pyriteFurthermore, surface we before discuss and spectroscopic after UV treatment. evidence Furthermore, of different wemolecular discuss adsorption spectroscopic mechanisms evidence on of differentthe surface molecular of pyrite adsorption constraine mechanismsd by oxidization on the (UV surface and/or of pyrite water) constrained or under byultra-high oxidization vacuum (UV and/orconditions. water) or under ultra-high vacuum conditions.

Figure 1. Chemical structure of triglycine. 2. Materials and Methods 2. Materials and Methods Ultra-high vacuum conditions: The pyrite single crystal sample (provided by Surface PreparationUltra-high Laboratory) vacuum wasconditions: transferred The topyrite an ultra-high single crystal vacuum sample (UHV) (provided chamber withby Surface a base pressurePreparation of Laboratory)3 × 10−10 mbar was. Thetransferred pyrite sampleto an ultra-high was cleaned vacuum by (UHV) repeated chamber cycles with of Ar a+ baseion −10 + sputteringpressure of at3 × 80010 eVmbar. and The annealing pyrite sample at 595 was K. cleaned Surface by cleanliness repeated cycles was monitoredof Ar ion sputtering using XPS. at The800 eV pyrite and annealing sample wasat 595 never K. Surface overheated cleanliness beyond was monitored 600 K to using avoid XPS. thermal The pyrite decomposition. sample was never overheated beyond 600 K to avoid thermal decomposition. Triglycine (NH2-CH2-CO-NH-CH2- Triglycine (NH2-CH2-CO-NH-CH2-CO-NH-CH2-COOH, purity ≥ 98%) powder was purchased from Sigma-AldrichCO-NH-CH2-COOH, (Missouri, purity US) ≥ and98%) used powder without was furtherpurchased purification. from Sigma-Aldrich A home-built (Missouri, molecular US) doser and wasused employed without tofurther sublimate purification. the tripeptide A home-built molecule inmolecular UHV conditions. doser was The employed doser contained to sublimate a tantalum the envelopetripeptide holding molecule the chemicalin UHV andconditions. a thermocouple The dose facingr contained the sample a tantalum material. Theenvelope tantalum holding envelope the waschemical heated and by a directthermocouple current. Afacing K-type the thermocouple sample material. was attachedThe tantalum to the bagenvelope on the was outside, heated close byto a thedirect chemical, current. toA probeK-type its thermocouple temperature. was Before attached sublimation, to the bag the on triglycine the outside, was close outgassed to the chemical, and then heatedto probe to its 380 temperature. K and exposed Before to the sublimation, pyrite crystal; the in triglycine situ molecular was outgassed deposition and was then done heated by evaporation to 380 K underand exposed UHV conditionsto the pyrite (simulated crystal; in absence situ molecular of oxygen). deposition During was the done sublimation, by evaporation the main under chamber UHV pressureconditions typically (simulated rose toabsence 1 × 10 −of9 mbar.oxygen). During the sublimation, the main chamber pressure −9 typicallySolution rose experiments:to 1 × 10 mbar. A pyrite surface (from the Navajún mine in Spain) previously cleaned and driedSolution was immersed experiments: into 10 A mL pyrite of tri-Gly surface solution (from the (1 mM,Navajún pH ofmine 6.0) in for Spain) 30 min previously at 298 K with cleaned stirring. and Afterdried thewas immobilization immersed into step10 mL (surface of tri-Gly being solution immersed (1 mM, in pH the of molecular 6.0) for 30 solution), min at 298 the K pyrite with stirring. surface sampleAfter the (solid) immobilization was rinsed step with (surface MilliQ-water, being immersed dried by in blowing the molecular compressed solution), air, and the thenpyrite analysed surface undersample UHV (solid) conditions was rinsed using with an MilliQ-water, XPS technique. dried by blowing compressed air, and then analysed underUV UHV irradiation conditions at air us conditions:ing an XPS Pyritetechnique. samples were cleaned three times in different solutions of UV irradiation at air conditions: Pyrite samples were cleaned three times in different solutions 1 M of H2SO4, in water (Milli-Q grade), dried by blowing air and then the pyrite surface was exposed toof UV1 M radiation of H2SO (200–4004, in water nm) (Milli-Q for 5 and grade), 27 h. Adried 150 Wby water-cooled blowing air deuteriumand then the UV pyrite lamp (Hamamatsusurface was exposed to UV radiation (200–400 nm) for 5 and 27 h. A 150 W water-cooled deuterium UV lamp C3150), placed perpendicular to the pyrite sample, was used to irradiate the sample. The UV radiation (Hamamatsu C3150), placed perpendicular to the pyrite sample, was used to irradiate the sample. from the lamp entered the system through a quartz window. The UV light hit a beam splitter placed The UV radiation from the lamp entered the system through a quartz window. The UV light hit a very close to the lamp, which allowed 88% of the radiation to pass through. The other 12% of the beam splitter placed very close to the lamp, which allowed 88% of the radiation to pass through. The beam was reflected onto another quartz window, where a UV detector was placed that permitted other 12% of the beam was reflected onto another quartz window, where a UV detector was placed the continuous monitoring of the incoming UV flux via a spectroradiometer (Bentham DMc150FC). that permitted the continuous monitoring of the incoming UV flux via a spectroradiometer (Bentham After the beam splitter, we set a focusing lens to focus the beam on the surface. The irradiance spectrum DMc150FC). After the beam splitter, we set a focusing lens to focus the beam on the surface. The of the deuterium lamp was a continuum that decreased for increasing photon wavelength; the UV irradiance spectrum of the deuterium lamp was a continuum that decreased for increasing photon flux measured at the sample position, obtained by integration of the irradiance over the 200–400 nm wavelength; the UV flux measured at the sample position, obtained by integration of the irradiance over the 200–400 nm wavelength range, was 2.3 × 1014 photons/cm2 in the current system. XPS spectra of the samples were recorded after UV exposure in a different dedicated XPS chamber; XPS of the pristine clean pyrite surface was also recorded to get information about the surface before UV irradiation.

