Formation of amino acid precursors in early aqueous alteration in small bodies: Synergetic effects of gamma rays and hydrothermal processing

Abstract

Organic compounds such as amino acids may have been delivered to the early Earth via carbonaceous chondrites and interplanetary dust particles. Mineralogical and petrological evidence has shown that liquid water was formed from water ice in the early stages of the formation of the parent bodies of carbonaceous chondrites, due to the heat from the radioactive decay of short-lived radionuclides such as ²⁶Al. In previous research, amino acid precursors were produced from aqueous solutions containing formaldehyde and ammonia by hydrothermal experiments and gamma-ray irradiation experiments to evaluate organic formation during aqueous alteration processes in meteorite parent bodies. However, the differences in the effects and reactions of gamma rays and heating, as well as the synergetic effects, are not well understood. In this study, both heating and gamma irradiation were applied to aqueous solutions containing formaldehyde, methanol, and ammonia to investigate the synergistic effects of heating and gamma rays on amino acid formation. The results showed that gamma irradiation followed by heating was more efficient in producing amino acid precursors compared to heating followed by gamma irradiation. The characteristic features of UV-visible and fluorescence spectra of the experimental products were consistent with Maillard-type reactions, suggesting that Maillard-type reactions led to the formation of amino acid precursors.

Introduction

How first life emerged on Earth is a fundamental question for us, which has not been solved despite various approaches by researchers in many fields. Immediately after the formation of the Earth, the surface temperature was too high for organic matter to exist, thus organic matter must have been supplied after the surface cooled. Several hypotheses and experimental findings suggest various pathways through which organic molecules could have formed on the pre-biotic Earth. The Miller-Urey Experiment demonstrated that amino acids could be synthesized from strongly reducing atmosphere when subjected to electrical sparks, simulating lightning (Miller, 1953; Miller and Urey, 1959). However, such an atmosphere is no longer regarded as realistic. Recent studies have shown the formation of amino acids via, for example, metal-promoted electrochemistry in early ocean alkaline hydrothermal systems (Kitadai et al., 2019), a simulated meteorite impact reaction on the Earth’s ocean (Takeuchi et al., 2020), UV photochemistry of a simulated early Earth atmosphere (Zang et al., 2022), and a simulated solar energetic particles from the young Sun into the early Earth atmosphere (Kobayashi et al., 2023). Alternatively, the supply of organic matter from extraterrestrial sources is also considered (Chyba and Sagan, 1992).

Carbonaceous chondrites, a class of primitive meteorites derived from small solar system bodies, contain a wide variety of organic materials, including amino acids (Elsila et al., 2016; Kvenvolden et al., 1970), sugars (Cooper et al., 2001; Furukawa et al., 2019), and nucleobases (Callahan et al., 2011; Martins et al., 2008; Oba et al., 2022), which may have been the raw materials of life. These organic materials are thought to have formed and reacted in various processes throughout the formation history of the Solar System, from molecular clouds to protoplanetary disks and small bodies. In the parent bodies of carbonaceous meteorites, it is known that the decay heat of radionuclides such as ²⁶Al melted ice and produced liquid water, which formed hydrous minerals and other secondary minerals (Brearley, 2006). Chemical processes in such small bodies were an important stage in determining the final forms of organic matter before it reached Earth.

Hydrothermal processes experienced by type 1 and type 2 carbonaceous chondrites containing organic matter have been estimated to have ranged from 0°C to 150°C (Brearley, 2006). Experimental studies suggested that hydrothermal reactions produced complex organic material through formose-type and Maillard-type reactions (Cody et al., 2011; Isono et al., 2019; Kebukawa and Cody, 2015; Kebukawa et al., 2013, 2020; Vinogradoff et al., 2018, 2020a). Amino acids could have been formed from simple molecules such as formaldehyde and ammonia (Kebukawa et al., 2017; Koga and Naraoka, 2017, 2022). The presence of minerals promoted or inhibited the formation of amino acids on these reactions (Elmasry et al., 2021; Vinogradoff et al., 2020b). Further alteration of amino acids may have occurred by geoelectrochemistry in carbonaceous chondrite parent bodies (Li et al., 2022, 2023). More recently, studies have shown that radiation such as gamma rays emitted by radionuclides also promotes the formation of amino acids (Ishikawa et al., 2024; Kebukawa et al., 2022). Such radiation-induced nonequilibrium reactions can produce products that are different from those produced by chemical equilibrium reactions.

