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Effect of thenardite on the direct detection of aromatic amino acids: implications for the search for life in the solar system

Published online by Cambridge University Press:  28 August 2009

C. Doc Richardson ,
Nancy W. Hinman  and
Jill R. Scott
C. Doc Richardson
Affiliation:
Geosciences Department, University of Montana, Missoula, 32 Campus Drive #1296, Missoula, MT 59812, USA
Nancy W. Hinman
Affiliation:
Geosciences Department, University of Montana, Missoula, 32 Campus Drive #1296, Missoula, MT 59812, USA
Jill R. Scott*
Affiliation:
Chemical Sciences, Idaho National Laboratory, 1765 North Yellowstone Hwy, Idaho Falls, ID 83415, USA
*
e-mail: Jill.Scott@inl.gov
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Abstract

With the discovery of Na-sulphate minerals on Mars and Europa, recent studies using these minerals have focused on their ability to assist in the detection of bio/organic signatures. This study further investigates the ability of thenardite (Na2SO4) to effectively facilitate the ionization and identification of aromatic amino acids (phenylalanine, tyrosine and tryptophan) using a technique called geomatrix-assisted laser desorption/ionization in conjunction with a Fourier transform ion cyclotron resonance mass spectrometry. This technique is based on the ability of a mineral host to facilitate desorption and ionization of bio/organic molecules for detection. Spectra obtained from each aromatic amino acid alone and in combination with thenardite show differences in ionization mechanism and fragmentation patterns. These differences are due to chemical and structural differences between the aromatic side chains of their respective amino acid. Tyrosine and tryptophan when combined with thenardite were observed to undergo cation-attachment ([M+Na]+), due to the high alkali ion affinity of their aromatic side chains. In addition, substitution of the carboxyl group hydrogen by sodium led to formation of [M-H+Na]Na+ peaks. In contrast, phenylalanine mixed with thenardite showed no evidence of Na+ attachment. Understanding how co-deposition of amino acids with thenardite can affect the observed mass spectra is important for future exploration missions that are likely to use laser desorption mass spectrometry to search for bio/organic compounds in extraterrestrial environments.

Keywords

aromatic amino acidsbiosignatureEuropaFTICR-MSGALDIgeomatrixMarsthenardite

Information

Type
Research Article
Information
International Journal of Astrobiology , Volume 8 , Issue 4 , October 2009 , pp. 291 - 300
Copyright
Copyright © Cambridge University Press 2009

Introduction

Both hydrated and unhydrated Na-sulphate minerals exist in numerous bodies throughout the solar system. On Earth, Na-sulphates form in non-marine environments (playas, sabkhas), in basaltic weathering (Karlo et al. Reference Karlo, Jorgenson and Shineldecker1980; Hill & Forti Reference Hill and Forti1997), as fumarolic exhalations (Hill & Forti, Reference Hill and Forti1997), in atmospheric aerosols (Rankin et al. Reference Rankin, Wolff and Martin2002), and in subsurface Antarctic ice (Ohno et al. Reference Ohno, Igarashi and Hondoh2006). Beyond Earth, Na-sulphates are found on Mars as weathering products in evaporitic environments (Zhu et al. Reference Zhu, Xie, Guan and Smith2006; Mangold et al. Reference Mangold, Gendrin, Gondet, LeMouelic, Quantin, Ansan, Bibring, Langevin, Masson and Neukum2008), and as surface components of the Jupiter moons Ganymede (McCord et al. Reference McCord, Hansen and Hibbitts2001), Io (Wiens et al. Reference Wiens, Burnett, Calaway, Hansen, Lykke and Pellin1997), and Europa (McCord et al. Reference McCord1998; McCord et al. Reference McCord1999; Johnson Reference Johnson2000). Additionally, numerous prebiotic organic compounds have been detected on these Solar bodies, making them high priority candidates for biological activity (Kotler et al. Reference Kotler, Richardson, Hinman, Scott and Basiuk2009). Thus, with the ubiquity of Na-sulphates in the Solar System, understanding their ability to preserve and relinquish bio/organic signatures, which are signatures that are organic and potentially biological in origin, is crucial in the search for extraterrestrial life.

