Raman Imaging of Metastable Opal in Carbonaceous Microfossils of the 700

Abstract

Opaline silica was detected, with Raman spectroscopy, in carbonaceous microfossils (especially Myxococcoides) in silicified filamentous microbial mats within dolomitized conglomerates of the Draken Formation (−800 to −700 Ma). High-resolution electron microscopy (HRTEM) and microprobe analyses were used to confirm the nature of this phase in the quartz matrix of the microbial mats. The silica likely precipitated in a microcrystalline form onto the organic macromolecules around, and within, the degrading microorganisms and preserved them by inhibiting the natural phase change to quartz. The Raman signal of opaline silica associated with carbonaceous matter and other biosignatures could be a potential indicator of biogenicity. This kind of association could be very useful during the future ExoMars mission (ESA/Roscosmos, 2018) that will search for traces of past life on Mars. Key Words: Silica—Raman spectroscopic imagery—Microfossils—Biosignatures. Astrobiology 13, 57–67.

1. Introduction

T he last decade has seen an important increase in the use of non-invasive micron-scale chemical mapping of microbial biosignatures (Boyce et al., 2001; Lepot et al., 2008; Westall, 2008; Allwood et al., 2009). Recognizing that identification of potential traces of martian life with in situ techniques on Mars will be highly challenging (Hoehler and Westall, 2010; Westall et al., 2011a), we are particularly interested in morphological and chemical signatures detectable by microscopy and Raman spectroscopy that, along with other biosignatures, would aid in identification of past traces of life and, eventually, the selection of suitable materials for return to Earth (Mars Sample Return project, >2025). The main science objective of the proposed European and Russian 2018 mission to Mars, ExoMars, is the search for traces of past or present life (Brack et al., 1999; Westall et al., 2000). The instrument payload will include a drill for obtaining samples from depths of up to 2 m, a means of observing rock outcrops (PanCam) and rock/core surfaces (HR camera, microscope), and analytical instruments for analyzing mineralogy and organics (IR and Raman spectrometry, GC– and LD–mass spectrometry). We are particularly interested in the combination of Raman spectrometry (Marshall et al., 2010) and microscopy. For this, we have chosen for a pilot study the conglomerates of the 700–800 Ma old Draken Formation from Spitzbergen. These conglomerates contain well-documented and easily identifiable microfossils preserved in cherty lenses in the dolomitic conglomerate (Knoll, 1982, 1985; Swett and Knoll, 1985; Fairchild et al., 1991; Knoll et al., 1991). From a technological point of view, our laboratory Raman instrumentation is more accurate than that in development for the ExoMars payload (Rull Pérez and Martinez-Frias, 2006); it is a confocal system designed for 2-D and 3-D mapping that thus has a better spatial resolution and mechanical stability. Moreover, the optical observations were made in transmitted light on thin sections, thus facilitating the localization of the microfossils, whereas the ExoMars microscope will observe rough and cut rock surfaces in reflected light. However, the relevance of our study is the documentation of phases of substances such as carbonaceous matter, opal, or hydroxyapatite that are associated with the microfossils that could be detected by the in situ instrumentation in the ExoMars mission.

Deposits hypothesized to be silica, including opaline silica, have been identified on Mars. Based on the NASA Opportunity Mini-TES measurement in Meridiani Planum, McLennan et al. (2005) inferred the presence of secondary silica from geochemical mass balance equations. Glotch et al. (2006) used models to interpret the Mini-TES spectrum and also concluded that amorphous silica/glass may be present in Meridiani Planum outcrop. These identifications were also made by Squyres et al. (2008) and Tosca and Knoll (2009). Complementary data from CRISM (Compact Reconnaissance Imaging Spectrometer for Mars) (Milliken et al., 2008; Ehlmann et al., 2009) also suggest the presence of H₂O- and SiOH-bearing phases consistent with the presence of opaline silica on the martian surface. These occurrences have been attributed to fumarole alteration and leaching of volcanic lithologies, or possibly hot spring sinter deposits (Ruff et al., 2011). The hypothetical nature of these identifications is related to the fact that quartz is difficult to identify from orbit and, to date, there have been no in situ mineralogical identifications.

