Research Article
No access
Published Online: 3 October 2022

Deep-UV Raman Spectroscopy of Carbonaceous Precambrian Microfossils: Insights into the Search for Past Life on Mars

Publication: Astrobiology
Volume 22, Issue Number 10


The current strategy for detecting evidence of ancient life on Mars—a primary goal of NASA's ongoing Mars 2020 mission—is based largely on knowledge of Precambrian life and of its preservation in Earth's early rock record. The fossil record of primitive microorganisms consists mainly of stromatolites and other microbially influenced sedimentary structures, which occasionally preserve microfossils or other geochemical traces of life. Raman spectroscopy is an invaluable tool for identifying such signs of life and is routinely performed on Precambrian microfossils to help establish their organic composition, degree of thermal maturity, and biogenicity. The Mars 2020 rover, Perseverance, is equipped with a deep-ultraviolet (UV) Raman spectrometer as part of the SHERLOC (Scanning Habitable Environments with Raman and Luminescence for Organics and Chemicals) instrument, which will be used in part to characterize the preservation of organic matter in the ancient sedimentary rocks of Jezero crater and therein search for possible biosignatures. To determine the deep-UV Raman spectra characteristic of ancient microbial fossils, this study analyzes individual microfossils from 14 Precambrian cherts using deep-UV (244 nm) Raman spectroscopy. Spectra obtained were measured and calibrated relative to a graphitic standard and categorized according to the morphology and depositional environment of the fossil analyzed and its Raman-indicated thermal maturity. All acquired spectra of the fossil kerogens include a considerably Raman-enhanced and prominent first-order Raman G-band (∼1600 cm−1), whereas its commonly associated D-band (∼1350 cm−1) is restricted to specimens of lower thermal maturity (below greenschist facies) that thus have the less altered biosignature indicative of relatively well-preserved organic matter. If comparably preserved, similar characteristics would be expected to be exhibited by microfossils or ancient organic matter in rock samples collected and cached on Mars in preparation for future sample return to Earth.

Get full access to this article

View all available purchase options and get full access to this article.


Abbey WJ, Bhartia R, Beegle LW, et al. (2017) Deep UV Raman spectroscopy for planetary exploration: the search for in situ organics. Icarus 290:201–214.
Alleon J, Bernard S, Le Guillou C, et al. (2016) Early entombment within silica minimizes the molecular degradation of microorganisms during advanced diagenesis. Chem Geol 437:98–108.
Allwood AC, Walter MR, and Marshall CP (2006) Raman spectroscopy reveals thermal palaeoenvironments of c. 3.5 billion-year-old organic matter. Vib Spectrosc 41:190–197.
Aoya M, Kouketsu Y, Endo S, et al. (2010) Extending the applicability of the Raman carbonaceous-material geothermometer using data from contact metamorphic rocks. J Metamorph Geol 28:895–914.
Arvidson RE, Ruff SW, Morris RV, et al. (2008) Spirit Mars rover mission to the Columbia Hills, Gusev Crater: mission overview and selected results from the Cumberland Ridge to Home Plate. J Geophys Res Planet 113:1–35.
Asher SA (1993) UV resonance Raman spectroscopy for analytical, physical, and biophysical chemistry. Anal Chem 65:201A–210A.
Asher SA, Ludwig M, and Johnson CR (1986) UV resonance Raman excitation profiles of the aromatic amino acids. J Am Chem Soc 108:3186–3197.
Barańska H, Łabudzińska A, and Terpiński J (1987) Laser Raman Spectrometry: Analytical Applications. Ellis Horwood Ltd., USA.
Barghoorn ES and Tyler SA (1965) Microorganisms from the Gunflint chert. Science 147:563–577.
Bartley JK (1996) Actualistic taphonomy of cyanobacteria; implications for the Precambrian fossil record. Palaios 11:571–586.
Baruah BP and Khare P (2007) Pyrolysis of high sulfur Indian coals. Energy Fuels 21:3346–3352.
Beegle LW, Bhartia R, DeFlores LP, et al. (2014a) SHERLOC: scanning Habitable Environments with Raman & Luminescence for Organics & Chemicals, an investigation for 2020. In AGU Fall Meeting Abstracts. Moscone Center, San Francisco, CA.