Since the Viking missions (Klein Reference Klein1979; Oro Reference Oro1979), the search for life in the Solar System has predominantly focused on the planet Mars (Chyba & McDonald Reference Chyba and McDonald1995). Unfortunately, due to the oxidizing Martian atmosphere, bio/organic compounds are better preserved when protected (via substitution, inclusion, adsorption) by a mineral host to avoid degradation (Parnell et al. Reference Parnell, Cullen, Sims, Bowden, Cockell, Court, Ehrenfreund, Gaubert, Grant, Parro, Rohmer, Sephton, Stan-Lotter, Steele, Toporski and Vago2007). On Earth, organic compounds are often co-deposited in sulphate salts during mineralization (Aubrey et al. Reference Aubrey, Cleaves, Chalmers, Skelley, Mathies, Grunthaner, Ehrenfreund and Bada2006; Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). Likewise, if life once existed on Mars, bio/organic compounds could be incorporated and preserved in the Martian geological record. Sulphate minerals are a likely candidate for bio/organic preservation, since they are ubiquitous on the Martian regolith, forming in evaporitic environments due to weathering of primary basaltic minerals (Squyres et al. Reference Squyres2004). Chemical/mineralogical models using data from SNC-type meteorites, Mars Exploration Rovers and Martian orbiters provide evidence that Na-sulphates are a likely constituent of evaporitic assemblages on Mars (Tosca & McLennan Reference Tosca and McLennan2006). Additionally, spectrometry data from the Visible and Infrared Mineralogical Mapping Spectrometer (OMEGA) aboard the Mars Express orbiter, detected signatures consistent with the presence of thenardite (Na2SO4) near the low-albedo region of Syrtis Major (Zhu et al. Reference Zhu, Xie, Guan and Smith2006). More recently, Mangold et al. (Reference Mangold, Gendrin, Gondet, LeMouelic, Quantin, Ansan, Bibring, Langevin, Masson and Neukum2008) suggested that polyhydrated Na-sulphates may be a constituent in the layered sulphate sequences of West Candor Chasma, known to contain one of the largest sequences of sulphate minerals on Mars.

In addition to Mars, several Galilean satellites have spectrometric signatures characteristic of surficial Na-sulphates. Of these satellites, the moon-sized satellite of Jupiter, Europa, is the most promising in the search for extraterrestrial life, as it probably contains liquid water, biogenic elements and chemical disequilibria (Gaidos et al. Reference Gaidos, Nealson and Kirschvink1999; Kargel et al. Reference Kargel, Kaye, Head, Marion, Sassen, Crowly, Ballesteros, Grant and Hogenboom2000; Chyba & Phillips Reference Chyba and Phillips2002; Chela-Flores Reference Chela-Flores2006). The surface composition of Europa is dominated by water ice with localized regions of non-ice components, consisting mostly of polyhydrated Na- and Mg-sulphate species (McCord et al. Reference McCord1998; McCord et al. Reference McCord1999; Kargel et al. Reference Kargel, Kaye, Head, Marion, Sassen, Crowly, Ballesteros, Grant and Hogenboom2000; Fanale et al. Reference Fanale, Li, De Carlo, Farley, Sharma, Horton and Granahan2001; Zolotov & Shock Reference Zolotov and Shock2001). These sulphate minerals originate as solutes in the internal ocean, probably derived from leaching and degassing of elements on the ocean-rock interface (Fanale et al. Reference Fanale, Li, De Carlo, Farley, Sharma, Horton and Granahan2001). These solutes subsequently are emplaced on the surface by cryovolcanism and impact events (Orlando et al. Reference Orlando, McCord and Grieves2005).

Geomatrix-assisted laser desorption/ionization mass spectrometry (GALDI-MS) is a proven technique capable of characterizing bio/organic compounds associated with terrestrial sulphate minerals (Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008), and possibly bio/organic compounds associated with returned samples from Mars and Europa. This technique uses a mineral matrix to aid in desorption so that organic signatures can be detected along with any bio/organic signatures present in the sample (Yan et al. Reference Yan, Stoner and Scott2007b). Further, the mineral matrix can stabilize organic ions to aid detection. Thus, the ability of minerals to facilitate the ionization and desorption of bio/organic compounds is a primary focus in the effectiveness of GALDI-MS. When used in conjunction with a Fourier transform ion cyclotron resonance mass spectrometer (FTICR-MS) (Scott & Tremblay Reference Scott and Tremblay2002), GALDI-FTICR-MS has the ability to obtain high-resolution spectra using a single laser shot, with low detection limits for chemical signatures, with little or no sample preparation (Yan et al. Reference Yan, Stoner, Kotler, Hinman and Scott2007a; Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). When coupled with imaging or mapping capability (Scott & Tremblay Reference Scott and Tremblay2002), GALDI-FTICR-MS can search for bio/organic signatures in heterogeneous geomatrices from both terrestrial samples (Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008) and future samples returned from Mars and Europa. While FTICR-MS systems are not practical for a rover, a low-power, compact laser desorption quadrupole ion trap mass spectrometer is being developed for deployment on Mars as part of the Mars Organic Molecule Analyzer as part of the ExoMars mission (Evans-Nguyen et al. Reference Evans-Nguyen, Becker, Doroschenko and Cotter2008).

Previous GALDI-FTICR-MS investigations have focused on sulphate salts and halides (NaCl) acting as mineral matrices to facilitate the ionization and desorption of bio/organic compounds (fatty acids, amino acids and proteins) (Yan et al. Reference Yan, Stoner, Kotler, Hinman and Scott2007a,Reference Yan, Stoner and Scottb; Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). These combinations produced inorganic and organic cluster ions (Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008), deprotonated bio/organic compounds ([M-H]−) (Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008) and/or cation-attached peaks [M+Na]+ (Yan et al. Reference Yan, Stoner, Kotler, Hinman and Scott2007a). Polycyclic aromatic hydrocarbon (PAH) compounds are also of interest due to their occurrence throughout the universe, including meteorites (Kotler et al. Reference Kotler, Richardson, Hinman, Scott and Basiuk2009). Unlike most bio/organic compounds, PAH compounds self-ionize during laser ablation and may facilitate the detection of non-ionizing bio/organic compounds (Yan et al. Reference Yan, Stoner and Scott2007b).