Life 2018, 8, 50 4 of 12 wavelength range, was 2.3 × 1014 photons/cm2 in the current system. XPS spectra of the samples were recorded after UV exposure in a different dedicated XPS chamber; XPS of the pristine clean pyrite surface was also recorded to get information about the surface before UV irradiation. Life 2018, 8, x FOR PEER REVIEW 4 of 12 X-ray photoelectron spectroscopy analysis of the samples was carried out in an ultrahigh-vacuum chamberX-ray equipped photoelectron with a hemisphericalspectroscopy analysis electron of analyser the samples and was an Al carried Kα X-ray out in source an ultrahigh- (1486.6 eV) −10 withvacuum an aperture chamber of 7equipped mm × 20 with mm. a hemispherical The base pressure electron in analyser the chamber and an wasAl K 3α ×X-ray10 sourcembar, (1486.6 and the experimentseV) with an were aperture performed of 7 mm at × room 20 mm. temperature. The base pressure The peak in the decomposition chamber was 3 in × different10−10 mbar, components and the wasexperiments shaped, after were background performed subtraction,at room temperature. as a convolution The peak decomposition of the Lorenztian in different and Gaussian components curves. Bindingwas shaped, energies after were background calibrated subtraction, against the bindingas a convolution energy ofof the Lorenztian C 1s peak atand 285.0 Gaussian eV for curves the pyrite. solutionBinding samples energies and were against calibrated the S against 2p peak the at binding 162.8 eV energy for the of the pyrite C 1s (FeSpeak2 at) under 285.0 eV the for UHV the pyrite samples. We hadsolution not observedsamples and any against beam the radiation S 2p peak damage at 162.8 of eV the for triglycine the pyrite layer (FeS2 during) under the UHV data acquisition.samples. We had not observed any beam radiation damage of the triglycine layer during the data acquisition. 3. Results and Discussion 3. Results and Discussion 3.1. Effect of Ultraviolet (UV) Radiation on the Pyrite Surface 3.1. Effect of Ultraviolet (UV) Radiation on the Pyrite Surface Regarding the pyrite clean surface (see Figure2), the sulfur peak showed three components: The Regarding the pyrite clean surface (see Figure 2),2− the sulfur peak showed three components: The main one at 162.8 eV, which corresponded to the S2 , clean pyrite surface (FeS2, 77%), in agreement main one at 162.8 eV, which corresponded to the S22−, clean pyrite surface (FeS2, 77%), in agreement with the literature [31–33]; a second component at 164.7 eV assigned to a polysulfide species (S-S bonds, with the literature [31–33]; a second component at 164.7 eV assigned to a polysulfide species 2(S-S− 12%)bonds, present 12%) in present natural in pyrite natural [33 pyrite–35]; [33–35]; and a third and a component third component at 161.8 at 161.8 eV assigned eV assigned to the to the S S2-(FeS, 2+ 11%).(FeS, The 11%). iron spectrumThe iron spectrum showed ashowed maincomponent a main component at 707.4 at eV 707.4 assigned eV assigned to Fe to(clean Fe2+ (clean iron sulphide, iron 2+ 69%),sulphide, a second 69%), component a second at compon 708.9 eVent assignedat 708.9 eV to Feassigned(FeS to + FeO,Fe2+ (FeS 24%) + andFeO, a 24%) third and component a third at 3+ 711.1component eV assigned at 711.1 to Fe eV assigned(Fe2O3, 7%)to Fe (see3+ (Fe Table2O3, 7%)1). (see Table 1). OnceOnce the the surface surface had had been been exposed exposed to to UVUV irradiationirradiation for for 5 5 and and 27 27 h,h, the the XPS XPS spectra spectra shows shows that that all theall peaksthe peaks seen seen and and identified identified in thein the non-irradiated non-irradiated pyrite pyrite surface, surface, are are also also presentpresent inin thethe pyritepyrite UV irradiatedUV irradiated for 5 and for 275 and h (see 27 h Table (see 1Table). In 1). addition In addition to these to these peaks, peaks, new new peaks peaks resulting resulting from from the the UV UV irradiation were observed at 168.5 eV and at 712.9 eV, assigned to sulfate (SO4−24−) species and to 3+ irradiation were observed at 168.5 eV and at 712.9 eV, assigned to sulfate (SO2 ) species and to Fe Fe3+ (Fe2SO4), respectively. It is noticeable that the proportions between these peaks changed (Fe2SO4), respectively. It is noticeable that the proportions between these peaks changed significantly significantly after 5 and 27 h of UV irradiation from 4–6% to 12–22% respectively (see Table 1). after 5 and 27 h of UV irradiation from 4–6% to 12–22% respectively (see Table1). UV irradiation has an effect on the pyrite surface even after a very short time, such as 5 h of UV irradiation has an effect on the pyrite surface even after a very short time, such as 5 h of exposure, confirmed by the appearance of the sulfate species and a remarkable increase in the exposure, confirmed by the appearance of the sulfate species and a remarkable increase in the oxidized oxidized species; furthermore, a higher increase in the oxides and sulfate species is shown at 27 h of species;exposure. furthermore, Consequently, a higher the increase pyrite surface in the is oxides highly and sensitive sulfate to species chemical is changes shown atinduced 27 h of by exposure. UV Consequently,irradiation, themeaning pyrite that surface pyrite is highlysurface sensitive chemistry to could chemical be changeseasily affected induced by byenvironmental UV irradiation, meaningconditions that pyriteand is surfacehighly reactive, chemistry which could would be easilybe a necessary affected condition by environmental for a potentially conditions effective and is highlycatalyst. reactive, which would be a necessary condition for a potentially effective catalyst.