A radioactive nuclide, ²⁶Al, with a half-life of 7.17 × 10⁵ years, which is considered to be the major heat source for aqueous alteration in the parent bodies during the early solar system, decays to ²⁶Mg by β⁺ decay, and its daughter ²⁶Mg atom is in an excited state, then decays to the ground level by emitting gamma rays (Castillo-Rogez et al., 2009). The initial abundance of ²⁶Al in parent bodies has been estimated from the excess of ²⁶Mg in meteorites (e.g., MacPherson et al., 1995). In the case of the Murchison meteorite, the total gamma-ray emission energy can be calculated to be approximately 6.3 × 10⁶ J/kg (Kebukawa et al., 2022). Half of this, ~3 × 10⁶ J/kg, would have been emitted during its half-life of ~0.7 million years.

Previous studies have shown that the formation processes of amino acids by gamma-ray-induced radical reactions are likely to be different from those by heating (Ishikawa et al., 2024; Kebukawa et al., 2022). The aim of this study is to investigate the synergy of both heat and gamma radiation in the parent bodies during aqueous alteration. We also analyzed the reaction product with UV-visible absorption and fluorescence spectroscopy to investigate complex mixtures of whole reaction products likely to contain macromolecular materials.

Methods

Gamma-ray irradiation and heating experiments

Gamma-ray irradiation and heating experiments were performed based on Kebukawa et al. (2022) and Ishikawa et al. (2024). Starting aqueous solutions containing ammonia, formaldehyde, and methanol with the molar ratios of H₂O:NH₃:HCHO:CH₃OH = 100:3:7:1.17 were prepared from 0.77 g of 25% ammonia aqueous solution and 2.28 g of 37% (mass/mass) formaldehyde aqueous solution (containing 6.6% methanol), in addition to 5.13 g of water. The initial pH was 10.2 which is consistent with the alteration conditions in parent bodies of CI and CM chondrites were estimated between pH 6 to pH 12 (Brearley, 2006 and references there in). A 300-μL aliquot of the solution was placed in a glass tube (6 mm diameter and typically 10–15 cm long) using a micropipette. The glass tubes were placed in liquid nitrogen to freeze the aqueous solution, and the tubes were flame sealed while evacuated to remove oxygen that could affect the reactions. Note that, because we did not know the initial composition of the parent bodies of the aqueously altered carbonaceous chondrites, the initial composition was based on the abundance of ammonia, formaldehyde, and methanol in comets, e.g., H₂O:NH₃:HCHO:CH₃OH = 100:≤1.5:≤4:≤4 (Mumma and Charnley, 2011). Such an estimation is at least reasonable for parent bodies of such as CI chondrites and Ryugu, which may have similar origins to comets (Gounelle and Zolensky, 2014) and may have come from lower temperature environments (Nakamura et al., 2023), and are expected to contain volatile species at the initial stages of aqueous alteration. In addition, the recent discovery of ammonium salts on the surface of comets and some asteroids suggests that ammonium salts may exist inner region of the ammonia snowline due to their higher sublimation temperatures (Poch et al., 2020). However, quantitative estimates of the expected abundance of ammonium salts in the parent bodies of hydrated asteroids are currently unknown, and with our current knowledge, the comet values are the best estimate of the starting materials for our experiments. In addition, our experiments were conducted in a closed system without the presence of minerals. Although these effects may be of interest, our current equipment did not allow open system experiments, and the effects of the presence of minerals have been studied elsewhere (Elmasry et al., 2021).