The occurrence of thenardite throughout the solar system makes it a primary candidate for GALDI-FTICR-MS studies. The mineral has sufficient gas-phase basicity to abstract a proton from the aliphatic amino acid glycine, contrary to results using other sulphate salts (Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). Furthermore, thenardite taken from a terrestrial evaporitic environment showed signatures consistent with bio/organic compounds (Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). Gas-phase reactions between thenardite and stearic acid produce organic and inorganic cluster ions, similar to cluster ions observed by matrix-assisted laser desorption/ionization (MALDI), such as an accumulation of adducts (Karas & Hillenkamp Reference Karas and Hillenkamp1988), matrix moieties (Knochenmuss et al. Reference Knochenmuss, Dubois, Dale and Zenobi1996) and/or analyte components (Ham et al. Reference Ham, Durham and Scott2003; Budimir et al. Reference Budimir, Blais, Fournier and Tabet2007). Thenardite was also used to ascertain the limit of detection for GALDI-FTICR-MS, estimated to be approximately three parts per trillion based on bulk concentrations, corresponding into ~7 zeptomoles (10−21) per laser shot (Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008).

In this study, we evaluate the ability of thenardite to facilitate the desorption, ionization and detection of aromatic amino acids using GALDI-FTICR-MS. Aromatic compounds were chosen because they have been proposed as primary biosignature targets in the solar system (Storrie-Lombardi et al. Reference Storrie-Lombardi, Hug, McDonald, Tsapin and Nealson2001; McKay Reference McKay2007; Parnell et al. Reference Parnell, Cullen, Sims, Bowden, Cockell, Court, Ehrenfreund, Gaubert, Grant, Parro, Rohmer, Sephton, Stan-Lotter, Steele, Toporski and Vago2007), as they readily donate electrons via multiple metabolic pathways during protein synthesis in terrestrial microorganisms (Porat et al. Reference Porat, Waters, Teng and Whitman2004; Plekan et al. Reference Plekan, Feyer, Richter, Coreno and Prince2008). Spectra obtained from mixing of individual aromatic amino acids (tryptophan, tyrosine and phenylalanine) with thenardite were evaluated for differences in ionization and fragmentation patterns. The effectiveness of thenardite to assist in the detection of aromatic amino acids and other bio/organic signatures, along with its occurrence on Mars and Europa, further signifies its importance in the search for life in the solar system.

Materials and methods

Physical mixtures of thenardite (Fischer Scientific, Pittsburgh, PA) with phenylalanine, tyrosine and tryptophan (Sigma-Aldrich, St. Louis, MO) were prepared following the methods of Richardson et al. (Reference Richardson, Hinman, McJunkin, Kotler and Scott2008) and Yan et al. (Reference Yan, Stoner, Kotler, Hinman and Scott2007a). Approximately 1×10−4 mole (0.02 g) of tryptophan was added to 10 g of thenardite. The mixture was then mixed for approximately 5 min at 70 Hz using a vortex mixer (Model 231, Fischer Scientific, Pittsburgh, PA) with two 4.5 mm zinc-plated steel ball bearings (Premium Grade BBs, Daisy Outdoor Products, Rogers, AR) to ensure a relatively homogeneous sample corresponding to a bulk concentration of approximately 2 ppm. The phenylalanine and tyrosine samples were produced in a similar manner to that of tryptophan.

Lower concentrations of phenylalanine, tyrosine and tryptophan with thenardite were produced by a series of dry serial dilutions with incremental steps of 10−3 molar. The resulting samples had an approximate concentration of 1 nM (approximately 3 ppb). Vortex mixing was completed between all dilutions steps to ensure homogeneity, similar to previous methods by Richardson et al. (Reference Richardson, Hinman, McJunkin, Kotler and Scott2008) and Yan et al. (Reference Yan, Stoner, Kotler, Hinman and Scott2007a). Samples were then pressed into half-inch pellets using a Beckman dye with a Carver Laboratory Press (Menomonee Falls, WI) at an approximate pressure of 3.5×10−7 Pa. Samples were subsequently mounted on copper discs using epoxy (Devcon 5 minute epoxy, Danvers, MA). To prevent absorption of the epoxy, the epoxy was allowed to dry for approximately 5 min before applying the sample pellet.