FigureFigure 2. XPS 2. XPS photoemission photoemission spectra spectra of of FeFe 2p,2p, andand S 2p core core level level peaks peaks of ofthe the clean clean pyrite pyrite surface surface beforebefore and and after after 5 and 5 and 27 27 h ofh of UV UV irradiation irradiationtreatment. treatment.

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Life 2018, 8, x FOR PEER REVIEW 5 of 12 Table 1. A Comparison study of Fe 2p and S 2p core-level peaks, deconvolution and ratios of their components peaks of the clean pyrite surface before and after 5 and 27 h of UV irradiation treatment. Table 1. A Comparison study of Fe 2p and S 2p core-level peaks, deconvolution and ratios of their componentsClean peaks Pyrite of the clean Clean pyrite Pyrite surface + 5 before h UV and Clean after Pyrite5 and 27 + 27h of h UV irradiation treatment. Assignment BE (eV)Clean Pyrite % Clean BE (eV) Pyrite + 5 h % UV Clean BE (eV)Pyrite + 27 h %UV Assignment BE (eV) % BE (eV) % BE (eV) % 2+ 707.3 69 707.3 63 707.3 54 Fe (FeS2) 707.3 69 707.3 63 707.3 54 Fe2+2+ (FeS2) Fe 2p 708.9 24 709.1 23 708.9 10 Fe (FeS + FeO) 2+ 3+ 711.1708.9 724 711.1 709.1 10 23 711.1 708.9 23 10 Fe (FeSFe + (FeFeO)2O 3) Fe 2p 3+ 3+ 711.1 7 712.9 711.1 4 10 712.9 711.1 12 23 FeFe (Fe2(FeO3)2 SO4) 3+ 161.8 11 161.9 712.9 104 161.9 712.9 12 6 Fe (FeS22−SO(FeS)4) 162.8161.8 7711 162.8 161.9 71 10 162.8 161.9 60 6 S2- (FeS)2− S 2p S2 (FeS2) 162.8 77 162.8 71 162.8 60 S22-2 −(FeS2≤) ≤ S 2p 164.7 12 164.6 13 164.6 12 Sn (2 n 8) 2- 4− 164.7 12 168.5 164.6 6 13 168.5 164.6 22 12 Sn SO (2 2≤ n ≤(sulfate) 8) 168.5 6 168.5 22 SO24- (sulfate)

TheThe UVUV irradiationirradiation processprocess ofof thethe surfacesurface overover severalseveral hourshours (5(5 andand 2727 h)h) resultsresults inin remarkableremarkable changeschanges inin the the shape shape of of the the S 2p S and2p and Fe 2p Fe spectrum 2p spectrum (Figure (Figure2). To clarify2). To theclarify chemical the chemical changes inducedchanges oninduced the pyrite on the surface, pyrite the surface, distributions the distributions of the S and of Fe the species S and during Fe species the UV during irradiation the UV process irradiation have beenprocess represented have been (see represented Figure3). (see Figure 3).

FigureFigure 3.3. FeFe andandS Ssurface surface species species distribution distribution along along the th UVe UV irradiation irradiation process process duration duration at 0,at 50, and 5 and 27 h27 of h UVof UV irradiation irradiation of theof the surface. surface.