The sealed glass tubes were irradiated with gamma rays at room temperature at 2.6 kGy/h using a ⁶⁰Co gamma ray source at the Zero Carbon Research Institute, Institute for the Creation of Science and Technology, Tokyo Institute of Technology. The temperatures during gamma-ray irradiation experiments did not exceed 40°C, as confirmed by a temperature label (VL-40, NiGK Corp.). Heating experiments were performed at 100°C for 72 h in an oven (ETTAS HTO-450s, AS ONE Co.). All the experimental conditions and sample name abbreviations are listed in Table 1. Some samples were exposed to gamma-ray irradiation followed by heating at 100°C (γ40 + Heat and γ80 + Heat), and some were exposed to heating at 100°C followed by gamma-ray irradiation (Heat + γ40 and Heat + γ80). A control sample was prepared in the same manner (an aqueous solution of NH₃, HCHO, and CH₃OH, but without heating or irradiation) and stored in a freezer until analysis.

Table 1.

Experimental conditions, yields of amino acids, UV-Vis absorption and fluorescence parameters

Experimental conditions	Abbreviation	Concentration (μM)**				Ala/Gly	β-ala/gly	UV-Vis			Fluorescence (Abs corrected)
		Glycine	Alanine	β-alanine	Total			Absmax	λmax	Integrated Abs (240–500 nm)	Ex. max (nm)	Em. max (nm)	Intensity
Control	Control	20.6	11.8	49.6	81.9	0.57	2.41	—	—	0.473	—	—	—
100°C 72 h	Heat	7.06	15.2	54.6	76.8	2.15	7.72	0.01	271.0	1.49	340	430	2.1
2.6 kGy/h × 40 h	γ40	50.6	30.4	184	265	0.60	3.63	0.65	263.0	27.2	330	410	13
2.6 kGy/h × 80 h	γ80	85.9	21.9	208	315	0.26	2.42	1.15	263.5	54.2	330	410	58
2.6 kGy/h × 168 h	γ168	156	53.5	403	612	0.34	2.58	1.24	268.0	102	330	410	482
2.6 kGy/h × 336 h	γ336	200	62.6	439	702	0.31	2.19	1.48	274.5	142	330	410	776
2.6 kGy/h × 504 h	γ504	192	57.2	369	619	0.30	1.92	1.65	278.0	192	330	410	1246
2.6 kGy/h × 1143 h	γ1143	281	89.3	552	922	0.32	1.97	—	—	222	340	420	1377
100°C 3d + 2.6 kGy/h × 40 h	Heat + γ40	33.8	23.6	122	179	0.70	3.60	0.61	289.0	31.1	340	420	42
100°C 3d + 2.6 kGy/h × 80 h	Heat + γ80	60.9	37.0	193	290	0.61	3.17	0.55	288.5	36.6	340	415	149
2.6 kGy/h × 40 h + 100°C 3d *	γ40 + Heat	60.9	74.4	275	410	1.22	4.52	4.02	274.5	382	340	430	391
2.6 kGy/h × 80 h + 100°C 3d *	γ80 + Heat	96.4	139	346	582	1.44	3.59	7.11	273.0	698	340	430	839

* The UV-Vis absorption and fluorescence spectra were obtained at 10× dilution, and the integrated absorbance and fluorescence intensity were multiplied by 10.

** Experimental errors for each amino acid concentrations were approximately ±3 and for the total amino acid concentrations were approximately ±5 based on the previous triplicate experiments (Elmasry et al., 2021).

Note: There is another peak in the lower excitation region of the 3D-EEM fluorescence spectra of γ40 + Heat and γ80 + Heat samples.

All glassware used in this study was cleaned with Extran MA01 (Merck) and water (prepared with Direct-Q UV3, Merck Millipore), followed by baking at 500°C for 4 h in an oven. The regents used in this study are listed in Supplementary Table S1.