Instrumentation

Mass spectra were obtained using a laboratory-built imaging laser desorption FTICR-MS (McJunkin et al. Reference McJunkin, Tremblay and Scott2002; Scott & Tremblay Reference Scott and Tremblay2002; Scott et al. Reference Scott, McJunkin and Tremblay2003) with a 7 T Oxford (Oxford, England) superconducting magnet. Instrumental parameters are similar to those previously described (Yan et al. Reference Yan, Stoner, Kotler, Hinman and Scott2007a,Reference Yan, Stoner and Scottb; Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). Data acquisition was accomplished using an Odyssey control and data acquisition computer system (Finnigan FT/MS, Bremen, Germany). Desorption/ionization was performed using a Nd:YAG laser (Continuum, Santa Clara, CA) operating at 355 nm with a 6 ns laser pulse and an irradiance of 1×108 W cm−2, unless otherwise specified. During ionization, voltage potential between the front and back plates was maintained at 0 V, while after ionization, a trapping potential of 2 V was applied to both trap plates. A delay of 0.5 s was allowed prior to chirp excitation over the range of 50 Hz to 4 MHz (corresponding to m/z 105 and 26.9, respectively) with a sweep rate of 3600 Hz μs−1. Ions were detected in direct mode using 128 K data points. After acquisition, data was baseline corrected, Hamming apodized, zero filled, and Fourier transformed. Pressure during analysis was at most 4×10−9 Torr. For the given parameters, the LD-FTICR-MS has a mass error of ±0.003 Da, resolution of ~10 000), high sensitivity (⩽400 ions for peaks with signal-to-noise ratio ~3) for m/z range <2000 Da. All spectra were acquired with single laser shots and in the positive mode unless specified otherwise. Peak identification was accomplished by systematic analysis following the method described in Kotler et al. (Reference Kotler, Hinman, Yan, Stoner and Scott2008). Additional information regarding FTICR-MS can be found in the literature (Comisarow Reference Comisarow1993; Marshall et al. Reference Marshall, Hendrickson and Jackson1998; Marshall & Hendrickson Reference Marshall and Hendrickson2002).

Results and discussion

The possibility of life on Mars and Europa in conjunction with the occurrence of endogenous Na-sulphates that could potentially harbour signatures of life makes understanding the interaction between Na-sulphates and bio/organic compounds crucial for the potential applications for laser desorption mass spectrometry (LDMS) techniques in the search for extraterrestrial life in the solar system. A first step towards understanding the spectra is distinguishing the difference between peaks produced from inorganic ions generated from the mineral and those of the bio/organic compounds of interest. The second major step is determining if the mineral is likely to affect the types of peaks observed from the bio/organic compounds, which is the primary focus of this paper.

Positive spectra of the mineral thenardite (Fig. 1) by itself are dominated by a small number of peaks. The peaks represent inorganic cluster ions at m/z 164, 265, 279 and 305. These peaks are easily identified as representing inorganic ions, based on their mass defect (Sack et al. Reference Sack, Lapp, Gross and Kimble1984; McLafferty & Tureček Reference McLafferty and Tureček1993; Kim et al. Reference Kim, Rodgers and Marshall2006; Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008). The high mass accuracy and resolution of FTICR-MS enables distinction between inorganic and organic ions. Detailed explanation and methodology for identification of peaks is found in Kotler et al. (Reference Kotler, Hinman, Yan, Stoner and Scott2008) and Richardson et al. (Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). The presence of H, and some of the O, in the inorganic ions is likely to be the result of remnant water left behind from hydrated Na-sulphate mineral phases. Similar inorganic cluster ions have been previously reported in Na-sulphate spectra (Van Vaeck et al. Reference Van Vaeck, Adriaens and Adams1998; Kotler et al. Reference Kotler, Hinman, Yan, Stoner and Scott2008; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008), including the Na3SO4+ peak at m/z 164 observed by Van Vaeck et al. (Reference Van Vaeck, Adriaens and Adams1998). Unlike the negative mode spectra of thenardite which show numerous inorganic cluster ions (Richardson et al., Reference Richardson, Hinman, McJunkin, Kotler and Scott2008), the positive mode spectrum of thenardite (Fig. 1) shows significantly fewer peaks.

Fig. 1.

Positive ion GALDI-FTICR-MS spectrum of thenardite.

The aromatic amino acids are presented from lowest to highest molecular weight, which also corresponds with their cation affinities (i.e. Phe<Tyr<Trp). A common fragmentation occurs from the cleavage of the Cα—Cβ bond (location of Cα—Cβ bond in the aromatic amino acids is shown in Fig. 2, using Phe for illustration) for all of the aromatic amino acids (Plekan et al. Reference Plekan, Feyer, Richter, Coreno and Prince2008). The structural schemes in Figs 3, 4 and 5 are provided as an aid to understanding how the ions are related to the neutral amino acid and as possible formation pathways to the observed ions. They are not necessarily indicative of the actual gas-phase structure, which can be quite complex (McLafferty & Tureček Reference McLafferty and Tureček1993; El Aribi et al. Reference El Aribi, Orlova, Hopkinson and Siu2004) and are beyond the scope of this paper.

Fig. 2.

The location of Cα—Cβ bond in the aromatic amino acids, using Phe for illustration.

Fig. 3.