Beegle LW, Bhartia R, DeFlores L, et al. (2014b) SHERLOC: scanning habitable environments with Raman & luminescence for organics & chemicals. In 11th International GeoRaman Conference. Washington University in St. Louis, St. Louis, MO.
Beegle L, Bhartia R, White M, et al. (2015) SHERLOC: scanning Habitable Environments with Raman & Luminescence for Organics & Chemicals. In IEEE Aerospace Conference Proceedings. Yellowstone Conference Center, Big Sky, MT.
Benner SA, Devine KG, Matveeva LN, et al. (2000) The missing organic molecules on Mars. Proc Natl Acad Sci USA 97:2425–2430.
Beny-Bassez C and Rouzaud JN (1985) Characterization of carbonaceous materials by correlated electron and optical microscopy and Raman microspectroscopy. Scan Electron Microsc 1:119–132.
Beyssac O, Goffé B, Chopin C, et al. (2002) Raman spectra of carbonaceous material in metasediments: a new geothermometer. J Metamorph Geol 20:859–871.
Beyssac O, Brunet F, Petitet J, et al. (2003) Experimental study of the microtextural and structural transformations of carbonaceous materials under pressure and temperature. Eur J Mineral 15:937–951.
Bhartia R, Beegle LW, DeFlores L, et al. (2021) Perseverance's Scanning Habitable Environments with Raman and Luminescence for Organics and Chemicals (SHERLOC) investigation. Space Sci Rev 217:1–115.
Bishop JL (2018) Remote detection of phyllosilicates on Mars and implications for climate and habitability. In From Habitability to Life on Mars, edited by N.A. Cabrol and E.A. Grin, Elsevier, Amsterdam, pp 37–75.
Bower DM, Steele A, Fries MD, et al. (2013) Micro Raman spectroscopy of carbonaceous material in microfossils and meteorites: improving a method for life detection. Astrobiology 13:103–113.
Butterfield NJ (2015) Early evolution of the Eukaryota. Palaeontology 58:5–17.
Cady SL, Farmer JD, Grotzinger JP, et al. (2003) Morphological biosignatures and the search for life on Mars. Astrobiology 3:351–368.
Casiraghi C, Piazza F, Ferrari AC, et al. (2005) Bonding in hydrogenated diamond-like carbon by Raman spectroscopy. Diam Relat Mater 14: 1098–1102.
Cataldo F, Keheyan Y, and Baccaro S (2004) The effect of gamma-irradiation of anthracite coal and oil bitumen. J Radioanal Nucl Chem 262:443–450.
Chieu TC, Dresselhaus MS, and Endo M (1982) Raman studies of benzene-derived graphite fibers. Phys Rev B 26:5867–5877.
Court RW, Sephton MA, Parnell J, et al. (2006) The alteration of organic matter in response to ionising irradiation: chemical trends and implications for extraterrestrial sample analysis. Geochim Cosmochim Acta 70:1020–1039.
Court RW, Sephton MA, Parnell J, et al. (2007) Raman spectroscopy of irradiated organic matter. Geochim Cosmochim Acta 71:2547–2568.
Cronin JR, Pizzarello S, and Cruikshank DP (1988) Organic matter in carbonaceous chondrites, planetary satellites, asteroids and comets. In Meteorites and the Early Solar System, edited by J.F. Kerridge and M.S. Matthews, University of Arizona Press, Tuscon, pp 819–857.
Cuesta A, Dhamelincourt P, Laureyns J, et al. (1994) Raman microprobe studies on carbon materials. Carbon 32:1523–1532.
Czaja AD, Kudryavtsev AB, and Schopf JW (2006) New method for the microscopic, nondestructive acquisition of ultraviolet resonance Raman spectra from plant cell walls. Appl Spectrosc 60:352–355.
Czaja AD, Kudryavtsev AB, Cody GD, et al. (2009) Characterization of permineralized kerogen from an Eocene fossil fern. Org Geochem 40:353–364.
Czaja AD, Beukes NJ, and Osterhout JT (2016) Sulfur-oxidizing bacteria prior to the Great Oxidation Event from the 2.52 Ga Gamohaan Formation of South Africa. Geology 44:983–986.
Dartnell LR, Storrie-Lombardi MC, Mullineaux CW, et al. (2011) Degradation of cyanobacterial biosignatures by ionizing radiation. Astrobiology 11:997–1016.
