Pushing Raman spectroscopy over the edge: purported signatures of organic molecules in fossil animals are instrumental artefacts.

Raman baseline subtraction biosignatures edge filter ripples fossil biomolecules wavelet transform

Journal

BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851

Informations de publication

Date de publication:
04 2021
Historique:
revised: 22 12 2020
received: 09 11 2020
accepted: 12 01 2021
pubmed: 6 2 2021
medline: 24 9 2021
entrez: 5 2 2021
Statut: ppublish

Résumé

Widespread preservation of fossilized biomolecules in many fossil animals has recently been reported in six studies, based on Raman microspectroscopy. Here, we show that the putative Raman signatures of organic compounds in these fossils are actually instrumental artefacts resulting from intense background luminescence. Raman spectroscopy is based on the detection of photons scattered inelastically by matter upon its interaction with a laser beam. For many natural materials, this interaction also generates a luminescence signal that is often orders of magnitude more intense than the light produced by Raman scattering. Such luminescence, coupled with the transmission properties of the spectrometer, induced quasi-periodic ripples in the measured spectra that have been incorrectly interpreted as Raman signatures of organic molecules. Although several analytical strategies have been developed to overcome this common issue, Raman microspectroscopy as used in the studies questioned here cannot be used to identify fossil biomolecules.

Identifiants

pubmed: 33543495
doi: 10.1002/bies.202000295
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2000295

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021 Wiley Periodicals LLC.