GALDI-FTICR-MS spectra showing (a) phenylalanine alone and (b) thenardite mixed with phenylalanine (3 ppb). The numbers next to the peaks on (a) correspond to the possible fragmentation ion illustrated in scheme (c). Inorganic cluster ions are designated by ×'s. Structures shown in (c) are not indicative of the actual gas-phase structure, but are shown as a reference to the neutral phenylalanine structure.

Fig. 4.

GALDI-FTICR-MS spectra showing (a) tyrosine alone and (b) thenardite mixed with tyrosine (3 ppb). The numbers next to the peaks on (a) correspond to the possible fragmentation ion illustrated in scheme (c). Likewise values on (b) correspond to the possible fragmentation ion illustrated in scheme (d). Inorganic cluster ions are designated by ×'s. Structures shown in (c) and (d) are not indicative of the actual gas-phase structure, but are shown as a reference to the neutral tyrosine structure.

Fig. 5.

GALDI-FTICR-MS spectra showing (a) tryptophan alone and (b) thenardite mixed with tryptophan (3 ppb). The numbers next to the peaks on (a) correspond to the possible fragmentation ion illustrated in scheme (c). Likewise values on (b) correspond to the possible fragmentation ion illustrated in scheme (d). Inorganic cluster ions are designated by ×'s. Structures shown in (c) and (d) are not indicative of the actual gas-phase structure, but are shown as a reference to the neutral tryptophan structure.

The spectrum of phenylalanine alone (Fig. 3(a)) is dominated by fragmentation of the molecular backbone and the phenyl aromatic ring ion. Decarboxylation of the molecular backbone results in the peak at m/z 120. Further fragmentation is seen in the cleavage of the Cα—Cβ bond of the molecular backbone resulting in the positively charged C2H4NO2+ fragmented backbone at m/z 74 and the phenyl ring fragment observed at m/z 91 (Fig. 3(c)). The high intensity peaks at m/z 155 and 139 in the phenylalanine spectrum (Fig. 3(a)) are due to sample contamination (<1%) of alkali ions (K+, Na+) and their subsequent gas-phase interactions. These contaminants may have been introduced via a salt with its own counter anion, or as a salt of phenylalanine. Regardless of the exact source of the contaminants, these cluster ions have inorganic compositions based on their high mass defects. Furthermore, systematic analysis of their isotopic distribution supports the presence of alkali elements and their subsequent interaction with the phenylalanine and thenardite moieties. Further, the peak at m/z 38.96 corresponds to singly charged K+ ions. Alkali element contamination has been reported in similar spectra of aromatic amino acids (Karas et al. Reference Karas, Bachmann and Hillenkamp1985; Willey et al. Reference Willey, Vorsa, Braun and Winograd1998; Plekan et al. Reference Plekan, Feyer, Richter, Coreno and Prince2008). The high intensity of the alkali element-attached peaks reflects the ease of alkali element ionization at 355 nm, resulting in abundant alkali element desorption and subsequent high intensity peaks (Karas et al. Reference Karas, Bachmann and Hillenkamp1985; Scott et al. Reference Scott, Yan and Stoner2006; Yan et al. Reference Yan, Stoner and Scott2007b), although the exact formation mechanisms of these cluster ions are highly speculative and unclear at this time.

Excluding the alkali element-cluster peaks, the highest intensity peak in the phenylalanine spectrum (Fig. 3(a)) is caused by decarboxylation ([M-COOH]+), contrary to studies by Plekan et al. (Reference Plekan, Feyer, Richter, Coreno and Prince2008) whose major peak corresponded to breakage of the Cα—Cβ bond and the subsequent formation of the molecular backbone ion. The difference in major peaks between studies is likely to be a function of the laser irradiance and system parameters. Major peaks corresponding to [M-COOH]+ were observed using LDMS instrumentation (Karas et al. Reference Karas, Bachmann and Hillenkamp1985) under higher laser intensities than were used in this study. High laser fluences could cause ablation at the laser–mineral interface rather than desorption (Aubriet et al. Reference Aubriet, Carre and Muller2005; Aubriet Reference Aubriet2007; Aubriet & Muller Reference Aubriet and Muller2008). However, the distinction between desorption and ablation processes for GALDI-FTICR-MS has not been determined because only one type of spectral signature was observed when varying the laser irradiance. The relatively high laser irradiance used in GALDI-FTICR-MS appears to be necessary for optimal ionization due to the refractory nature of the host minerals.