Dartnell LR, Page K, Jorge-Villar SE, et al. (2012) Destruction of Raman biosignatures by ionizing radiation and the implications for life detection on Mars. Anal Bioanal Chem 403:131–144.
Delarue F, Rouzaud J-N, Derenne S, et al. (2016) The Raman-derived carbonization continuum: a tool to select the best preserved molecular structures in Archean kerogens. Astrobiology 16:407–417.
Delarue F, Robert F, Derenne S, et al. (2020) Out of rock: a new look at the morphological and geochemical preservation of microfossils from the 3.46 Gyr-old Strelley Pool Formation. Precambrian Res 336:105472.
Des Marais DJ (2010) Exploring Mars for evidence of habitable environments and life. Proc Am Philos Soc 154:402–421.
Durand B (1980) Kerogen: Insoluble Organic Matter from Sedimentary Rocks. Editions Technip, Paris, France.
Ehlmann BL and Edwards CS (2014) Mineralogy of the Martian surface. Annu Rev Earth Planet Sci 42:291–315.
Ehlmann BL, Mustard JF, Fassett CI, et al. (2008a) Clay minerals in delta deposits and organic preservation potential on Mars. Nat Geosci 1:355–358.
Ehlmann BL, Mustard JF, Murchie SL, et al. (2008b) Orbital identification of carbonate-bearing rocks on Mars. Science 322:1828–1832.
Eichmann SL, Jacobi D, Haque MH, et al. (2018) Non-destructive investigations of thermal maturity and mechanical properties of source rocks. J Pet Geol 41:421–446.
Eigenbrode JL, Summons RE, Steele A, et al. (2018) Organic matter preserved in 3-billion-year-old mudstones at Gale crater, Mars. Science 360:1096–1101.
Escribano R, Sloan JJ, Siddique N, et al. (2001) Raman spectroscopy of carbon-containing particles. Vib Spectrosc 26:179–186.
Eshelman E, Daly MG, Slater G, et al. (2014) An ultraviolet Raman wavelength for the in-situ analysis of organic compounds relevant to astrobiology. Planet Space Sci 93:65–70.
Farmer JD and Des Marais DJ (1999) Exploring for a record of ancient Martian life. J Geophys Res Planet 104:26977–26995.
Ferralis N, Matys ED, Knoll AH, et al. (2016) Rapid, direct and non-destructive assessment of fossil organic matter via microRaman spectroscopy. Carbon 108:440–449.
Ferrari AC and Robertson J (2000) Interpretation of Raman spectra of disordered and amorphous carbon. Phys Rev B 61:95–107.
Ferrari AC and Robertson J (2001) Resonant Raman spectroscopy of disordered, amorphous, and diamondlike carbon. Phys Rev B Condens Matter Mater Phys 64:1–13.
Ferrari AC and Robertson J (2004) Raman spectroscopy of amorphous, nanostructured, diamond-like carbon, and nanodiamond. Philos Trans R Soc Lond A 362:2477–2512.
Flannery DT, Allwood AC, Summons RE, et al. (2018) Spatially-resolved isotopic study of carbon trapped in ∼3.43 Ga Strelley Pool Formation stromatolites. Geochim Cosmochim Acta 223:21–35.
Foucher F, Ammar MR, and Westall F (2015) Revealing the biotic origin of silicified Precambrian carbonaceous microstructures using Raman spectroscopic mapping, a potential method for the detection of microfossils on Mars. J Raman Spectrosc 46:873–879.
Fralick P, Davis DW, and Kissin SA (2002) The age of the Gunflint Formation, Ontario, Canada: single zircon U-Pb age determinations from reworked volcanic ash. Can J Earth Sci 39:1085–1091.
Gaft M and Panczer G (2013) Laser-induced time-resolved luminescence spectroscopy of minerals: a powerful tool for studying the nature of emission centres. Mineral Petrol 107:363–372.
Gaft M, Panczer G, Reisfeld R, et al. (2001) Laser-induced time-resolved luminescence as a tool for rare-earth element identification in minerals. Phys Chem Miner 28:347–363.
Goudge TA, Milliken RE, Head JW, et al. (2017) Sedimentological evidence for a deltaic origin of the western fan deposit in Jezero crater, Mars and implications for future exploration. Earth Planet Sci Lett 458:357–365.