Reverse-phase High-Performance Liquid Chromatograph (HPLC) analysis for amino acids

Amino acid analyses were performed according to the method described by Elmasry et al. (2021). After the gamma-ray/heating experiments, a 100-μL aliquot of each solution was mixed with 100 μL of 12 M HCl (35% hydrochloric acid) for acid hydrolysis and heated at 110°C for 24 h (in 6 M HCl). After acid hydrolysis, the samples were dried using an evaporator (Smart Evaporator K4, BioChromato) at 60°C for 30 min. Each dried sample was dissolved in 3 mL of water and then filtered through a 0.2 μm membrane filter (Ekicrodisc 13CR PTFE, Nihon Pall Ltd.) before analysis by an ultra-high-performance liquid chromatograph (UHPLC, Nexera X2, Shimadzu) system. A reversed-phase column (Inertsil ODS-4, 3 μm HP, 3.0 mm × 100 mm, Cat. No. 5020-14004, GL Science) was used to separate the amino acids. The UHPLC system was equipped with a system controller (CBM-20A), two solvent delivery units (LC-30AD), a degasser (DGU-20A_5R), a mixer (MR180μL II), an autosampler (SIL-30AC), a column oven (CTO-20AC), a fluorescence detector (RF-20Axs), and a workstation (LabSolutions LC/GC). A 1-μL aliquot of each sample solution was injected to the column maintained at 35°C. Chromatography was performed by gradient elution with mobile phases of (A) an aqueous solution of 15 mmol/L potassium dihydrogen phosphate and 5 mmol/L dipotassium hydrogen phosphate (a mixture of 2.04 g of potassium dihydrogen phosphate (136.09 g/mol), 0.87 g dipotassium hydrogen phosphate (174.18 g/mol), and 1000 mL of water), and (B) water : acetonitrile : methanol = 15:45:40 (v/v/v) at a flow rate of 0.8 mL/min. Fluorescence detection was performed using excitation at 350 nm and emission at 450 nm. Pre-column derivatization with o-phthalaldehyde/3-mercaptopropionic acid (OPA/MPA) and 9-fluorenylmethyl chloroformate (FMOC-Cl) was used. The derivatization reagents used were a borate buffer solution of MPA (a mixture of MPA 10 μL and 0.1 M borate buffer 10 mL), a borate buffer solution of OPA (a mixture of OPA 10 mg, ethanol 0.3 mL, 0.1 M borate buffer 0.7 mL, and water 4 mL), an acetonitrile solution of FMOC-Cl (a mixture of FMOC-Cl 10 mg and acetonitrile 25 mL), and 0.1 M potassium phosphate buffer (a mixture of 85% phosphoric acid 0.34 mL, potassium dihydrogen phosphate 0.68 g, and water 100 mL). 0.1 M borate buffer was prepared using boric acid 0.62 g, sodium hydroxide 0.20 g, and water 100 mL. Commercially available amino acid standard solutions (Amino Acid Mixed Standard Solution AN type and B type, FUJIFILM Wako Pure Chemical) were diluted to 25 μM and used for the quantitative analysis of glycine (Gly), alanine (Ala), and β-alanine (β-Ala). Other amino acids in the standard were too low to quantify. There were also some peaks in the chromatograms that could not be identified.

UV-Vis spectroscopy

Ultraviolet-visible (UV-Vis) spectroscopy was performed as described by Elmasry et al. (2020), which represents the changes in electronic energy levels within the molecule arising due to the transfer of electrons from π- or nonbonding orbitals, providing information on π electron systems, conjugated unsaturation, aromatic compounds, and conjugated nonbonding electron systems. A 100-μL aliquot of each solution after the gamma-ray/heating experiments was diluted with 3 mL water in a 10-mm quartz cell and then analyzed using a UV-Vis spectrometer (V-660, JASCO). Absorption spectra were obtained in the wavelength range of 200–900 nm using a deuterium lamp (187–350 nm) and a halogen lamp (350–900 nm), with single accumulation. The optical system was double-beam, one for the sample and the other for the reference (water). Some sample solutions (γ40 + Heat and γ80 + Heat) were further diluted 10 times to avoid spectral saturation and thus the absorbance was multiplied by 10 for comparison. Integrated absorbance was calculated in the range of 240–500 nm.