The absence of peaks in mixed phenylalanine–thenardite spectra (Fig. 3(b)) implies that there are competitive gas-phase reactions. This competition results in the self-ionized peaks of phenylalanine being completely suppressed. However, there is also an absence of cation-attached peaks of phenylalanine, which would be expected due to the presence of thenardite. The absence of cation-attached peaks associated with phenylalanine may also be the result of the low binding energy of Na+ with the phenyl ring as well as with the carbonyl oxygen and the nitrogen of the amine group (Dunbar Reference Dunbar2000; Ryzhov et al. Reference Ryzhov, Dunbar, Cerda and Wesdemiotis2000). Binding energies associated with the aromatic amino acids tend to decrease with decreasing polarization of the aromatic ring, although the stability of Na+ chelation with phenylalanine is largely controlled by the carbonyl oxygen and/or amine nitrogen (Ryzhov et al. Reference Ryzhov, Dunbar, Cerda and Wesdemiotis2000). It follows that cation affinity associated with tryptophan will be greater than tyrosine and even more so than phenylalanine. This is further supported by collision-induced dissociation experiments showing that Na+ tends to form stronger bonds with phenol than with benzene rings (Armentrout & Rodgers Reference Armentrout and Rodgers2000), which is contradictory to studies by Ryzhov et al. (Reference Ryzhov, Dunbar, Cerda and Wesdemiotis2000) and Dunbar (Reference Dunbar2000) that suggest Na+ binds to phenol and benzene rings with equal strength. Even though phenylalanine is less prone to cationization than tyrosine or tryptophan, cation attachment can occur when the laser intensity is near the optimized peak height irradiances of singly-charged alkali element ions (Karas et al. Reference Karas, Bachmann and Hillenkamp1985). At these irradiances, the alkali element ions and cation-attached peaks have comparable peak heights, but at higher intensities alkali element ion formation dominates, while cation-attached abundances decrease (Karas et al. Reference Karas, Bachmann and Hillenkamp1985). This observation is concurrent with the peak heights of the singly charged K+ ions and alkali element-attached inorganic cluster ions in Fig. 3(a). Thus, the absence of Na-attachment peaks in Fig. 3(b) could reflect both the low cation binding energy of phenylalanine and the typical laser intensity used in this study, while the absence of self-ionized peaks in Fig. 3(b) may result from thenardite suppressing the self-ionization mechanisms of phenylalanine. The exact mechanisms are still unclear, but could reflect the suppression of ion formation or that the self-ionization occurs, but is subsequently neutralized in the desorption plume due to their interaction with desorption products from thenardite.

The major peak of the tyrosine spectrum (Fig. 4(a)) is observed at m/z 107 (C7H7O+), which is consistent with previous tyrosine spectra (Vorsa et al. Reference Vorsa, Kono, Willey and Winograd1999; Plekan et al. Reference Plekan, Feyer, Richter, Coreno and Prince2008). The C7H7O+ ions arise from fragmentation of the Cα—Cβ bond and the concomitant loss of the H+ ion from the attached hydroxyl group (Fig. 4(c)). The additional loss of the O from the C7H7O+ ion leads to the C7H7+ fragment ion (m/z 91). Fragmentation of the molecular backbone (Fig. 4(c)) is observed by successive cleaving of the amine group ([M-NH2]) and the carboxyl group ([M-COOH]) at m/z 165 and 136, respectively. This fragmentation is consistent with previous tyrosine spectra (Vorsa et al. Reference Vorsa, Kono, Willey and Winograd1999). Both fragments are less than 10% of the major peak and comparable in intensity to the molecular ion at m/z 182.

Structurally, tyrosine is identical to phenylalanine with the addition of a hydroxyl group bonded to the aromatic ring. Although this hydroxyl group is located far from the Cα—Cβ bond, the tyrosine spectrum is much different than the phenylalanine spectrum. This dichotomy results from the ionization energy potentials and the preferential organization of the positive charge after cleavage of the Cα—Cβ bond. For tyrosine, the lowest ionization energy is attributed to the removal of the π-electron from the phenol functional group; this differs from phenylalanine where the lowest ionization energy corresponds to removal of the amine-group electron or the phenyl-group electron (Campbell et al. Reference Campbell, Beauchamp, Rempe and Lichtenberger1992; McLafferty & Tureček Reference McLafferty and Tureček1993). As a result, the positive charge in tyrosine is transferred to the Cβ fragment (phenol ring) (Willey et al. Reference Willey, Vorsa, Braun and Winograd1998; Plekan et al. Reference Plekan, Feyer, Richter, Coreno and Prince2008). Conversely, for phenylalanine the relocation of the positive charge is dominated by the Cα fragment. This preferential charge localization in tyrosine along with the subsequent hydroxyl deprotonation from the phenol group leads to the formation of the C7H7O+ major peak. The presence of this peak suggests that thenardite does not significantly affect the C7H7O+ formation mechanism. Conversely, the self-ionization peaks in the phenylalanine spectrum are suppressed and absent when phenylalanine is associated with thenardite.

Unlike the corresponding phenylalanine spectrum, the spectrum of tyrosine mixed with thenardite (Fig. 4(b)) is virtually devoid of inorganic cluster ions, although inorganic cluster ions were observed in other spectra from the same sample. This discrepancy is not unusual considering the single-shot technique and the heterogeneity of the sample. Additionally, it is possible that inorganic cluster ion formation may be affected by the relative amount of organic constituent present in a particular shot. However, only a small number of peaks are typically observed in the spectra, which are either from tyrosine fragmentation or cation attachment between thenardite and tyrosine (Fig. 4(d)). An exception is found in the peaks at m/z 78 and 100, which represent inorganic cluster ions based on their mass defect, similar to peaks found in previous spectra of Na-sulphates (Van Vaeck et al. Reference Van Vaeck, Adriaens and Adams1998; Richardson et al. Reference Richardson, Hinman, McJunkin, Kotler and Scott2008). It is likely that the presence of the organic analyte affects the production of the inorganic peaks from thenardite, possibly through alterations of the desorption process or through competitive gas-phase reactions.