Grady MM, Verchovsky AB, and Wright IP (2004) Magmatic carbon in Martian meteorites: attempts to constrain the carbon cycle on Mars. Int J Astrobiol 3:117–124.
Grant JA, Golombek MP, Wilson SA, et al. (2018) The science process for selecting the landing site for the 2020 Mars rover. Planet Space Sci 164:106–126.
Grotzinger JP and Milliken RE (2012) The sedimentary rock record of Mars: distribution, origins, and global stratigraphy. Sediment Geol Mars 102:1–48.
Grotzinger JP, Sumner DY, Kah LC, et al. (2014) A habitable fluvio-lacustrine environment at Yellowknife Bay, Gale crater, Mars. Science 343:1242777.
Guo H, Du Y, Kah LC, et al. (2013) Isotopic composition of organic and inorganic carbon from the Mesoproterozoic Jixian Group, North China: implications for biological and oceanic evolution. Precambrian Res 224:169–183.
Guo Z, Peng X, Czaja AD, et al. (2018) Cellular taphonomy of well-preserved Gaoyuzhuang microfossils: a window into the preservation of ancient cyanobacteria. Precambrian Res 304:88–98.
Hays LE, Graham HV, Des Marais DJ, et al. (2017) Biosignature preservation and detection in Mars analog environments. Astrobiology 17:363–400.
Henry DG, Jarvis I, Gillmore G, et al. (2019) Raman spectroscopy as a tool to determine the thermal maturity of organic matter: application to sedimentary, metamorphic and structural geology. Earth Sci Rev 198:102936.
Holland HD (1984) The Chemical Evolution of the Atmosphere and Oceans. Princeton University Press, Princeton, NJ.
Horgan BH, Anderson RB, Dromart G, et al. (2020) The mineral diversity of Jezero crater: evidence for possible lacustrine carbonates on Mars. Icarus 339:113526.
Husson JM, Schoene B, Bluher S, et al. (2016) Chemostratigraphic and U–Pb geochronologic constraints on carbon cycling across the Silurian–Devonian boundary. Earth Planet Sci Lett 436:108–120.
Javaux EJ (2007) The early eukaryotic fossil record. Adv Exp Med Biol 607:1–19.
Jawhari T, Roid A, and Casado J (1995) Raman spectroscopic characterization of some commercially available carbon black materials. Carbon 33:1561–1565.
Jubb AM, Botterell PJ, Birdwell JE, et al. (2018) High microscale variability in Raman thermal maturity estimates from shale organic matter. Int J Coal Geol 199:1–9.
Kanavarioti A and Mancinelli RL (1990) Could organic matter have been preserved on Mars for 3.5 billion years?. Icarus 84:196–202.
Kelemen SR and Fang HL (2001) Maturity trends in Raman spectra from kerogen and coal. Energy Fuels 15:653–658.
Knoll AH (2012) The fossil record of microbial life. In Fundamentals of Geobiology, edited by A.H. Knoll, D.E. Canfield, and K.O. Konhauser, Wiley-Blackwell, Hoboken, NJ, pp 297–314.
Knoll AH, Javaux EJ, Hewitt D, et al. (2006) Eukaryotic organisms in Proterozoic oceans. Philos Trans R Soc Lond B Biol Sci 361:1023–1038.
Kouketsu Y, Mizukami T, Mori H, et al. (2014) A new approach to develop the Raman carbonaceous material geothermometer for low-grade metamorphism using peak width. Isl Arc 23:33–50.
Kremer B, Kazmierczak J, Łukomska-Kowalczyk M, et al. (2012) Calcification and silicification: fossilization potential of cyanobacteria from stromatolites of Niuafo‘ou's Caldera Lakes (Tonga) and implications for the early fossil record. Astrobiology 12:535–548.
Kudryavtsev AB, Schopf JW, Agresti DG, et al. (2001) In situ laser-Raman imagery of precambrian microscopic fossils. Proc Natl Acad Sci USA 98:823–826.
Lamb DM, Awramik SM, Chapman DJ, et al. (2009) Evidence for eukaryotic diversification in the ∼1800 million-year-old Changzhougou Formation, North China. Precambrian Res 173:93–104.
Love GD, Snape CE, Carr AD, et al. (1995) Release of covalently-bound alkane biomarkers in high yields from kerogen via catalytic hydropyrolysis. Org Geochem 23:981–986.