The XPS data for the Fe species showed a decrease of the 707.3 eV signal (FeS2, black line) and The XPS data for the Fe species showed a decrease of the 707.3 eV signal (FeS2, black line) and the 709.1 eV signal (FeS + FeO, red line) after increasing the UV irradiation time. Finally, the Fe2O3 the 709.1 eV signal (FeS + FeO, red line) after increasing the UV irradiation time. Finally, the Fe2O3 contribution at the 711.1 eV signal (blue line) increased, and a significant appearance of the signal contribution at the 711.1 eV signal (blue line) increased, and a significant appearance of the signal from Fe2SO4 (pink line) at 712.9 eV, along the UV irradiation process, developed. This is in agreement from Fe2SO4 (pink line) at 712.9 eV, along the UV irradiation process, developed. This is in agreement withwith thethe sulfursulfur XPSXPS results.results. ForFor thethe sulfursulfur species,species, thethe 161.9161.9 eVeV componentcomponent assignedassigned toto thethe FeSFeS ++ FeOFeO species (red line) decreased, and the main component at 162.8 eV assigned to the FeS2 species (black species (red line) decreased, and the main component at 162.8 eV assigned to the FeS2 species (black line)line) decreaseddecreased asas well;well; therethere waswas thethe remarkableremarkable appearanceappearance ofof aa newnew componentcomponent assignedassigned toto thethe Fe2SO4 at 168.5 eV (pink line), which appeared due to the UV irradiation process, and the component Fe2SO4 at 168.5 eV (pink line), which appeared due to the UV irradiation process, and the component 2− at 164.6 eV assigned to polysulfides (Sn ) remained constant as expected. at 164.6 eV assigned to polysulfides (Sn2−) remained constant as expected. InIn summary,summary, thethe exposureexposure ofof pyritepyrite toto longerlonger UVUV irradiationirradiation processesprocesses (5(5 andand 2727 h)h) inducedinduced aa decrease in the originally observed chemical species, assigned to phases disulfide (FeS2), monosulfide decrease in the originally observed chemical species, assigned to phases disulfide (FeS2), monosulfide (FeS) and FeO (see Figure3). The increased amount of Fe 2O3 species was obtained because of the (FeS) and FeO (see Figure 3). The increased amount of Fe2O3 species was obtained because of the UV UVirradiation irradiation process process during during 5 h 5 and h and 2727 h, h,which which also also induced induced the the appearance appearance of of the iron sulfatessulfates species. The pyrite UV irradiation process carried out the oxidation of Fe2+ into Fe3+, and the presence species. The pyrite UV irradiation process carried out the oxidation of Fe2+ into Fe3+, and the presence of Fe3+ favoured the oxidising process of Fe2+. Therefore, Fe3+ is a reaction product in the presence of oxygen (Fe2+ → Fe3+) as well as an oxidant reactive for pyrite (the presence of Fe3+ favour the oxidising process of Fe2+); in this sense, the oxidation of pyrite due to the UV irradiation treatment

Life 2018, 8, 50 6 of 12 of Fe3+ favoured the oxidising process of Fe2+. Therefore, Fe3+ is a reaction product in the presence Lifeof oxygen2018, 8, x FOR (Fe2+ PEER→ FeREVIEW3+) as well as an oxidant reactive for pyrite (the presence of Fe3+ favour6 of the 12 oxidising process of Fe2+); in this sense, the oxidation of pyrite due to the UV irradiation treatment can be considered an autocatalytic process [[27].27]. Pyrite is a good catalyst candidate since its surface is very reactive, even after a short time of <5 h of UV exposure. Furthermore, we are interested in the molecular interaction of short peptides from inert conditions under UHV conditions to more reactive conditions and molecular adsorption from solutionssolutions beforebefore andand afterafter UVUV pyritepyrite surfacesurface treatment.treatment.

