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Abiotic synthesis of amino acids in the recesses of the oceanic lithosphere

Nature volume 564, pages 59–63 (2018)Cite this article

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Abstract

Abiotic hydrocarbons and carboxylic acids are known to be formed on Earth, notably during the hydrothermal alteration of mantle rocks. Although the abiotic formation of amino acids has been predicted both from experimental studies and thermodynamic calculations, its occurrence has not been demonstrated in terrestrial settings. Here, using a multimodal approach that combines high-resolution imaging techniques, we obtain evidence for the occurrence of aromatic amino acids formed abiotically and subsequently preserved at depth beneath the Atlantis Massif (Mid-Atlantic Ridge). These aromatic amino acids may have been formed through Friedel–Crafts reactions catalysed by an iron-rich saponite clay during a late alteration stage of the massif serpentinites. Demonstrating the potential of fluid-rock interactions in the oceanic lithosphere to generate amino acids abiotically gives credence to the hydrothermal theory for the origin of life, and may shed light on ancient metabolisms and the functioning of the present-day deep biosphere.

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Fig. 1: Endogenous UV-autofluorescence locally revealed by S-DUV imaging of a highly altered mantle-rock recovered at 173.15 m below sea floor from IODP Expedition 304 Hole U1309D.
Fig. 2: The presence of tryptophan in the Fe-rich saponite was confirmed by TOF-SIMS imaging with the co-localized collection of its characteristic fragment ions.
Fig. 3: Fe-rich saponite as a catalysing pillared-clay for the abiotic synthesis of tryptophan.

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Data availability

The data supporting the findings of this study are available within the paper, its Extended Data and its Supplementary Information. The datasets generated and analysed in this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank B. Van de Moortèle for the FIB sections, O. Boudouma for assistance during SEM experiments and V. Pasini, D. Brunelli, M. Chaussidon and J. Badro for help and discussion. We acknowledge the IODP program (https://www.iodp.org/) and SOLEIL synchrotron for granted access to DISCO and SMIS beamlines. This research was supported by the Deep Carbon Observatory, the deepOASES ANR project (ANR-14-CE01-0008) and the French CNRS (Défi Origines M.I. 2018). This is IPGP contribution no. 3976.

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Nature thanks J. Baross, M. Russell and the anonymous reviewer(s) for their contribution to the peer review of this work.

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Authors and Affiliations

  1. Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, CNRS, Paris, France

    Bénédicte Ménez & Céline Pisapia

  2. Synchrotron SOLEIL, Gif-sur-Yvette, France

    Céline Pisapia, Frédéric Jamme, Paul Dumas & Matthieu Réfrégiers

  3. Laboratoire de Géologie de Lyon: Terre, Planètes, Environnement, UMR5276, ENS-Université Lyon I, Villeurbanne, France

    Muriel Andreani

  4. Institut de Chimie des Substances Naturelles, CNRS UPR2301, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France

    Quentin P. Vanbellingen & Alain Brunelle

  5. Nazarbayev University, School of Mining & Geosciences, Astana, Kazakhstan

    Laurent Richard

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  1. Bénédicte Ménez
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Contributions

B.M., C.P. and M.A. conceived the research. B.M., C.P., F.J., M.R., Q.P.V., A.B., M.A. and P.D. performed the experiments. L.R. performed the thermodynamic calculations. B.M. wrote the manuscript. All authors contributed to the interpretation of the data and commented on the manuscript.

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Correspondence to Bénédicte Ménez.

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Extended data figures and tables

Extended Data Fig. 1 Large optical views of the deeply serpentinized harzburgite recovered by drilling the Atlantis Massif (173.15 m below sea floor) during the IODP Expedition 304 at Hole U1309D12.

a, b, Both photomicrographs are centred on the two areas described in the present study (in Figs. 1–3, Extended Data Figs. 2–5 for a and Extended Data Figs. 6, 7 for b, respectively). The high-temperature hydrated paragenesis is composed of serpentine and magnetite, both after olivine (Ol), and forming a characteristic mesh texture. Yellow to brownish phases are frequently found in the core of the mesh serpentine. They correspond to Fe-rich serpentine and Fe-rich saponite, formed at lower temperature during secondary and tertiary alteration reactions that occur at the expense of the mesh serpentine and olivine kernels15, some remnants of which can still be observed. Hole figures an olivine crystal removed during sample thinning and polishing. Green arrows indicate sample orientation.

Extended Data Fig. 2 SEM images of the Fe-rich saponite enriched in organic carbon.

a, b, SEM-BSE images collected at 15 kV on the mineral assemblage displayed in Figs. 1, 2 and Extended Data Fig. 1a. b, Magnified view of the area represented by the green box in a. The green arrow indicates sample orientation; the orange dashed line and the associated arrow denote the location and front face, respectively, of the FIB foil milled for TEM observations (Fig. 3a, b, Extended Data Fig. 4). Textures and differences in grey levels resulting from chemical contrasts allow the recognition of each mineral phase previously characterized by S-FTIR and electron microprobe analysis, namely mesh serpentine, Fe-rich serpentine and Fe-rich saponite. c, SEM-SE image collected at 3 kV accelerating voltage (location shown by an asterisk in a), in which the characteristic platelets of saponite14 are well recognizable. Fe-rich saponite presents distinct grey levels in a and b that relate to its variable content in organic carbon, hence darkening its aspect when carbon is abundant. The image in panel a was adapted from ref. 15, Springer Nature Limited.