3D fluorescence spectroscopy

3D fluorescence spectroscopy was performed as described by Elmasry et al. (2020). Briefly, a 100-μL aliquot of each solution after the gamma-ray/heating experiments was diluted with 3 mL water in a 10-mm quartz cell and then analyzed using a spectrofluorometer (FP-6300, JASCO), equipped with a Xe light source. Some sample solutions (γ40 + Heat and γ80 + Heat) were further diluted 10 times to avoid spectral saturation and thus the intensities were multiplied by 10 for comparison. The three-dimensional excitation-emission matrix (3D-EEM) of the sample solutions was determined in an excitation range of 220–690 nm and an emission range of 230–750 nm. The EEM was then corrected for internal shielding effects using UV-Vis absorption spectra with the following equation:

I_c(λ_ex, λ_em) = I₀(λ_ex, λ_em) ∙ 10^[A(λ_ex) + A(λ_em)]/2

where I_c(λ_ex, λ_em) is the corrected fluorescence intensity, I₀(λ_ex, λ_em) is the observed fluorescence intensity, A(λ_ex) is the absorbance at the excitation (ex.) wavelength, and A(λ_em) is the absorbance at the emission (em.) wavelength (Lakowicz, 2006). The EEM before correction is shown in Supplementary Figure S1.

Results

Amino acids

Figure 1 shows chromatograms of the amino acid standard mixture and samples after the gamma-ray/heating experiments. The amino acids were identified on the basis of retention times using standards. The yields of amino acids (Gly, Ala, and β-Ala) after the gamma-ray/heating experiments are shown in Fig. 2 and Table 1, but the possibility of the formation of other amino acids cannot be excluded. The total amino acid concentrations (Gly, Ala, and β-Ala) increased in the order of Control ~ Heat < γ40/80 < Heat + γ40/80 < γ40/80 + Heat ~ γ168/336/504 < γ1143. β-Ala was dominant in all of the samples, followed by Gly and Ala. Interestingly, γ40/80 + Heat produced amino acids more efficiently than Heat + γ40/80 and γ40/80.

Fig. 1.

HPLC chromatograms of the acid-hydrolyzed products after the gamma-ray/heating experiments. Note that the chromatograms of samples were shifted 0.15 min earlier than the standard within ±0.5 min, probably due to the high ionic strength of the samples, which reduces the retention time.

Fig. 2.

Yields of amino acids from the acid-hydrolyzed products after the gamma-ray/heating experiments.

UV-Vis spectra and 3D-EEM

In UV-Vis spectra, if there is a conjugated double bond in an organic compound, the larger the conjugated system, the more the peak wavelength shifts to the longer wavelength side. Functional groups affect the conjugated system, shifting the absorption peak to the longer wavelength side, but not into the visible region above 400 nm. Therefore, the size of the conjugated system has a greater effect on the color of organic compounds than functional groups. Figures 3 and 4 show the color changes and UV-Vis spectra, respectively, of the samples after gamma-ray/heating experiments. The longer the sample was exposed to gamma rays, the more visibly yellow it became (Fig. 3). The absorption wavelength gradually increased even at longer wavelengths, which might be due to the extension of the conjugated system (Fig. 4). γ40/80 + Heat samples were colored brown to red, but Heat + γ40/80 samples did not change color significantly as well as Heat sample (Fig. 3). The integrated absorbance in the range of 240–500 nm increased in the order of Heat < γ40 ~ Heat + γ40/80 < γ80/168/336/504/1143 < γ40/80 + Heat (Fig. 5a). This trend was similar to the maximum absorbance (Abs_max) (>260 nm) (Table 1). In contrast, the peak wavelength (λ_max) increased in the order of γ40/80/168 < Heat < γ40/80 + Heat < γ336/504 < Heat + γ40/80 (Table 1). The increases in λ_max values indicate the development of conjugated structures from shorter to longer in the reaction products.

Fig. 3.

Color changes of the products after the gamma-ray/heating experiments. (a) Control, (b) 100°C 3 d, (c) 2.6 kGy/h × 40 h, (d) 2.6 kGy/h × 80 h, (e) 2.6 kGy/h × 168 h, (f) 2.6 kGy/h × 336 h, (g) 2.6 kGy/h × 504 h, (h) 2.6 kGy/h × 1143 h, (i) 100°C 3d + 2.6 kGy/h × 40 h, (j) 100°C 3d + 2.6 kGy/h × 80 h, (k) 2.6 kGy/h × 40 h + 100°C 3d, and (l) 2.6 kGy/h × 80 h + 100°C 3d.