Silica was a common chemical deposit on the volcanically active early Earth, where the seawater was enriched in silica from altered and weathered volcanic crust and hydrothermal fluids. Silica was also responsible for the preservation of the oldest forms of terrestrial life known (Schopf and Walter, 1982; Walsh, 1992; Tice and Lowe, 2004; Westall et al., 2006a, 2006b). There are some similarities from a microbial point of view in the environmental conditions of early Earth and early Mars (Westall, 2005; Southam et al., 2007; Westall et al., 2011a), and the search for past life on Mars in the future 2018 mission will therefore be concentrated in the ancient Noachian terrains that date from the period when water was episodically stable on the surface of Mars and life could have existed (McKay, 1997) (the Noachian period covers much the same time frame as the terrestrial Early Archean period, 3.5–4.0 Ga). Moreover, early Mars was volcanically very active, and the volcanism, along with water (Manga et al., 2012), may have led to hydrothermal activity associated with silica-rich fluids, as was the case on early Earth. Silica could thus have been an important means of preservation by which potential biogenic signatures were preserved (Westall et al., 2011a).

In situ analyses of martian rocks that may contain traces of life will be made by miniaturized instrumentation with limited performance capabilities. The instrumentation may nevertheless be able to detect potential biosignatures in the rocks, for example, the association of kerogen with metastable mineral phases and/or other biominerals, that will aid in identification of traces of life. The combination of Raman spectrometry with microscopic analysis is particularly useful, as has been demonstrated by a number of studies of ancient microbial or potentially microbial biosignatures on Earth. Allwood et al. (2009) used this combination to study layers of carbonaceous matter that they interpreted as microbial mats formed from photosynthetic organisms. Foucher and Westall (2009), Foucher et al. (2010), and Westall et al. (2011a) used a combination of microscopy (optical and scanning and transmission electron microscopy) with confocal micro-Raman spectrometry and mapping for the study of ancient carbonaceous remains in sediments of an origin and an age similar to that of Noachian sediments. These authors documented the presence of silicified colonies of very small coccoidal microorganisms (of the order of 1 μm or less) on the surfaces of sedimented volcanic particles in the 3.5 Ga old Kitty's Gap chert, in the Pilbara. Schopf et al. (2002a, 2002b, 2007, 2010) documented a carbonaceous composition in bacteriomorph features, which may have had an abiogenic origin (Brasier et al., 2004; Pinti et al., 2009), associated with a hydrothermal chert vein in the 3.46 Ga old Apex chert from the Pilbara in Australia.

In the course of our investigation of the silicified microfossils in the Draken Formation, we became aware of an unusual opaline silica phase that was almost invariably associated with the microfossils. Further investigation also documented a rare association of hydroxyapatite with the microfossils. (Butterfield et al., 1994, identified apatite in another Neoproterozoic formation, Svanbergfjellet, from Spitsbergen). Association of opal with carbonaceous microfossils in the 1.9 Ga old Gunflint Formation was previously recorded by Moreau and Sharp (2004) with the use of transmission electron microscopy (TEM). The detection of this unstable mineral phase associated with organic material by Raman spectroscopy, in association with other biosignatures, could be very useful during the search for life on Mars, if it can be proven that the phenomenon is not abiogenic.

The objectives of our present investigation are to evaluate the utility of combined Raman spectroscopy and microscopy for detecting biosignatures, especially the association of a metastable mineral (opaline silica) and carbon, and the biomineral hydroxyapatite, which may be present on Mars. The main part of this article focuses on samples from the Draken formation (−800 Ma), but samples from the Gunflint formation (−1.9 Ga) and the Duck Creek formation (−1.8 Ga) were also used to examine the effect of metamorphism. A sample from the quarry of Mazerier (France) was used to study the influence of the biological origin on the presence of opaline silica. Apart from the identification of a new potential biosignature (to be used in conjunction with other biosignatures), our results provide additional information about the fossilization and early diagenetic processes involved in the preservation of the Draken Formation conglomerates.

2. Materials and Methods

The Draken Formation sediments from Spitzbergen were deposited in the lagoonal zone of a tropical sea in the Neoproterozoic era, 700–800 million years ago. The sediments now form a dolomitic conglomerate that includes silicified lenses that contain a rich microbial mat/planktonic microfossil assemblage (Knoll, 1982; Knoll et al., 1991, 1993). The sample studied was collected by A. Knoll. All the microfossils used for this study occur in the cherty lenses.