Extended Data Fig. 3 S-FTIR confirmed the presence of N-bearing organic compounds in the Fe-rich saponite.

a, S-FTIR distribution maps of the aliphatic CH2/CH3 stretching band area between 2,800 and 3,000 cm−1 shown in c and collected in the area indicated by the blue box in Fig. 1a. b, c, Associated S-FTIR spectra. The spectrum collected in the C-rich saponite (Extended Data Fig. 2a, b) shows the presence of organic compounds with modes at (1) 1,270 cm−1 and 1,285 cm−1, (2) 1,380 cm−1, (3) 1,412 cm−1, (4) 1,460–1,465 cm−1, (5) 1,550–1,650 cm−1, and 1,728 cm−1 in b, and 2,855, 2,871, 2,924 and 2,958 cm−1 in c. Band assignments are compiled in Supplementary Table 3. Contributions of the H–O–H bending from the saponite interlayer water at 1,627 cm−1 may interfere15. Also shown are the S-FTIR spectra collected in the mesh serpentine and the Fe-rich serpentine, both being nearly depleted in absorption bands related to organic compounds. They show instead characteristic O–H stretching bands at 3,570 and 3,610 cm−1 and M–O–H bending modes (with M indicating any of the cations in the hydrated silicate structure) in the range 1,500–1,680 cm−1. Dotted brown curves correspond to a mixture of saponite and serpentine. Precise locations of analysis are indicated in a with the corresponding coloured dots. FTIR spectra of protein26 and l-tryptophan (https://webbook.nist.gov/cgi/cbook.cgi?ID=C73223&Mask=80) are shown for comparison. ‘o’ denotes overtone-combination bands; ‘ν’ denotes stretching; ‘νas’ and ‘νs’ denote asymmetric and symmetric stretching, respectively.

Extended Data Fig. 4 SEM image sequence illustrating FIB milling, which allowed cross-sectional visualization of the interfaces between the C-bearing Fe-rich saponite, the Fe-rich serpentine, the mesh serpentine and the associated textures.

a, SEM-SESI view at low magnification of the UV-fluorescent area depicted in Fig. 1 and Extended Data Fig. 5. The white arrow denotes the region where an ultrathin foil was milled for TEM observations (Fig. 3a, b). The green arrow provides the orientation of the sample. b, Enlarged SEM-SESI view of the region of interest coated with a carbon protective layer. The orange arrow denotes the milling direction. c, SEM-BSE image showing the front face of the milled section. d, e, Enlarged SEM-InLens views of the Fe-rich saponite displaying a nanoporous texture with maximum pore size of less than 100 nm, in contrast to the compact Fe-rich serpentine hosted in the mesh serpentine. Pores of the Fe-rich saponite are large enough to support the presence of a 1.2-nm-sized molecule such as tryptophan66 (see also Fig. 3a, b for associated TEM observations). f, Associated EDS spectra collected at 5 kV accelerating voltage.

Extended Data Fig. 5 S-DUV spectral signature of the endogenous fluorescence revealed in the Fe-rich saponite.

a, Full-field S-DUV image displayed in Fig. 1 and collected using an excitation wavelength (λexc) of 275 nm, and a detection range of fluorescence emission between 400 and 440 nm. b, Fluorescence emission spectra collected with excitation wavelength of 275 nm summed from the hyperspectral datacube acquired in the area indicated by the orange box in a (30 s per point, 2-µm step). Fit of the S-DUV hyperspectral maps, performed using Gaussian functions and 10 iterations, resolved 4 main contributions at 340 ± 6, 358 ± 3, 380 ± 3 and 403 ± 3 nm (mean ± s.d. of three independent measurements). c, Associated spatial distributions of fluorescence emissions at 340, 358, 380 and 403 nm. They revealed systematic co-localization of these four components. The green arrows indicate sample orientation.

Extended Data Fig. 6 Systematic association of Fe-rich saponite with tryptophan.