3.2. Interaction of Triglycine with Pyrite SurfacesSurfaces underunder SeveralSeveral ConditionsConditions

3.2.1. Interaction of Triglycine with Pyrite Surfaces byby MolecularMolecular EvaporationEvaporation DepositionDeposition underunder Ultra-High Vacuum ConditionsConditions Triglycine adsorption on the pyrite surface under ultra-high vacuum conditions (absence of oxygen and and in-situ in-situ molecular molecular deposition deposition by by evaporation evaporation in UHV) in UHV) was was analysed analysed by XPS, by XPS, which which is well is wellsuited suited to characterize to characterize the possible the possible chemical chemical changes changes in molecular in molecular interactions interactions on surfaces on surfaces due to due its highto its sensitivity high sensitivity and non-destructive and non-destructive nature. nature. The in Thesitu inXPS situ analysis XPS analysis of triglycine of triglycine adsorption adsorption on the pyriteon the surface pyrite revealed surface revealed the presence the presenceof carbon, of ox carbon,ygen and oxygen nitrogen and on nitrogen the pyrite on surface the pyrite under surface UHV conditionsunder UHV (see conditions Figure 4). (see The Figure best-fit4). curve The best-fit for the curve C 1s peak for the was C 1sobtained peak was using obtained three components using three forcomponents the small forpeptide, the small triglycine, peptide, and triglycine, the first carbon and the component first carbon had component a binding hadenergy a binding (B.E.) of energy 285.8 (B.E.)eV and of was 285.8 attributed eV and wasto the attributed C-N group to the[36,37]; C-N th groupe second [36, 37component]; the second was component observed at was 287.7 observed eV due toat 287.7the amide eV due group to the (-NH-CO-), amide group and (-NH-CO-), the presence and of thea third presence carbon of acomponent third carbon at component289.2 eV was at − assigned289.2 eV wasto the assigned COOH to or the COO COOH- groups or COO [38]. groupsThe intensity [38]. The ratio intensity of the ratiothree of components the three components was 3:2:1 − was(CN: 3:2:1 -NH-CO-:COO (CN: -NH-CO-:COO− or COOH),or which COOH), is whichin close is agreement in close agreement with the with chemical the chemical formula formula of the molecule.of the molecule. The O 1s The peak O was 1s peak observed was observedat 531.8 eV at and 531.8 was eV attributed and was to attributed one component, to one component,the oxygen − inthe the oxygen COO in- groups the COO [31–34,39]groups and [31– the34,39 C=O] and of the the C=O amide of thegroup. amide The group. best-fit The curve best-fit of the curve N of1s thepeak N 1sconsists peak consistsof two ofcomponents two components centred centred at the at bind the bindinging energies energies of 400.0 of 400.0 and and 402.0 402.0 eV, eV, which which were + assigned to the the NH NH22 ++ -NH-CO- -NH-CO- and and NH NH3+ 3functionalfunctional groups, groups, respectively respectively [27,34,35] [27,34, 35(see] (see Figure Figure 1 for1 thefor thetriglycine triglycine molecule). molecule). XPS XPSdemonstrates demonstrates successful successful adsorption adsorption of the ofintact the intactmolecule molecule on the onpyrite the pyritesurface. surface.

Figure 4. XPS spectra for triglycine adsorption on th thee pyrite surface from the gas phase under UHV conditions. These XPS spectra were obtained immediat immediatelyely after the triglycine adsorbed on the surface.

+ The presence of the NH3 functional group was only observed when the molecular adsorption 3+ The presence of the NH functional group was only observed when the molecular+ adsorption occurred under UHV conditions, which favours the presence of the NH2 and NH3 functional groups, occurred under UHV conditions, which favours the presence of the NH2 and NH3+ functional groups, for cystine molecules, as previously reported by our group [30]. UHV conditions facilitate the formation for cystine molecules, as previously reported by our group [30]. UHV conditions facilitate the of a diversity of chemical species. Because the anionic form of amino acids is the predominant form formation of a diversity of chemical species. Because the anionic form of amino+ acids is the observed when these compounds adsorb onto surfaces, it is remarkable that NH3 was observed on predominant form observed when these compounds adsorb onto surfaces, it is remarkable that NH3+ the surface of pyrite only under UHV conditions. The presence of sulfur vacancies on the surface may was observed on the surface of pyrite only under UHV conditions. The presence of sulfur vacancies on the surface may rationalize the adsorption of cations under UHV conditions because they are compensated for [40,41], whereas under solution conditions, sulfur vacancies are readily passivated by water molecules, and the presence of iron oxides makes it more likely that only the anionic form of the molecule will be present. Surface vacancies on pyrite could affect the chemical form in which

Life 2018, 8, 50 7 of 12 rationalize the adsorption of cations under UHV conditions because they are compensated for [40,41], whereas under solution conditions, sulfur vacancies are readily passivated by water molecules, and the presenceLife 2018, 8, ofx FOR iron PEER oxides REVIEW makes it more likely that only the anionic form of the molecule will7 of be 12 present. Surface vacancies on pyrite could affect the chemical form in which the molecule is adsorbed, determiningthe molecule the is molecularadsorbed, chemistrydetermining on thethe surface.molecular We chemistry focused our on studies the surface. to confirm We focused this fact our for morestudies complex to confirm molecules this fact than for aminomore complex acids, such molecules as the small than peptide,amino acids, triglycine. such as the small peptide, triglycine. 3.2.2. Interaction of Triglycine Solution Adsorption on the Pyrite Surface 3.2.2. Interaction of Triglycine Solution Adsorption on the Pyrite Surface Figure5 shows the XPS spectra for the triglycine adsorption on a pyrite surface from a solution. The CFigure 1s peak 5 shows shows the three XPS contributions spectra for the at triglycine 284.9 eV, adsorption 286.6 eV and on a 288.7 pyrite eV, surface which from were a assignedsolution. toThe C-H C 1s groups peak shows with a three contribution contributions from at contamination 284.9 eV, 286.6 during eV and sample 288.7 eV, preparation which were in airassigned instead to ofC-H under groups UHV with conditions a contribution and CN from groups, contamination to the amide during group sample (-NH-CO-) preparation and to in the air carboxylicinstead of groupsunder UHV or carboxylate conditions groupsand CN (COO groups,−), to respectively the amide group [30]. Regarding(-NH-CO-) the and O to 1s the peak, carboxylic we fitted groups the experimentalor carboxylate data groups points (COO using-), respectively two components. [30]. Regarding The first componentthe O 1s peak, occurred we fitted at athe binding experimental energy ofdata 531.2 points eV, using which two was components. assigned to The the twofirst equivalentcomponent oxygenoccurred atoms at a binding belonging energy to the of so-called531.2 eV, resonantwhich was state assigned of the to deprotonated the two equivalent carboxylic oxygen group atoms (carboxylate belonging group)to the so-called and to the resonant amide state group of (-NH-CO-)the deprotonated [31–34, 39carboxylic], and the group second (carboxylate component group) appears and at to 532.2 the amide eV, but group this component(-NH-CO-) is[31– a contribution34,39], and the from second contamination component during appears sample at 532.2 preparation eV, but inthis air component instead of under is a contribution UHV conditions. from Thecontamination N 1s core level during peak sample presented preparation a single in componentair instead of centred under UHV at 400.2 conditions. eV, which The was N assigned1s core level to thepeak NH presented2 species a and single to the component amide group centred (-NH-CO-), at 400.2 eV, indicating which was that assigned anions in to the the solution NH2 species were and the onlyto the adsorption amide group species (-NH-CO-), present indicating on the pyrite that anions surface. in Thethe solution molecule were successfully the only adsorption adsorbed species on the pyritepresent surface. on the pyrite surface. The molecule successfully adsorbed on the pyrite surface.