Complementary analyses were made on black cherts from the lower algal facies chert of the Paleoproterozoic Gunflint Formation (−1.9 Ga) in Canada and chert from the late Paleoproterozoic Duck Creek Formation (−1.8 Ga) in Western Australia. The sizes and shapes of Duck Creek microfossils are closely similar to those found in Gunflint chert, including filaments and coccoidal microfossils (Barghoorn and Tyler, 1965; Wilson et al., 2010). The Duck Creek Formation, however, underwent higher metamorphism ranging into prehnite-pumpellyite/pumpellyite-actinolite facies (Schopf, 1983). An unmetamorphosed chert containing abiotic carbon that occurs in an aplitic quartz-fluorite vein that intersects a porphyraceous granite in the quarry of Mazerier, Allier, France, was also analyzed to determine whether opaline silica could be detected in association with abiotic carbon.

Observations were made on 30 μm thick, polished thin sections. Optical microscopy (Olympus BX51, CBM, Orléans) was used to locate the microfossils exhibiting a wide range of morphologies in the cherty lenses. All the structures located at the surface of the thin sections were referenced in order to carry out complementary scanning electron microscopy (SEM) and TEM observations on exactly the same structures. The areas of interest were then analyzed by Raman spectral mapping with a WITec Alpha500 RA, at the CNRS-CBM, Orléans. Two- and three-dimensional compositional maps were made, the latter constructed by stacking several 2-D scans. The confocality of the system permitted a z resolution of <1.5 μm and a lateral resolution of <400 nm. The light source used was a frequency-doubled Nd:YAG green laser (wavelength λ=532 nm), which is similar to the light source to be used during the ExoMars mission. The laser power on the sample was limited to ∼5 mW to prevent any deterioration of the phases associated with the microfossil (the Raman spectra of opaline silica and carbonaceous matter were accumulated for more than 1 h on a fixed point, and no change in the parameters of the carbon peaks was observed with this power). SEM observations were made of both polished and etched surfaces (HF 5% for 20 min) with a FEG SEM, Hitachi S4200 of the Centre de Microscopie Électronique in Orléans. The individual structures of interest were first circled by using a diamond tip objective on the optical microscope in order to aid re-localization of the structures with the SEM. Energy-dispersive X-ray spectroscopy was used to identify the elemental composition, and quantitative analyses were made with an electron microprobe (Cameca SX 50, BRGM, Orléans). Finally, 1 μm thick slices were made within individual microfossils with a focused ion beam (FIB, FEI STRATA DB 235, IEMN, Lille) for the TEM/STEM observations. The latter were carried out with a Jeol 2010 TEM operating at 200 keV at the LRS of Jussieu, Paris, and with a FEI Tecnai F20 TEM/STEM operating at 200 keV at the CNR-IMN Institute of Bologna in Italy.

3. Results

3.1. Petrographic observations

The microfossil taxonomy of the Draken Formation was characterized by Knoll (1982), Swett and Knoll (1985), and Knoll et al. (1991). The cherty lenses consist of benthic microbial mats of the filamentous cyanobacterium Siphonophycus, approximately 5 μm in diameter and several tens of micrometers in length. Associated with the mats are the remains of spherical planktonic microorganisms (mainly Myxoccoides), whose cells range from 10 to 20 μm in size. These coccoidal fossils are randomly dispersed in the microbial mats and occur either as isolated cells or colonies.

Most of the microfossils are well preserved and occur as dark carbonaceous structures that have a single or double wall. Some examples have a degraded, lysed membrane and contain a ball of collapsed cytoplasm (cf. Westall et al., 1995). Pyrite crystals frequently occur inside or adjacent to the structures. Images of the observed microfossils are shown in Fig. 1.

FIG. 1.

Optical images and Raman maps of microfossils from the Draken formation [(a–e, g, h) Myxococcoides; (f) unidentified fossils; (j) exposed cross sections of the sheaths of the possible filamentous Synodophycus]. For each microfossil, from left to right: optical image, Raman kerogen, and opaline silica maps [(h) carbon and opaline silica maps in 3-D, 50×50 μm² over ∼30 μm in depth], and for (i) Raman hydroxyapatite map. Note the collapsed cytoplasm inside the examples in (a, b) and (e) (cf. Fig. 7). The stars in the optical image (a) correspond to the microprobe analyses [(1) 98.11% SiO₂+1.89% H₂O; (2) 98.78% SiO₂+1.22% H₂O].