Love GD, Stalvies C, Grosjean E, et al. (2008) Analysis of molecular biomarkers covalently bound within Neoproterozoic sedimentary kerogen. Paleontol Soc Pap 14:67–83.
Mangold N, Dromart G, Ansan V, et al. (2020) Fluvial regimes, morphometry, and age of Jezero crater paleolake inlet valleys and their exobiological significance for the 2020 Rover Mission Landing Site. Astrobiology 20:994–1013.
Manning-Berg A, Wood R, Williford K, et al. (2019) The taphonomy of Proterozoic microbial mats and implications for early diagenetic silicification. Geosciences 9:1–31.
Mapelli C, Castiglioni C, Zerbi G, et al. (1999) Common force field for graphite and polycyclic aromatic hydrocarbons. Phys Rev B 60:12710–12725.
Marshall CP, Love GD, Snape CE, et al. (2007) Structural characterization of kerogen in 3.4 Ga Archaean cherts from the Pilbara Craton, Western Australia. Precambrian Res 155:1–23.
Marshall CP, Edwards HGM, and Jehlicka J (2010) Understanding the application of Raman spectroscopy to the detection of traces of life. Astrobiology 10:229–243.
Matthews MJ, Pimenta MA, Dresselhaus G, et al. (1999) Origin of dispersive effects of the Raman D-band in disordered carbon materials. Phys Rev B 59:R6585.
McKeegan KD, Kudryavtsev AB, and Schopf JW (2007) Raman and ion microscopic imagery of graphitic inclusions in apatite from older than 3830 Ma Akilia supracrustal rocks, west Greenland. Geology 35:591–594.
McKirdy DM and Hahn JH (1982) The composition of kerogen and hydrocarbons in Precambrian rocks. In Mineral Deposits and the Evolution of the Biosphere, edited by H.D. Holland and M. Schidlowski, Springer, Dordrecht, the Netherlands, pp 123–154.
McMahon S, Bosak T, Grotzinger JP, et al. (2018) A field guide to finding fossils on Mars. J Geophys Res Planet 123:1012–1040.
Mustard JF, Murchie SL, Pelkey SM, et al. (2008) Hydrated silicate minerals on Mars observed by the Mars Reconnaissance Orbiter CRISM instrument. Nature 454:305–309.
Mustard J, Adler M, Allwood A, et al. (2013) Report of the Mars 2020 Science Definition Team. In Mars Exploration Program Analysis Group (MEPAG). NASA Jet Propulsion Laboratory, Pasadena, CA, pp 155–205.
Nakamura Y, Hara H, and Kagi H (2019) Natural and experimental structural evolution of dispersed organic matter in mudstones: the Shimano accretionary complex, southwest Japan. Island Arc 28:E12318.
Nemanich RJ and Solin SA (1979) First- and second-order Raman scattering from finite-size crystals of graphite. Phys Rev B 20:392–401.
Oehler JH (1976) Experimental studies in Precambrian paleontology: structural and chemical changes in blue-green algae during simulated fossilization in synthetic chert. Bull Geol Soc Am 87:117–129.
Oehler D and Cady S (2014) Biogenicity and syngeneity of organic matter in ancient sedimentary rocks: recent advances in the search for evidence of past life. Challenges 5:260–283.
Oehler JH and Schopf JW (1971) Artificial microfossils: experimental studies of permineralization of blue-green algae in silica. Science 174:1229–1231.
Osterhout JT, Czaja AD, Bartley JK, et al. (2019) Preservation of carbon isotopes in kerogen from thermally altered Mesoproterozoic lacustrine microbialites. Can J Earth Sci 56:1017–1026.
Pasteris JD and Wopenka B (1991) Raman spectra of graphite as indicates of degree of metamorphism. Can Mineral 29:1–9.
Pasteris JD and Wopenka B (2003) Necessary, but not sufficient: Raman identification of disordered carbon as a signature of ancient life. Astrobiology 3:727–738.
Pavlov AA, Vasilyev G, Ostryakov VM, et al. (2012) Degradation of the organic molecules in the shallow subsurface of Mars due to irradiation by cosmic rays. Geophys Res Lett 39:1–5.
Pehr K, Bisquera R, Bishop AN, et al. (2021) Preservation and distributions of covalently bound polyaromatic hydrocarbons in ancient biogenic kerogens and insoluble organic macromolecules. Astrobiology 21:1049–1075.