The major peak in spectra from the tyrosine mixed with thenardite samples (Fig. 4(b)) corresponds to Na+ binding to the π-electron from the aromatic ring of tyrosine (Fig. 4(d)). This Na-π bond is likely to be centred across the face of the aromatic ring with chelation by the phenol ring as well as the amine nitrogen and carbonyl oxygen (Ryzhov et al. Reference Ryzhov, Dunbar, Cerda and Wesdemiotis2000). An additional sodium exchanges with the hydrogen of the carboxyl group to form the alkaline carboxylate salt, either in the condensed phase or in a gas-phase reaction, leading to formation of [M-H+Na]Na+ ions observed at m/z 226 with a peak height roughly half that of the single cation-attached peak. An ion with two alkali metals attached is sometimes referred to as a double-cation attached ion (Tomlinson et al. Reference Tomlinson, Scott, Wilkins, Wright and White1999; Lou et al. Reference Lou, Sinkeldam, van Houts, Nicolas, Janssen, van Dongen, Vekemans and Meijer2007), which is a slight misnomer because only one of the alkali metals is providing the charge for the singly charged ion.

The structure of tryptophan is characterized by the indole functional group: a benzene ring attached to an N-heterocyclic five-member ring (pyrrole). The major peak (m/z 130) of the tryptophan spectrum (Fig. 5(a)) is attributed to the dehydroindole ion (C9H8N+). This major peak is consistent with previous studies of tryptophan mass spectra (Junk & Svec Reference Junk and Svec1963; Vorsa et al. Reference Vorsa, Kono, Willey and Winograd1999; Wilson et al. Reference Wilson, Jimenez-Cruz, Nicolas, Belau, Leone and Ahmed2006; Plekan et al. Reference Plekan, Feyer, Richter, Coreno and Prince2008). Fragmentation of the molecular backbone (Fig. 5(c)) is evident as loss of the amine group ([M-NH2]) at m/z 188, similar to previous observations using LDMS (Karas et al. Reference Karas, Bachmann and Hillenkamp1985; Wilson et al. Reference Wilson, Jimenez-Cruz, Nicolas, Belau, Leone and Ahmed2006; Gogichaeva et al. Reference Gogichaeva, Williams and Alterman2007), and time-of-flight secondary ion mass spectrometry techniques (Vorsa et al. Reference Vorsa, Kono, Willey and Winograd1999). Additional fragmentation of the molecular backbone is seen at m/z 159, corresponding to decarboxylation.

Figure 5(b) shows a spectrum of thenardite mixed with tryptophan. The major peak in the spectrum, as with the tryptophan spectrum, corresponds to the dehydroindole ion at m/z 130. Simple cation attachment [M+Na]+ is observed at m/z 227, corresponding to a Na+ ion attaching to the indole functional group (Fig. 5(d)). Further gas-phase reactions between tryptophan and thenardite lead to the formation of the double cation-attached ion ([M-H+Na]Na+) observed at m/z 249 (Fig. 5(d)). This peak is roughly 80% of the major peak and slightly less abundant than the [M+Na]+ peak.

As previously mentioned, Na+ has the strongest affinity to bind with tryptophan, evidenced by the presence and high abundance of both the single and double cation-attached peaks in Fig. 5(b). The formation of the double cation-attached peak (m/z 249) is accomplished via a multiple step process (Fig. 5(d)). Initially, a Na+ ion attaches to the π-electron of the indole aromatic ring. This attachment is likely to be offset to the side of the pyrrole ring face, rather than the benzene ring, because of differences in binding energies between the two regions of the indole group. This offset position above the pyrrole ring results in cation chelation to the nitrogen from the amine group, the oxygen from the carbonyl group, and the π-electrons from the pyrrole group (Ryzhov et al. Reference Ryzhov, Dunbar, Cerda and Wesdemiotis2000). Secondly, another Na+ from thenardite replaces the H+ ion from the carboxyl group, either in the desorption plume or in the gas phase, leading to the formation of the [M+Na-H]Na+ ion (Yan et al. Reference Yan, Stoner and Scott2007b). Comparison of the tyrosine and tryptophan spectra, with and without thenardite present, suggests that cation attachment competes with and suppresses the self-ionization mechanisms and some related fragmentation pathways. However, fragment peaks related to the aromatic side chains of tyrosine and tryptophan are still observed in the presence of thenardite.