Références

Javaux, E. J., Knoll, A. H., & Walter, M. (2003). Recognizing and interpreting the fossils of early eukaryotes. Orig. Life Evol. Biosph., 33(1), 75-94.
Briggs, D. E. G., & Summons, R. E. (2014). Ancient biomolecules: Their origins, fossilization, and role in revealing the history of life. Bioessays, 36(5), 482-490.
Vinther, J. (2015). A guide to the field of palaeo colour. Bioessays, 37(6), 643-656.
Loron, C. C., François, C., Rainbird, R. H., Turner, E. C., Borensztajn, S., & Javaux, E. J. (2019). Early fungi from the Proterozoic era in Arctic Canada. Nature, 570(7760), 232-235.
Boyce, C. K., Cody, G. D., Feser, M., Jacobsen, C., Knoll, A. H., & Wirick, S. (2002). Organic chemical differentiation within fossil plant cell walls detected with X-ray spectromicroscopy. Geology, 30(11), 1039-1042.
Boyce, C. K., Abrecht, M., Zhou, D., & Gilbert, P. U. P. A. (2010). X-ray photoelectron emission spectromicroscopic analysis of arborescent lycopsid cell wall composition and Carboniferous coal ball preservation. Int. J. Coal Geol., 83(2-3), 146-153.
Bernard, S., Benzerara, K., Beyssac, O., Menguy, N., Guyot, F., Brown, G. E., & Goffé, B. (2007). Exceptional preservation of fossil plant spores in high-pressure metamorphic rocks. Earth Planet. Sci. Lett., 262(1), 257-272.
Cody, G. D., Gupta, N. S., Briggs, D. E. G., Kilcoyne, A. L. D., Summons, R. E., Kenig, F., … Scott, A. C. (2011). Molecular signature of chitin-protein complex in Paleozoic arthropods. Geology, 39(3), 255-258.
Cosmidis, J., Benzerara, K., Gheerbrant, E., Esteve, I., Bouya, B., & Amaghzaz, M. (2013). Nanometer-scale characterization of exceptionally preserved bacterial fossils in Paleocene phosphorites from Ouled Abdoun (Morocco). Geobiology, 11(2), 139-153.
Cosmidis, J., Benzerara, K., Menguy, N., & Arning, E. (2013). Microscopy evidence of bacterial microfossils in phosphorite crusts of the Peruvian shelf: Implications for phosphogenesis mechanisms. Chem. Geol., 359, 10-22.
Ehrlich, H., Rigby, J. K., Botting, J. P., Tsurkan, M. V., Werner, C., Schwille, P., … Sivkov, V. N. (2013). Discovery of 505-million-year old chitin in the basal demosponge Vauxia gracilenta. Sci. Rep., 3(1), 1-6.
Wysokowski, M., Zatoń, M., Bazhenov, V. V., Behm, T., Ehrlich, A., Stelling, A. L., … Ehrlich, H. (2014). Identification of chitin in 200-million-year-old gastropod egg capsules. Paleobiology, 40(4), 529-540.
Alleon, J., Bernard, S., Le Guillou, C., Marin-Carbonne, J., Pont, S., Beyssac, O., … Robert, F. (2016). Molecular preservation of 1.88 Ga Gunflint organic microfossils as a function of temperature and mineralogy. Nat. Commun., 7, 11977. https://doi.org/10.1038/ncomms11977
Alleon, J., Bernard, S., Le Guillou, C., Beyssac, O., Sugitani, K., & Robert, F. (2018). Chemical nature of the 3.4 Ga Strelley Pool microfossils. Geochem. Perspect. Lett., 7, 37-42. https://doi.org/10.7185/geochemlet.1817
Wiemann, J., Yang, T.-R., & Norell, M. A. (2018). Dinosaur egg colour had a single evolutionary origin. Nature, 563(7732), 555-558.
Wiemann, J., Fabbri, M., Yang, T.-R., Stein, K., Sander, P. M., Norell, M. A., & Briggs, D. E. G. (2018). Fossilization transforms vertebrate hard tissue proteins into N-heterocyclic polymers. Nat. Commun., 9(1), 1-9.
Wiemann, J., Crawford, J. M., & Briggs, D. E. G. (2020). Phylogenetic and physiological signals in metazoan fossil biomolecules. Sci Adv., 6(28), eaba6883.
Fabbri, M., Wiemann, J., Manucci, F., & Briggs, D. E. G. (2020). Three-dimensional soft tissue preservation revealed in the skin of a non-avian dinosaur. Palaeontology, 63(2), 185-193.
McCoy, V. E., Wiemann, J., Lamsdell, J. C., Whalen, C. D., Lidgard, S., Mayer, P., … Briggs, D. E. G. (2020). Chemical signatures of soft tissues distinguish between vertebrates and invertebrates from the Carboniferous Mazon Creek Lagerstätte of Illinois. Geobiology, 18(5), 560-565.
Norell, M. A., Wiemann, J., Fabbri, M., Yu, C., Marsicano, C. A., Moore-Nall, A., … Zelenitsky, D. K. (2020). The first dinosaur egg was soft. Nature, 583, 406-410.
Pasteris, J. D., & Beyssac, O. (2020). Welcome to Raman spectroscopy: Successes, challenges, and pitfalls. Elements, 16(2), 87-92.
Pasteris, J. D., & Wopenka, B. (2003). Necessary, but not sufficient: Raman identification of disordered carbon as a signature of ancient life. Astrobiology, 3(4), 727-738.
Beyssac, O., & Lazzeri, M. (2012). Application of Raman spectroscopy to the study of graphitic carbons in the Earth Sciences. Applications of Raman spectroscopy to Earth sciences and cultural heritage. EMU Notes in Mineralogy, 12, 415-454.