Figure 5. XPS photoemission spectra of the C 1s, O 1s and N 1s core-level peaks of triglycine adsorbed Figure 5. XPS photoemission spectra of the C 1s, O 1s and N 1s core-level peaks of triglycine adsorbed on the pyrite surface from solution 1 mM. Experimental core-level spectra (red) and the fitting results on the pyrite surface from solution 1 mM. Experimental core-level spectra (red) and the fitting results for all the components (black) and individual components (dotted lines). for all the components (black) and individual components (dotted lines). 3.2.3. Interaction of Triglycine Solution Adsorption on the UV Oxidized Pyrite Surface 3.2.3. Interaction of Triglycine Solution Adsorption on the UV Oxidized Pyrite Surface Once we had studied and characterized pyrite surface oxidation under UV exposure conditions, we turnedOnce we to studyhad studied triglycine and peptidecharacterized affinity pyrite adsorbed surface on oxidation the pyrite under oxidized UV exposure surface. conditions, Therefore, triglycinewe turned adsorption to study triglycine on the pyrite peptide surface affinity was analysedadsorbed by on XPS, the whichpyrite isoxidized well suited surface. to characterize Therefore, thetriglycine possible adsorption chemical on changes the pyrite in molecular surface was interactions analysed by on XPS, surfaces which due is towell its suited high sensitivity to characterize and non-destructivethe possible chemical nature. changes in molecular interactions on surfaces due to its high sensitivity and non-destructiveXPS analysis nature. of triglycine adsorption on the UV oxidized pyrite surface revealed the presence of carbon,XPS oxygen analysis and of nitrogentriglycine on adsorption the pyrite on surface. the UV The oxidized best-fit pyrite curve surface for the Crevealed 1s peak the was presence obtained of usingcarbon, three oxygen components and nitrogen for the on small the pyrite peptide. surface. The first The carbon best-fit component curve for the had C a 1s binding peak was energy obtained (B.E.) ofusing 284.9 three eV assigned components to the for air the contribution small peptide. and The CH, fi arst second carbon component component at had 286.5 a binding eV was attributedenergy (B.E.) to theof 284.9 C-N groupeV assigned [31,32] to and the the air amide contribution group (-NH-CO-), and CH, a whereassecond component the third component at 286.5 eV was was observed attributed at to the C-N group [31,32] and the amide group (-NH-CO-), whereas the third component was observed at 288.5 eV and was assigned to the COOH or COO− groups [33]. For the O 1s, a peak was observed at 531.4 eV and was attributed to one component; the oxygen in the COO- groups [31–34,39], and amide group, and the second component at 532.5 eV was assigned to the air contribution. The best-fit curve of the N 1s peak consisted of only one component centred at the binding energy of 399.8 eV, which was assigned to the NH2 and the amide group (-NH-CO-) [33–35].