Other minerals can also provide cations to function in a similar manner to thenardite for ionizing bio/organic compounds. Sodium ions from the mineral halite (NaCl) participate in the formation of cation-attached peaks associated with the amino acids histidine, threonine and cysteine (Yan et al. Reference Yan, Stoner and Scott2007b). These results are not surprising considering the ease with which Na+ ionizes and its affinity to interact with bio/organic compounds in the desorption plume or gas phase (Liu et al. Reference Liu, Tseng and Lebrilla2001); however, it is interesting to note that high concentrations of salts, similar to the minerals halite and thenardite, suppress ion formation in MALDI (Goheen et al. Reference Goheen, Wahl, Campbell and Hess1997; Yao et al. Reference Yao, Scott, Young and Wilkins1998). Cation attachment to histidine (Yan et al. Reference Yan, Stoner and Scott2007b) is not surprising, considering the aromaticity and the high alkali affinity of histidine (Kish et al. Reference Kish, Ohanessian and Wesdemiotis2003). Thus, cation-attachment mechanisms of histidine with halite are likely to be similar to that described above for tyrosine and tryptophan in the presence of thenardite. As threonine and cysteine are aliphatic amino acids, the formation of their cation-attached peaks is likely to be different than their aromatic counterparts. Regardless of the formation mechanisms, the occurrence of cation-attached peaks associated with different Na-salt geomatrices (halide and sulphate) suggests that Na+ ionization and subsequent gas-phase interactions are common, regardless of the anion or oxyanion moiety.

Conclusions

Pure samples of the aromatic amino acids (phenylalanine, tyrosine and tryptophan) all produce ions through self-ionization mechanism(s) and produce similar fragmentation patterns when thenardite is absent. In all spectra, the fragmentation of the molecular backbone is observed by loss of the carboxyl group. Spectra from tyrosine and tryptophan show additional loss of the amine group. Further, fragmentation is observed in aromatic side chains, which accounts for the major peaks in the tyrosine and tryptophan spectrum, which is consistent with ionization potentials between the aromatic ring and the molecular backbone.

Of the aromatic amino acids used in this study, tyrosine and tryptophan associated with thenardite are observed to undergo cationization. The cation attachment results from the high affinity of the aromatic side chain for binding with alkali metal ions. Substitution of the carboxyl hydrogen by Na leads to formation of ‘double cation-attached’ ions. In contrast, phenylalanine shows no evidence of Na+ interaction, a consequence of system parameters (e.g. laser intensity, wavelength) and/or lower alkali element-binding energy. In addition, the presence of thenardite suppresses all of the self-ionized peaks that are definitive for the presence of phenylalanine, leaving only fragment peaks common to all three aromatic amino acids studied. However, the ability of cation attachment to out-compete and suppress the majority of the self-ionized peaks for tyrosine and tryptophan associated with thenardite makes interpretation of spectra for these aromatic amino acids less complicated.

The effectiveness of thenardite, and other Na-related geomatrices, for detection of bio/organic compounds is a product of analyte–matrix interactions and competitive gas-phase reactions. Understanding these types of Na–sulphate mineral and bio/organic compound interactions has astrobiological implications because terrestrial Na–sulphate mineral deposits are known to harbour bio/organic compounds; therefore, the presence of these minerals on Mars and Europa represents a prime opportunity to search for signs of life using LDMS instruments on rovers.

Acknowledgments

The authors acknowledge support from the National Aeronautics and Space Agency (NASA) Exobiology Program (NNX08AP59G). CDR would also like to thank Montana Space Grant Consortium for support. Research performed at the Idaho National Laboratory under DOE Idaho Operations Office Contract DE-AC07-05ID14517.

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Figure 0

Fig. 1. Positive ion GALDI-FTICR-MS spectrum of thenardite.

Figure 1

Fig. 2. The location of Cα—Cβ bond in the aromatic amino acids, using Phe for illustration.

Figure 2

Fig. 3. GALDI-FTICR-MS spectra showing (a) phenylalanine alone and (b) thenardite mixed with phenylalanine (3 ppb). The numbers next to the peaks on (a) correspond to the possible fragmentation ion illustrated in scheme (c). Inorganic cluster ions are designated by ×'s. Structures shown in (c) are not indicative of the actual gas-phase structure, but are shown as a reference to the neutral phenylalanine structure.

Figure 3

Fig. 4. GALDI-FTICR-MS spectra showing (a) tyrosine alone and (b) thenardite mixed with tyrosine (3 ppb). The numbers next to the peaks on (a) correspond to the possible fragmentation ion illustrated in scheme (c). Likewise values on (b) correspond to the possible fragmentation ion illustrated in scheme (d). Inorganic cluster ions are designated by ×'s. Structures shown in (c) and (d) are not indicative of the actual gas-phase structure, but are shown as a reference to the neutral tyrosine structure.

Figure 4

Fig. 5. GALDI-FTICR-MS spectra showing (a) tryptophan alone and (b) thenardite mixed with tryptophan (3 ppb). The numbers next to the peaks on (a) correspond to the possible fragmentation ion illustrated in scheme (c). Likewise values on (b) correspond to the possible fragmentation ion illustrated in scheme (d). Inorganic cluster ions are designated by ×'s. Structures shown in (c) and (d) are not indicative of the actual gas-phase structure, but are shown as a reference to the neutral tryptophan structure.