Fig. 4.

UV-Vis spectra of the products after the gamma-ray/heating experiments. γ40/80 + Heat samples were saturated (shown as dashed curves) and therefore analyzed after ten-time dilution and the absorbance is shown in ×10 (shown as solid curves). The shaded area indicates the region affected by water absorption.

Fig. 5.

(a) Integrated absorbance in the range of 240 nm to 500 nm from the UV-Vis spectra of the products after the gamma-ray/heating experiments. (b) Fluorescence intensity (absorbance-corrected) at ex./em. max from three-dimensional excitation-emission matrix (3D-EEM) of the products after the gamma-ray/heating experiments. γ40/80 + Heat samples were analyzed after ten-time dilution and the values are in ×10.

3D fluorescence spectroscopy is a technique for observing the emission of light (fluorescence) when a substance absorbs light in the UV and visible regions and excites, and then deactivates from the excited state to the ground state. The wavelength of the light used to excite the molecule and the wavelength of the light emitted as fluorescence are specific to each molecule. Figure 6 shows 3D-EEM (absorbance corrected) of the samples after gamma-ray/heating experiments, and Fig. 7 shows fluorescence spectra at ex. 340 nm obtained from the EEM. Fluorescence analysis showed that fluorescent material was produced in most of the samples. The γ40/80 + Heat samples showed bimodal peaks (Fig. 6k, l), indicating that more complex organic matter was formed. The fluorescence intensity at the maximum (Fig. 5b) increased with increasing total dose in the case of γ40–1143 samples, and overall increased in the order of Heat < γ40 < γ80 ~ Heat + γ40 < Heat + γ80 < γ168/336 ~ γ40/80 + Heat < γ504/1143, which was a similar trend to the UV-Vis absorbance intensity.

Fig. 6.

Three-dimensional excitation-emission matrix (3D-EEM) (absorbance-corrected) of the products after the gamma-ray/heating experiments. (a) Control, (b) 100°C 3 d, (c) 2.6 kGy/h × 40 h, (d) 2.6 kGy/h × 80 h, (e) 2.6 kGy/h × 168 h, (f) 2.6 kGy/h × 336 h, (g) 2.6 kGy/h × 504 h, (h) 2.6 kGy/h × 1143 h, (i) 100°C 3d + 2.6 kGy/h × 40 h, (j) 100°C 3d + 2.6 kGy/h × 80 h, (k) 2.6 kGy/h × 40 h + 100°C 3d, and (l) 2.6 kGy/h × 80 h + 100°C 3d. γ40/80 + Heat samples were analyzed after ten-time dilution and the intensities are shown in ×10.

Fig. 7.

Fluorescence spectra (absorbance corrected) at ex. 340 nm.

Discussion

Maillard reaction

The formation of amino acids from ammonia and aldehydes is well known from various experiments simulating aqueous alteration in meteorite parent bodies (Elmasry et al., 2021; Ishikawa et al., 2024; Kebukawa et al., 2017, 2022; Koga and Naraoka, 2017, 2022; Vinogradoff et al., 2020b), besides Strecker reaction from aldehyde and ketone with NH₃ and HCN (Peltzer and Bada, 1978). Koga and Naraoka (2017) proposed reactions of amino acid formation, starting with the production of formic acid from formaldehyde by the Cannizzaro reaction, which is then converted to formamide by reaction with ammonia, followed by the production of the carbomyl anion, which reacts with formaldehyde and acetaldehyde to produce glycine and alanine, respectively after hydrolysis. Later, Koga and Naraoka (2022) also proposed the reaction from the oxidation of glycolaldehyde to glyoxylic acid, which reacts with ammonia to produce N-oxalylglycine, and after hydrolysis to produce glycine. Vinogradoff et al. (2020b) also proposed the formation of amino acids from formaldehyde and ammonia, in addition, Maillard reaction led the reaction diversity and produced more diverse amino acids including β-alanine. On the other hand, the formation of amino acids by gamma rays was led by different mechanisms from hydrothermal reactions, and including radical reactions (Ishikawa et al., 2024; Kebukawa et al., 2022), particularly the formation of glycolaldehyde by gamma rays (López-Islas et al., 2019) is the key to produce amino acids by gamma rays from ammonia and formaldehyde.