Life 2018, 8, 50 8 of 12

288.5 eV and was assigned to the COOH or COO− groups [33]. For the O 1s, a peak was observed at 531.4 eV and was attributed to one component; the oxygen in the COO− groups [31–34,39], and amide group, and the second component at 532.5 eV was assigned to the air contribution. The best-ﬁt curve ofLife the 2018 N, 8 1s, x peakFOR PEER consisted REVIEW of only one component centred at the binding energy of 399.8 eV, which8 wasof 12 assigned to the NH2 and the amide group (-NH-CO-) [33–35]. Therefore,Therefore, thethe triglycinetriglycine peptidepeptide waswas successfullysuccessfully adsorbedadsorbed inin threethree cases:cases: UHVUHV conditionsconditions andand fromfrom aa solutionsolution beforebefore andand afterafter UVUV pyritepyrite surfacesurface treatment.treatment. RemarkableRemarkable differencesdifferences werewere shownshown basedbased onon thethe nitrogen nitrogen signal: signal: two two chemical chemical forms form weres were observed observed under under UHV UHV conditions, conditions, i.e., NHi.e.,2 NHand2 + + NHand3 NH, whereas3 , whereas only only the the NH NH2 was2 was detected detected when when adsorbing adsorbing the the molecule molecule from from solution. solution. FigureFigure6 6 showsshows nitrogennitrogen differences differences from from the threethe three different different molecular molecular adsorption adsorption conditions. conditions. The XPS The nitrogen XPS signalnitrogen is asignal molecular is a molecular ﬁngerprint fingerprint on its surface, on its andsurface, a higher and a intensity higher intensity of the signal of the means signal ameans higher a concentrationhigher concentration of molecules of molecules on the surface; on the therefore,surface; therefore, as has been as previously has been previously explained, UVexplained, irradiation UV favoursirradiation molecular favours adsorption molecular ofadsorption triglycine of on triglycine the pyrite on surface the pyrite (see surface Figure6 (see). Figure 6).

FigureFigure 6.6. XPS photoemission spectraspectra ofof NN 1s core level peakpeak of triglycine adsorbed fromfrom thethe gasgas phasephase underunder anoxicanoxic conditionsconditions andand fromfrom solutionsolution beforebefore andand afterafter pyritepyrite surfacesurface UVUV irradiationirradiation exposure.exposure.

AA summarysummary ofof thethe XPSXPS results,results, C1C1 s,s, N1N1 ss andand O1O1 ss core-levelcore-level peakspeaks andand assignmentsassignments inin theirtheir componentscomponents forfor triglycine/pyrite triglycine/pyrite under under UHV UHV conditions, conditions, molecular molecular immobilization immobilization from from solution solution and afterand after UV surface UV surface irradiation irradiation treatment, treatment, are shown are shown in Table in Table2. 2.

TableTable 2.2. AA ComparisonComparison studystudy ofof CC 1s,1s, NN 1s1s andand OO 1s1s core-levelcore-level peakspeaks andand deconvolutiondeconvolution ofof theirtheir componentscomponents forfor thethe triglycine/pyritetriglycine/pyrite system system under under different different environmental conditions (UHV, solutionsolution andand solutionsolution afterafter UV).UV).

UHVUHV Conditionsconditions Solution Solution Solution Solution after after UV UV

BEBE (eV) (eV) Assignment Assignment BE (eV) Assignment Assignment BE BE (eV) (eV) Assignment Assignment 285.8285.8 C-N C-N 284.9 C-H C-H + + air air 284.9 284.9 C-H C-H + +air air 287.7 -NH-CO- 286.6 C-N + -NH-CO- 286.5 C-N + -NH-CO- C 1sC 1s 287.7 -NH-CO- 286.6 C-N + -NH-CO- 286.5 C-N + -NH-CO- COOH or − − − 289.2289.2 COOH or COO 288.7 COOH or COO- 288.5288.5 COOH COOH or or COO COO- COO- 531.8 COO− + -NH-CO- 531.2 COO− + -NH-CO- 531.4 COO− + -NH-CO- O 1s COO- + -NH- COO- + -NH- COO- + -NH- 531.8 531.2532.2 air531.4 532.5 air O 1s CO- CO- CO- 400.0 NH2 + -NH-CO- 400.2 NH2 + -NH-CO- 399.8 NH2 + -NH-CO- N 1s + 402.0 NH3 532.2 air 532.5 air NH2 + -NH- 400.0 400.2 NH2 + -NH-CO- 399.8 NH2 + -NH-CO- N 1s CO- 402.0 NH3+

A comparison study of triglycine adsorption on the pyrite surface shows the presence of the NH2 and NH3+ functional groups, under UHV conditions, but nevertheless, more molecules accumulated on the surface when molecular adsorption was conducted from a solution and was even higher if the pyrite surface had been previously exposed to UV irradiation (see the nitrogen signal from Figure 6). The fact that the surface had been oxidized, inferred different properties. UV irradiation makes the pyrite surface more reactive and enables it to accumulate more molecules; this fact would be a helpful

Life 2018, 8, 50 9 of 12

A comparison study of triglycine adsorption on the pyrite surface shows the presence of the NH2 + and NH3 functional groups, under UHV conditions, but nevertheless, more molecules accumulated on the surface when molecular adsorption was conducted from a solution and was even higher if the pyrite surface had been previously exposed to UV irradiation (see the nitrogen signal from Figure6). The fact that the surface had been oxidized, inferred different properties. UV irradiation makes the pyrite surface more reactive and enables it to accumulate more molecules; this fact would be a helpful condition to allow for reactions between molecules. Therefore, these results are in agreement with the Bernal theory that mineral surface adsorption could help to overcome the problem of an extremely dilute concentration of amino acids in prebiotic oceans. Minerals can be potential surfaces to adsorb molecules, and furthermore, environmental conditions could be the determining factor to increase the probability of molecular reactions. From these experiments, we have calculated triglycine molecules adsorbed on the surface of the pyrite during different experimental conditions. Calculations of the nitrogen/sulfur ratio for each experimental case, taking in account the experimental area (I) and the atomic sensitivity factor (S) for X-ray source for each element has been done. The equation applied is the following:

n1/n2 = (I1/S1)/(I2/S2) (1)