3.2. Raman analyses

Two- and three-dimensional Raman compositional maps were made of more than 40 microfossil-containing areas. All the microfossils are characterized by spectral peaks typical of kerogen centered around 1340 cm⁻¹ (the D peak) and around 1600 cm⁻¹ (the G peak) that represent disordered and graphitic carbon, respectively (Tuinstra and Koenig, 1970; Jehlicka and Bény, 1999). Another broad peak located around 300 cm⁻¹ was also associated with most of the microfossils (Fig. 1). There is a distinct correlation between the kerogen and the phase producing the ∼300 cm⁻¹ peak. This correlation is especially visible in the thicker cell membranes and collapsed cytoplasm of the planktonic coccoidal microfossils but also occurs in the sheaths of the filamentous microorganisms that make up the microbial mats. With use of the RRUFF Raman database (http://rruff.info) and the literature (Ostrooumov et al., 1999), the closest fit for the 300 cm⁻¹ is that of opal CT, which presents a variety of peak positions, depending upon its microstructure and water content (Fig. 2). However, our spectrum lacks the peak at 800 cm⁻¹, which is typical for opal CT. Since no other silica peaks occur at this wavelength, we henceforth refer to this phase as “opaline silica.” Note that the spectra in Fig. 2 show a quartz “parasite” peak at 465 cm⁻¹ from the quartz matrix due to the fact that the interaction volume of the laser includes both quartz and opaline silica. The shift of the 300 cm⁻¹ peak to the lower wavenumbers with the increasing signal of quartz can be explained by the increase of the 205 and 264 cm⁻¹ peaks of quartz intensity. The Raman analyses also demonstrate the presence of pyrite and, very rarely, hydroxyapatite associated with some microfossils (Fig. 1i).

FIG. 2.

Microfossils from the Draken Formation and Raman spectra of various silica phases. (a, b) optical images of Myxococcoides microfossils and associated Raman maps of opal where single spectra were accumulated. (i–v) Raman spectra of various silica phases: (i) fused quartz (after Foucher et al., 2010), (ii) opal A from Australia and (iii) opal CT from Mexico (after Ostrooumov et al., 1999); (iv, v) opal from Draken Formation observed in two different microfossils [yellow stars in (a) and (b), respectively], the peak at 465 cm⁻¹ being associated with quartz in the matrix. Color images available online at www.liebertpub.com/ast

3.3. Scanning electron microscopy

The SEM images made on etched (HF) thin sections show distinct orientations in the silica grains, in particular in the membrane (Fig. 3). This change is in accordance with the presence of a finer crystalline silica phase in the carbonaceous remains of the microfossils than in the matrix.

FIG. 3.

Structure of silica phase in the cell wall of a Myxococcoides microfossil. (a) Optical image, (b) Raman carbon, (c) opaline silica maps, and (d, e) SEM images. (e) The detail of the cell wall outlined in (d) clearly shows the orientation of the silica crystals. Image sizes: (a, b) 30×30 μm². Scale bars: 10 μm in (d) and 1 μm in (e). Color images available online at www.liebertpub.com/ast

3.4. Electron microprobe analyses

The microfossils located at the surface were analyzed by electron microprobe. The quantitative analyses only showed the presence of SiO₂ and water. Water contents deduced by stoichiometry in the silica phase inside the fossil were 1.89% compared to 1.22% H₂O in the matrix (Fig. 1a).

3.5. Transmission electron microscopy

High-resolution transmission electron microscopy (HRTEM) observations were made on a FIB slice cutting through the membrane of one of the coccoidal microfossils. Figure 4c shows the Raman signature of opaline silica in the membrane and in the center of the microfossil. The cell wall that was analyzed by HRTEM is clearly visible in the FIB section taken across the wall (Fig. 4e). Figure 5 shows that the carbon in the cell wall is more or less well organized and that the microstructure of the silica associated with the organic matter is amorphous, as indicated by the halo in the diffraction pattern. Note that the energy of the electron beam that was used (200 keV) was not high enough to cause the amorphitization of the quartz (cf. Cady et al., 1996).

FIG. 4.