a, Optical view of an olivine kernel in the mesh serpentine, as shown in Extended Data Fig. 1b. b, c, SEM-BSE images collected at 15 kV in the area indicated by the green box in a. The image in panel b was modified from ref. 15, Springer Nature Limited. The orange dashed line and associated arrow in b, respectively, provide the location and front face of the FIB foil (Extended Data Fig. 7) milled for the TEM observations displayed in d. c, Magnified view of the area represented by the green box in b. Textures and chemical contrasts allow the recognition of each mineral phase previously characterized by S-FTIR and electron microprobe analysis, namely magnetite, olivine, mesh serpentine, Fe-rich serpentine and Fe-rich saponite. d, TEM image that shows the Fe-rich saponite layers appear perpendicular to the interface between the olivine kernel and the mesh serpentine, with lizardite crystallites appearing in black. The Fe-rich saponite lamellae are mainly subparallel although some sheet distortions are visible. e, Associated S-DUV full-field fluorescence images collected after excitation (λexc) at 275 nm in the range 327–353, 370–410 and 412–438 nm. For all of these wavelengths, the UV autofluorescence emission is shown at the interface between the olivine crystal and serpentine where the Fe-rich saponite is located. f, TOF-SIMS ion image collected in the 500 × 500 µm2 area displayed in a, and showing the distribution of the characteristic fragment ions of tryptophan22 (Supplementary Table 2), hence confirming its presence close to the olivine kernel. Evidence for the absence of common biomarkers23,24,25 can be found in the detailed spectra provided in Extended Data Fig. 8o–v. The green arrows provide sample orientation.

Extended Data Fig. 7 SEM image sequence that illustrates FIB milling, which allowed cross-sectional visualization of the interfaces between the UV-fluorescent Fe-rich saponite, the olivine kernel and the mesh serpentine.

a, SEM-SESI view at low magnification of the UV-fluorescent area shown in Extended Data Fig. 6. The white arrow denotes the region of interest, where an ultrathin foil was milled for TEM observations (Extended Data Fig. 6d). The green arrow indicates the orientation of the sample. b, SEM-SESI view of the region of interest coated with a carbon-protective layer. The orange arrow designates the milling direction. c, SEM-SESI image showing the FIB milled trench at the leading edge of the region of interest. d, SEM-BSE image showing the front face of the milled section. Similarly to Extended Data Fig. 4, it revealed marked textural contrasts between the mineral phases, the Fe-rich saponite presenting the highest porosity.

Extended Data Fig. 8 Enlarged views of the positive TOF-SIMS spectra collected in the Fe-rich saponite.

a–n, Enlarged views of the positive TOF-SIMS spectrum from Fig. 2d reconstructed from the region displaying the highest count rate in Fig. 2b. i–n, Selected magnified views of this TOF-SIMS spectrum showing regions in which the peaks of fragment ions characteristic of isoprenoids such as pristane (C19H40), squalane (C30H50) and lycopane (C40H56) along with polycyclic compounds (cholestane, C27H48; β-carotane, C40H56 and hopanoids) should be found if present23,24,25. These biomarkers were previously detected using gas chromatography in the bulk rock13 but are not detected locally in our mineral assemblage. o–v, Enlarged views of the positive TOF-SIMS spectra reconstructed from the region displaying the highest count rate in Extended Data Fig. 6f. a–c and o–q exhibit peaks of fragments ions characteristic of siloxane, a common plasticizer contaminant. No notable peaks can be found in the 350–450 m/z regions (d, e, r and s), in which the aliphatic fraction (including fragment ions from the sterane and hopane classes and from alkanes and monocyclic alkanes) is expressed in positive TOF-SIMS spectra23,24,25.

Extended Data Fig. 9 Chemical affinity as a function of the logarithm of the activity of aqueous dihydrogen (H2(aq.)) for the reactions corresponding to the abiotic synthesis of pyruvate (C3H3O3-), indole (C8H7N), and tryptophan (C11H12N2O2).

The vertical lines indicate the range of H2 activities reported for the moderate-temperature fluids of the Lost City hydrothermal field38. See Supplementary Information.

Extended Data Fig. 10 Activity diagram of aqueous dihydrogen H2(aq.) depicting, as a function of pH, the fields of relative predominance of nitrogen species at 200 °C and 150 bar and considering a total nitrogen amount (∑N) of 6 × 10−6 M.

The limits between two predominance fields have been drawn for equal activities of the nitrogen species (that is, ammonium (NH4+), aqueous ammonia (NH3(aq.)) and aqueous dinitrogen (N2(aq.)). The blue star indicates conditions encountered at depth in the Atlantis Massif by considering a mean H2 activity of 10.5 mM38 and a pH of 7.12, calculated with tremolite-chrysotile-diopside as the alteration assemblage consistent with hydrothermal fluid composition37. The activity of water was assumed equal to 1. Diagram shows that NH3(aq.) is thermodynamically favoured at 200 °C. QFM, quartz-fayalite-magnetite mineral buffer.

Supplementary information

Supplementary Information

This file contains Supplementary Tables 1-5 and Supplementary References. The table legends are: Supplementary Table 1: Experimental and theoretical abiotic synthesis of amino acids at conditions of hydrothermal systems, Supplementary Table 2: List of TOF-SIMS fragment ions potentially characteristic of tryptophan, Supplementary Table 3: Assignment for the S-FTIR bands related to organic compounds identified in the UV fluorescent saponite, Supplementary Table 4: Electron microprobe analyses of the Fe-rich saponite and Supplementary Table 5: Fe-rich saponite formulas and associated Fe3+ content.

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Ménez, B., Pisapia, C., Andreani, M. et al. Abiotic synthesis of amino acids in the recesses of the oceanic lithosphere. Nature 564, 59–63 (2018). https://doi.org/10.1038/s41586-018-0684-z

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