We observed significant color changes in our samples, and thus we discuss such color changes based on the Maillard reaction. The Maillard reaction is the reaction of sugars and amino acids to produce brown substances called melanoidin. The Maillard reaction starts with the carbonyl-amino reactions of aldehydes, ketones, and reducing sugars with amines and amino acids, leading to the formation of brown pigments known as melanoidins. The initial stage of the Maillard reaction involves the N-substituted glycosylamine, followed by the Amadori rearrangement of glycosylamines to form an Amadori compound (Hodge, 1953). The Amadori compound then undergoes further complex reactions, leading to the formation of various brown pigments (Hodge, 1953).

UV-visible analysis revealed the formation of colored organic matter by gamma irradiation (Fig. 4), and in particular, a brownish color was evident in the products after gamma irradiation followed by heating (Fig. 3k, l). Such color changes were similar to the Maillard reaction products of 0.1 M glycine and 0.1 M ribose solutions heated at 80°C for 0–168 h (Nakaya et al., 2018b). Since aldose sugars were produced in gamma irradiation experiments of aqueous solutions of formaldehyde and methanol with/without ammonia via formose-type reaction (Abe et al., 2024), compounds with sugar carbonyl groups were likely formed and used for the Maillard reaction in our experiments. The Maillard reaction products from glycine and ribose showed an increase in 280 nm absorption (Nakaya et al., 2018b), and such an increase was also observed in our products, but with some variation in the peak wavelength (λ_max) (Table 1). The trend of increasing λ_max values was different from the trend of increasing peak intensity (Abs_max) and integrated absorbance, and the products involving heating showed relatively higher λ_max values. This indicates the development of conjugated structures was more effective by heating than gamma rays, probably because gamma rays primarily break chemical bonds to produce radicals, and thus heating is more efficient for producing complex molecules through condensation reactions.

Fluorescent products are known to be developed through the Maillard reaction along with the brown pigments, and fluorescent products have been proposed as indicators of the early process of this reaction (Matiacevich and Pilar Buera, 2006). The EEM of typical Maillard reaction products have a maximum of excitation (ex. max) at 340–370 nm, and a maximum emission (em. max) at 420–450 nm (Matiacevich and Pilar Buera, 2006), and was similar range to our products involving heating. Nakaya et al. (2018a) reported ex. max of 345 nm and em. max of 430 nm of the products from 0.1 M glycine and 0.1 M ribose solutions heated at 80°C for 0–168 h, which is consistent with our product after heating (100°C for 72 h). However, the products involving gamma irradiation showed slightly lower ex. max and ex. min, indicating that gamma rays may induce somewhat different reactions.

Overall, the yields of amino acids showed positive correlations with coloration (UV-Vis intensity) and fluorescence intensity—both indicating the progress of the Maillard-type reactions (Fig. 8). This correlation indicates that amino acid precursors are produced as the Maillard reaction proceeds. However, the Maillard-type reactions probably proceeded at most in the solutions after gamma irradiation followed by heating (γ40/80 + Heat), but the gamma-irradiated products (γ168–1143) were superior in the formation of amino acids, suggesting that gamma rays efficiently produce amino acid precursors (Fig. 8a). These differences suggest that some progress of Maillard-type reactions produce molecules containing amino acid structures and the released free amino acids after acid hydrolysis, but further proceed of the reaction may not maintain amino acid structures in the products. It should be noted that gamma irradiation followed by heating (γ40/80 + Heat) efficiently produces amino acids, and the Maillard-type reactions proceed compared to the products by heating followed by gamma irradiation (Heat + γ40/80). This is likely due to the initial formation of glycolaldehyde (C₂H₄O₂) by gamma rays (López-Islas et al., 2019). Subsequently, glycine can be produced from glycolaldehyde by the addition of ammonia, and β-alanine can be produced from glyceraldehyde (C₃H₆O₃) by the addition of ammonia (Vinogradoff et al., 2020b), in the simplest case. Simultaneously, sugars would be produced by formose reaction, which further react with amino acids to produce macromolecular pigments (Maillard reaction). The products likely contain amino acid precursors that release amino acids after acid hydrolysis.