Quirico, E., Montagnac, G., Rouzaud, J.-N., Bonal, L., Bourot-Denise, M., Duber, S., & Reynard, B. (2009). Precursor and metamorphic condition effects on Raman spectra of poorly ordered carbonaceous matter in chondrites and coals. Earth Planet. Sci. Lett., 287(1-2), 185-193.
Bernard, S., Horsfield, B., Schulz, H.-M., Schreiber, A., Wirth, R., Vu, T. T. A., … Sherwood, N. (2010). Multi-scale detection of organic and inorganic signatures provides insights into gas shale properties and evolution. Chem. Erde, 70, 119-133.
Alleon, J., Flannery, D. T., Ferralis, N., Williford, K. H., Zhang, Y., Schuessler, J. A., & Summons, R. E. (2019). Organo-mineral associations in chert of the 3.5 Ga Mount Ada Basalt raise questions about the origin of organic matter in Paleoarchean hydrothermally influenced sediments. Sci. Rep., 9, 1-13.
Beyssac, O. (2020). New trends in Raman spectroscopy: From high-resolution geochemistry to planetary exploration. Elements, 16(2), 117-122.
Pucéat, E., Reynard, B., & Lécuyer, C. (2004). Can crystallinity be used to determine the degree of chemical alteration of biogenic apatites? Chem. Geol., 205(1-2), 83-97.
Torrence, C., & Compo, G. P. (1998). A practical guide to wavelet analysis. Bull. Am. Meteorological Soc., 79(1), 61-78.
Debret, M., Bout-Roumazeilles, V., Grousset, F., Desmet, M., McManus, J. F., Massei, N., … Trentesaux, A. (2007). The origin of the 1500-year climate cycles in Holocene North-Atlantic records. Clim. Past, 3, 569-575.
Ehrentreich, F., & Sümmchen, L. (2001). Spike removal and denoising of Raman spectra by wavelet transform methods. Anal. Chem., 73(17), 4364-4373.
Hu, Y., Jiang, T., Shen, A., Li, W., Wang, X., & Hu, J. (2007). A background elimination method based on wavelet transform for Raman spectra. Chemometr. Intell. Lab. Syst., 85(1), 94-101.
Stankiewicz, B. A., Mastalerz, M., Hof, C. H. J., Bierstedt, A., Flannery, M. B., Briggs, D. E. G., & Evershed, R. P. (1998). Biodegradation of the chitin-protein complex in crustacean cuticle. Org. Geochem., 28(1-2), 67-76.
Casadio, F., Daher, C., & Bellot-Gurlet, L. (2017). Raman spectroscopy of cultural heritage materials: Overview of applications and new frontiers in instrumentation, sampling modalities, and data processing. In: R. Mazzeo (Ed.), Analytical Chemistry for Cultural Heritage. (pp. 161-211). Topics in Current Chemistry Collections. Springer.
Gueriau, P., Bernard, S., Farges, F., Mocuta, C., Dutheil, D. B., Adatte, T., … Charbonnier, S. (2020). Oxidative conditions can lead to exceptional preservation through phosphatization. Geology, 48, 1164-1168
Sanz-Arranz, A., Manrique-Martinez, J. A., Medina-Garcia, J., & Rull-Perez, F. (2017). Amorphous zinc borate as a simple standard for baseline correction in Raman spectra. J. Raman Spectrosc., 48(11), 1644-1653.
Quirico, E., Bonal, L., Montagnac, G., Beck, P., & Reynard, B. (2020). New insights into the structure and formation of coals, terrestrial and extraterrestrial kerogens from resonant UV Raman spectroscopy. Geochim. Cosmochim. Acta, 282, 156-176.
Jehlička, J., Edwards, H. G. M., & Vítek, P. (2009). Assessment of Raman spectroscopy as a tool for the non-destructive identification of organic minerals and biomolecules for Mars studies. Planet. Space Sci., 57(5-6), 606-613.
Gueriau, P., Rueff, J.-P., Bernard, S., Kaddissy, J. A., Goler, S., Sahle, C. J., … Bergmann, U. (2017). Noninvasive synchrotron-based X-ray Raman scattering discriminates carbonaceous compounds in ancient and historical materials. Anal. Chem., 89(20), 10819-10826.
Georgiou, R., Gueriau, P., Sahle, C. J., Bernard, S., Mirone, A., Garrouste, R., … Bertrand, L. (2019). Carbon speciation in organic fossils using 2D to 3D x-ray Raman multispectral imaging. Sci. Adv., 5(8), eaaw5019.
Alleon, J., & Summons, R. E. (2019). Organic geochemical approaches to understanding early life. Free Radic. Biol. Med., 140, 103-112.

Auteurs

Julien Alleon (J)

Institute of Earth Sciences, University of Lausanne, Géopolis, Lausanne, CH-1015, Switzerland.

Gilles Montagnac (G)

Université de Lyon, ENS de Lyon, Université Lyon 1, CNRS, LGL-TPE, Lyon, F-69007, France.

Bruno Reynard (B)

Université de Lyon, ENS de Lyon, Université Lyon 1, CNRS, LGL-TPE, Lyon, F-69007, France.

Thibault Brulé (T)

HORIBA France SAS, Palaiseau, 91120, France.

Mathieu Thoury (M)

Universitè Paris-Saclay, CNRS, ministère de la Culture, UVSQ, MNHN, Institut photonique d'analyse non-destructive européen des matériaux anciens, Saint-Aubin, 91192, France.

Pierre Gueriau (P)

Institute of Earth Sciences, University of Lausanne, Géopolis, Lausanne, CH-1015, Switzerland.

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