FIB section through a Myxococcoides microfossil. (a) Optical image, (b) Raman carbon, (c) opaline silica maps, and (d, e) SEM images. (e) The FIB cut through the microfossil (black rectangle in d), shows the profile of the microfossil. Image sizes: (a–d) 20×20 μm². Scale bars: 5 μm in (d) and (e). Color images available online at www.liebertpub.com/ast

FIG. 5.

TEM images of FIB slice made in a microfossil from the Draken Formation. The cytoplasm and the membrane of the cell are clearly observable (black arrows). The diffraction pattern associated with amorphous/opaline silica is shown in insert.

3.6. Complementary Raman investigation

As noted above, opaline silica has previously been observed by HRTEM in association with microfossils from the Gunflint formation (−1.9 Ga) by Moreau and Sharp (2004). We therefore made complementary analyses of Gunflint microfossils in order to find the Raman signature of opaline silica associated with these structures. As seen in Fig. 6, a subtle opaline silica signal, similar to the one observed in the Draken Formation, was detected, thus confirming its identification.

FIG. 6.

Gunflint microfossils in thin section. (a) Optical image, (b) Raman carbon, and (c) opaline silica maps. Image sizes: 40×40 μm². Color images available online at www.liebertpub.com/ast

4. Discussion

The identification of the metastable silica phase, opaline silica, in association with kerogen in a fossilized microbial structure was made by Raman spectroscopy. Comparison of the Raman spectral peaks with those from the literature and from the RRUFF Raman spectral database showed that the closest correspondence to the peaks documented in the Draken microfossils was opal CT (Fig. 2). There are no other silica mineral peaks at 300 cm⁻¹. However, since there was no corresponding peak at 800 cm⁻¹, we consider this phase to be more amorphous than opal CT and refer to it as opaline silica. Complementary techniques were used to confirm this identification: HRTEM and calculations of water content based on microprobe analyses. The HRTEM electron diffraction pattern documented a phase characterized by the diffuse halo of a noncrystalline material. Identification of opal by electron microbe is based on the stoichiometrically calculated water content. However, although the resulting ∼2% H₂O is consistent with opal, the variation in water concentration between the matrix and the microfossil is relatively low (less than 1%); thus, definitive identification of opal with this technique is not possible. Opal is a metastable phase of silica, and under normal conditions, it converts to the more stable quartz phase, as in the quartz matrix. Ghost opal CT lepispheres in the matrix are evidence of this recrystallization (Fairchild et al., 1991). The question is, why did the silica in the kerogen of the Draken microfossils remain in the metastable phase? The fact that this phase is always associated with the carbonaceous remains of the microfossils may provide a clue. For instance, the influence of organic matter on the preservation of metastable crystal phases has previously been invoked to explain the existence of metastable aragonite in kerogen associated with a 2.7 Ga old stromatolite in the Pilbara, Australia (Lepot et al., 2008), and in a 3.3 Ga old microbial biofilm from Barberton, South Africa (Westall et al., 2011b). Could the presence of organic matter have prevented growth and recrystallization of the opaline silica within the microfossils? If so, by what mechanism, and what is the implication regarding the timing of the silicification of the microfossils? Knoll (1985) suggested that permineralization of the microfossils occurred by fixation of silica to organic matter via hydrogen bonding. Hydrogen bonding between silicic acid and organic compounds occurs at a low pH<4, whereas cation bridging can take place at all pH values (Iler, 1979). It is possible that mixing of meteoric waters with the peritidal seawater in which the Draken Formation sediments formed could have provoked low pH conditions (cf. Hesse, 1989). Cation bridging as well as possible hydrogen bonding has been previously invoked to explain silicification of microorganisms in both experimental setups and in natural environments, such as hot springs (Urrutia and Beveridge, 1993; Westall et al., 1995; Konhauser et al., 2004; Orange et al., 2009, 2011). Westall et al. (1995) showed that, after initial fixation of the silica to the cell walls, death and lysis occurred, enabling the silica to penetrate into the interior of the cells. The degraded organic molecules remain trapped within the precipitated silica either in a diffuse manner or as a ball of collapsed cytoplasm, as in Fig. 7. The interaction of the silica and the carbon molecules can then have a direct influence on further growth of the silica phase, resulting in the preservation of a metastable phase by inhibiting recrystallization. The fact that we observed initial reorientation of the microcrystalline silica within the cell walls in a few microfossils, that is, silica that was in direct contact with the recrystallized matrix, demonstrates the strong influence of the organic molecules as inhibitors of silica recrystallization.