Fig. 8.

Comparison of amino acid concentrations (total of Gly, Ala, and β-ala) with (a) integrated absorbance (240–500 nm), and (b) corrected fluorescence intensity (ex./em. max). Experimental errors for the total amino acid concentrations were approximately ±5 based on the previous triplicate experiments (Elmasry et al., 2021) and are within the markers.

Aqueous alteration in parent bodies of carbonaceous chondrites

The β-alanine/glycine ratio is known to increase with increasing degree of aqueous alteration (Glavin et al., 2006; Martins et al., 2015). In our experiments, Heat + γ40/80 and γ40/80 + Heat samples have higher β-alanine/glycine ratios than gamma irradiated samples (γ80 to γ1143), except for γ40, and the Heat sample has the highest β-alanine/glycine ratio (Fig. 9, Table 1). Similar trends were observed for alanine/glycine ratios, indicating that heating is the key to the production of β-alanine and alanine. Compared to carbonaceous chondrites, the alanine/glycine ratios in most of our experimental products were similar to those of highly aqueously altered chondrites such as CI1, CM1, and CM2.0 (Fig. 9). In contrast, our experimental products had higher β-alanine/glycine ratios than carbonaceous chondrites, but the ratios of γ80 to γ1143 samples were similar to those of Type 1 carbonaceous chondrites (Orgueil, CI1 and SCO 06043, CM1).

Fig. 9.

A comparison of the relative molar amino acid abundances in meteorites. Meteorite data from *Glavin et al. (2011); **Glavin et al. (2006); ***Martins et al. (2015).

In the actual parent bodies of chondrites, the gamma-ray dose was highest at the time of accretion, then gradually decreased, followed by increasing temperature due to decay of radioactive nuclides—75% of the gamma-ray energy from ²⁶Al was consumed in the first ~1.5 × 10⁶ y (twice the half-life), whereas the temperature reaches the peak in a few million years (Fujiya et al., 2012). Such conditions—first gamma rays followed by heating—are likely favorable for amino acid formation in the parent bodies.

Conclusions

The purpose of this study is to investigate the combined effects of heating and gamma rays in the simulated environments of hydrated meteorite parent bodies, as well as to elucidate the reaction mechanisms. In the experiments, we sequentially applied heating and gamma irradiation to simple starting materials containing ammonia, formaldehyde, methanol, and water to produce amino acid precursors. For comparison, experiments involving only heating and only gamma irradiation were also conducted.

Comparing the total amino acid yields after acid hydrolysis, the products after gamma irradiation followed by heating (γ40/80 + Heat) were higher than those after heating followed by gamma irradiation (Heat + γ40/80), gamma irradiation only (γ40/80), and heating only (Heat). Based on UV-visible absorption and fluorescence spectroscopy, Maillard-type reactions proceeded most effectively in samples irradiated with gamma rays followed by heating. However, higher dose gamma irradiated products (γ168/336/504/1143) showed higher yields of amino acids but less progress of Maillard-type reactions. These results indicate that the conditions with first gamma rays followed by heating are the best for amino acid production, and the heating efficiently proceeds the Maillard-type reactions, but gamma rays efficiently proceed the formation of amino acid precursors.

Acknowledgments

We thank two anonymous reviewers for helpful comments and suggestions for improving the manuscript. This work was supported by Japan Society for the Promotion of Science KAKENHI (grant numbers JP20H02014, JP21K18648, JP21H00036, JP23H01286, JP23K03561, and JP23K17700) and the Astrobiology Center of National Institutes of Natural Sciences (NINS) (Grant Numbers AB0501 and AB0605).

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