N/N = (INitrogen/SNitrogen)/(ISulfur/SSulfur) (2) Then, the ratio N/S for UHV conditions is the lowest with a value of 0.06, for solution conditions is 0.12 and for solution after UV conditions is the highest ratio with a value 0.18, meaning that immobilization of the triglycine molecules from solution after UV conditions helps to concentrate molecules on the surface. The pyrite surface is reactive to environmental conditions, such as UHV conditions, water solutions, UV irradiation and chemical changes induced on the surface, which modify the molecular interactions; furthermore, pyrite surfaces show an affinity for adsorption of molecules, including small peptides. The pyrite surface can be proposed as a good reservoir to concentrate molecules and to have the potential to react when the environmental conditions are optimal. The ability to respond to environmental conditions and its molecular affinity have positioned pyrite as a good candidate for being a surface promotor of catalytic reactions in the prebiotic chemistry context. Chemically, the fact that iron sulfide surfaces contain at least two types of surface functional groups has some interesting implications, such as the possibility of binding species that are chemically different and the subsequent interactions, including electron transfer, between the co-adsorbates that may produce products that would be difficult to form on a surface with a single surface site. Molecular adsorption from solution conditions was slightly more favorable, concentrating a larger number of molecules on the surface compared to under UHV conditions (see the nitrogen comparison study, Figure6), even though only anionic chemical species were present on the surface. In solution, the carbon and oxygen peaks showed atmospheric and water contributions on the surface of pyrite, producing a stronger overall spectral signal than that observed under UHV conditions. Hence, the triglycine molecules are adsorbed only in their more favorable anionic form. On the other hand, under UHV conditions, in which sulfur anion vacancies are not compensated for, the zwitterionic and anionic chemical species coexist on the pyrite surface. UV exposure rapidly changes pyrite surface species, and furthermore, UV exposure has critical implications for the adsorption of triglycine molecules onto the pyrite surface and changing molecular chemical functionalities is expected to affect its molecular reactivity between different chemical species; therefore, it is relevant to study conditions which may be encountered in various natural environments. In summary, this spectroscopic analysis demonstrates the presence of oxide compounds as well as new sulfur species on the surface of pyrite due to the UV irradiation and indicates that triglycine adsorbs on the pyrite surface in its anionic form when adsorbed from solution. Furthermore, UV is a relevant parameter to increase molecular concentration on pyrite surfaces. The findings and Life 2018, 8, 50 10 of 12 their implications are relevant in the prebiotic chemistry research field, showing that environmental conditions drive the appearance of new species on surfaces, which modify the molecular interactions. Furthermore, a UV irradiation of mineral surfaces may help to concentrate such compounds for potential catalytic reactions on surfaces to occur.

4. Conclusions We have performed the first spectroscopic characterization of triglycine adsorption on a UV irradiated pyrite surface. XPS analysis was employed to efficiently explore the molecular adsorption, to understand surface chemistry, and finally, to describe the critical influence of the different environmental conditions in the small peptides-pyrite system. We demonstrated how pyrite minerals can concentrate and act as adsorption substrates for small peptides during wetting conditions and even under inert UHV conditions. The successful adsorption of several molecules from amino acids to small peptides under a wide range of experimental conditions indicates the potential of pyrite as a catalyst under different environmental conditions. The pyrite surface offers the possibility of binding species that are chemically different as a multiple-site surface, and therefore, the co-adsorbates may produce products that would be difficult to form on a surface with a single surface site. These studies could therefore shed light onto prebiotic chemistry reactions. Mineral surfaces may play a relevant role to concentrate molecules, even under extremely diverse environments (UHV, solution, UV), which does not inhibit molecule/mineral surface interaction. Therefore, minerals could act as a molecular surface concentrator to overcome the controversy matter from “dilute prebiotic soup”. Mimicking the complex prebiotic geochemical environment is still an enormous challenge; nevertheless, different environmental conditions could help to discriminate under which conditions molecule/mineral interactions would or would not be negligible.

Author Contributions: Formal analysis, S.G.-M. and E.M.-M.; Investigation, S.G.-M. and E.M.-M.; Methodology, S.G.-M. and E.M.-M.; Supervision, E.M.-M.; Writing—original draft, E.M.-M.; Writing—review & editing, E.M.-M. Funding: This research was funded by MINECO grant number [ESP2014-55811 and ESP2017-89053]. Acknowledgments: This work has been supported by the MINECO project ESP2014-55811 and ESP2017-89053. The Instituto Nacional de Tecnica Aeroespacial supported the work performed at CAB. We are grateful to D. Hochberg for English improvement. Conﬂicts of Interest: The authors declare no conﬂict of interest.

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