FIG. 7.

Comparison of distribution of degraded cytoplasm in both experimentally fossilized microorganisms and in the Draken microfossils. (a, e) TEM images of artificially silicified microorganisms (after Westall et al., 1995) and larger coccoidal structures observed in the cherty lens of the Draken Formation (b–d) and (f–h) respectively. In (a), the degraded cytoplasm forms a collapsed ball within the organisms, whereas in (e) it is diffuse. Color images available online at www.liebertpub.com/ast

The silicification of the microbial mats in the cherty lenses was a primary event, as indicated by the intimate relationship between the kerogen of the microfossils and their opaline silica infilling. Fairchild et al. (1991) noted that both silicification and dolomitization of the Draken conglomerate were syndepositional processes. Knoll (1985) proposed that the microbial mat fragments were deposited in the conglomerate as unsilicified flakes that were rapidly silicified. This is certainly the case for the roll-up fragments. Our observations suggest that silicification may have occurred as multiple episodes. Many of the cherty flakes are flat and show no evidence for overturning and little or no bending. Given that microbial mats, although cohesive, can be easily deformed plastically and that roll-up structures do occur in the conglomerate, it could be argued that, in the peritidal environment in which these mats formed, some of them must have been silicified and lithified before disaggregation and transport, whereas those that are bent must have been disaggregated before complete polymerization and crystallization of the silica. In situ silicification of the mats is a feasible scenario, since the Neoproterozoic seawater would have been saturated with silica and, furthermore, silica could have been further concentrated by evaporation in the tropical shallow waters in which the Draken Formation was deposited. However, further silicification after the formation of the conglomerate appears to have occurred, for example, where secondary silicification at the edges of the already partially silicified mats caused bending of the filamentous laminae (Fig. 8) or in the case of the roll-up mats (Knoll, 1982).

FIG. 8.

Multiple phases of silicification of the microbial mat chert flakes in the Draken Formation. (a, b) Optical images in transmitted and polarized light, respectively, of a silicified flake of the filamentous mat exhibiting gentle deformation of the laminae. The secondary silicification at the edges of the already partially silicified mat has caused bending of the filamentous laminae (arrow). Scale bar 200 μm. Color images available online at www.liebertpub.com/ast

As noted above, opal is a metastable phase of silica that naturally recrystallizes to quartz with time. However, the detection of opal in the Draken and Gunflint samples thus demonstrates its possible preservation over long periods of geological time. The microorganisms of the Duck Creek Formation are similar to those observed in the Gunflint Formation and have been fossilized in the same conditions and by the same processes (Wilson et al., 2010). It can thus be hypothesized that, during silicification, the silica precipitated onto the microorganisms in the form of opal. However, as shown in Fig. 9, there is no opal signature in the Raman spectral map. The Duck Creek formation underwent slightly higher metamorphism, prehnite-pumpellyite facies, sufficient to convert opal into quartz. Indeed, Dralus et al. (2011) showed that opal is totally converted into quartz in only 600 h at 310°C and 2 kbar, that is, in the prehnite-pumpellyite facies pressure-temperature conditions after the glossary of the Rock Library of the Imperial College of London. The higher metamorphism of the Duck Creek Formation is also shown by the consequent higher maturity of the kerogen in the Raman spectrum in Fig. 9 (increase of the disorder peak intensity at 1350 cm⁻¹ with respect to the graphite peak intensity at 1600 cm⁻¹; Quirico et al., 2009).

FIG. 9.

Carbonaceous structures observed in (a–c) Duck Creek formation from Australia. (a) Optical image, (b, c) Raman maps of (b) 1350 cm⁻¹ carbon peak area and (c) 300 cm⁻¹ opal peak area. The signal of opal is not observed on the map. Image size: 60×50 μm². (d) Comparison of Raman spectra from the carbon-silica microbial remains from the Duck Creek Formation and from the carbon-opaline silica in the microfossils from the Draken and Gunflint Formations. (e) Detail of the spectral area showing the presence of the opal peak around 300 cm⁻¹ in the Draken and Gunflint samples and the lack of this peak in the Duck Creek cherts. Color images available online at www.liebertpub.com/ast

Can the association of opaline silica and carbonaceous matter be considered a biosignature? Coexisting silica and carbon have been observed in abiotic hydrothermal deposits (Holm and Charlou, 2001), but there is no record in the literature of opaline silica having been detected in such cases. However, the precipitation of opaline silica takes place by nucleation of the silica molecule to a functional group, such as hydroxyl or carboxyl groups of the organic materials; that is, the organic matter serves as a template for the nucleation of silica (Westall et al., 1995, and references within). Pure carbon, such as graphite, is thus not expected to favor the precipitation of silica. On the other hand, organic matter can form abiogenically by Fischer-Tropsch processes. This could be tested by using an unmetamorphosed chert containing abiotic carbon. Although rare on Earth, we obtained such a sample from the Mazerier quarry, Allier, in France, where this type of association has previously been described (Grollier et al., 1975; Buisson, 2011). Raman analyses of a thin section of this rock showed no opaline silica signature in association with the carbonaceous matter, as seen in Fig. 10. This observation supports the hypothesis that opaline silica associated with carbonaceous matter could be considered as a potential biosignature, in particular if associated with other biosignatures.

FIG. 10.

Carbonaceous structures observed in (a–c) sample from the Mazerier quarry, France. (a) Optical image, (b–d) Raman maps of (b) 1600 cm⁻¹ carbon peak area, (c) 300 cm⁻¹ opal peak area, and (d) 512 cm⁻¹ orthoclase peak area. The signal of opal is not observed on the map. The detrital crystal of orthoclase comes from the granite in which the chert vein occurs. Image size: 30×30 μm². (e) Comparison of Raman spectra from the carbon-silica structures from the Mazerier sample and from the carbon-opaline silica in the microfossils from the Draken Formation. (f) Detail of the spectral area showing the presence of the opal peak around 300 cm⁻¹ in the Draken samples and the lack of this peak in the Mazerier chert. Color images available online at www.liebertpub.com/ast

Finally, we conclude that the association of opaline silica and carbonaceous matter Raman signals could have useful applications in the search for biosignatures in martian materials. This is particularly applicable to the international ExoMars 2018 mission, which will have both a Raman spectrometer and a microscope in its payload.

5. Conclusions

The metastable phase, opaline silica, was documented as a Raman spectral peak centered around 300 cm⁻¹ in intimate association with carbonaceous microfossils in flaky lenses of silicified microbial mats in a conglomerate from the 700–800 Ma Draken Formation. Its nanoscale structure was corroborated by the SEM observations and by its transmission electron diffraction pattern. Stoichiometrical analysis of its elemental composition (up to 2% H₂O) is in accordance with opaline silica. The preservation of metastable opaline silica is probably due to the fact that it was directly fixed to the degrading organic matter within the microbial structure, while the silica in the matrix of the chert flakes was recrystallized to quartz. A rare example of the biomineral hydroxyapatite was also documented.

Raman spectral analysis can be a powerful tool for identifying mineral phases and carbonaceous matter at the micrometer scale. This instrument will be embarked on the international ExoMars mission. Identification of the metastable opaline silica (and possibly other metastable minerals) in association with carbonaceous matter and other biosignatures could be very helpful in the detection of past traces of life on Mars.

Footnotes

Acknowledgments

Thanks are expressed to J.N. Rouzaud for the TEM observations in the LRS, Jussieu, Paris, and B. Cavalazzi for the TEM observations in the CNR-IMN Institute of Bologna, in Italy. D. Troadec from the IEMN, Lille, France, made the FIB sections. Thanks to A. Knoll from the Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, for allowing us to use the Duck Creek chert. N. Bost is acknowledged for his useful comments and for the sample from Mazerier. We thank the reviewers whose comments helped us improve the manuscript.

Abbreviations

FIB, focused ion beam; HRTEM, high-resolution electron microscopy; SEM, scanning electron microscopy, scanning electron microscope; TEM, transmission electron microscopy, transmission electron microscope.

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Raman Imaging of Metastable Opal in Carbonaceous Microfossils of the 700–800 Ma Old Draken Formation

Abstract

1. Introduction

2. Materials and Methods

3. Results

3.1. Petrographic observations

3.2. Raman analyses

3.3. Scanning electron microscopy

3.4. Electron microprobe analyses

3.5. Transmission electron microscopy

3.6. Complementary Raman investigation

4. Discussion

5. Conclusions

Footnotes

Acknowledgments

Abbreviations

References