Perry EC and Lefticariu L (2013) Formation and geochemistry of Precambrian cherts. In Treatise on Geochemistry, 2nd ed., edited by H.D. Holland and K.K. Turekian, Vol. 9, Elsevier, Amsterdam, pp 113–139.
Pizzarello S and Shock E (2010) The organic composition of carbonaceous meteorites: the evolutionary story ahead of biochemistry. Cold Spring Harb Perspect Biol 2:1–19.
Preiss WV (2000) The Adelaide Geosyncline of South Australia and its significance in Neoproterozoic continental reconstruction. Precambrian Res 100:21–63.
Quirico E, Rouzaud JN, Bonal L, et al. (2005) Maturation grade of coals as revealed by Raman spectroscopy: progress and problems. Spectrochim Acta A Mol Biomol Spectrosc 61:2368–2377.
Rahl JM, Anderson KM, Brandon MT, et al. (2005) Raman spectroscopic carbonaceous material thermometry of low-grade metamorphic rocks: calibration and application to tectonic exhumation in Crete, Greece. Earth Planet Sci Lett 240:339–354.
Razzell Hollis J, Rheingold D, Bhartia R, et al. (2020) An optical model for quantitative Raman microspectroscopy. Appl Spectrosc 74:684–700.
Razzell Hollis J, Abbey W, Beegle LW, et al. (2021a) A deep-ultraviolet Raman and Fluorescence spectral library of 62 minerals for the SHERLOC instrument onboard Mars 2020. Planet Space Sci 209:105356.
Razzell Hollis J, Ireland S, Abbey W, et al. (2021b) Deep-ultraviolet Raman spectra of Mars-relevant evaporite minerals under 248.6 nm excitation. Icarus 357:114067.
Robertson J (1986) Amorphous carbon. Adv Phys 35:317–374.
Ruff SW, Farmer JD, Calvin WM, et al. (2011) Characteristics, distribution, origin, and significance of opaline silica observed by the Spirit rover in Gusev crater, Mars. J Geophys Res Planet 116:1–48.
Ruff SW, Campbell KA, Van Kranendonk MJ, et al. (2020) The case for ancient hot springs in Gusev crater, Mars. Astrobiology 20:475–499.
Sapers HM, Razzell Hollis J, Bhartia R, et al. (2019) The cell and the sum of its parts: patterns of complexity in biosignatures as revealed by deep UV Raman spectroscopy. Front Microbiol 10:679.
Sato K, Saito R, Oyama Y, et al. (2006) D-band Raman intensity of graphitic materials as a function of laser energy and crystallite size. Chem Phys Lett 427:117–121.
Schidlowski M (2001) Carbon isotopes as biogeochemical recorders of life over 3.8 Ga of Earth history: evolution of a concept. Precambrian Res 106:117–134.
Schito A, Romano C, Corrado S, et al. (2017) Diagenetic thermal evolution of organic matter by Raman spectroscopy. Org Geochem 106:57–67.
Schopf JW (1968) Microflora of the Bitter Springs Formation, Late Precambrian, Central Australia. J Paleontol 42:651–688.
Schopf JW (2006) Fossil evidence of Archaean life. Philos Trans R Soc Lond B Biol Sci 361:869–885.
Schopf JW and Kudryavtsev AB (2005) Three-dimensional Raman imagery of precambrian microscopic organisms. Geobiology 3:1–12.
Schopf JW and Kudryavtsev AB (2009) Confocal laser scanning microscopy and Raman imagery of ancient microscopic fossils. Precambrian Res 173:39–49.
Schopf JW, Kudryavtsev AB, Agresti DG, et al. (2002) Laser-Raman imagery of Earth's earliest fossils. Nature 416:73–76.
Schopf JW, Kudryavtsev AB, Agresti DG, et al. (2005) Raman imagery: a new approach to assess the geochemical maturity and biogenicity of permineralized Precambrian fossils. Astrobiology 5:333–371.
Schopf JW, Farmer JD, Foster IS, et al. (2012) Gypsum-permineralized microfossils and their relevance to the search for life on Mars. Astrobiology 12:619–633.
Schopf JW, Kudryavtsev AB, Osterhout JT, et al. (2017) An anaerobic ∼3400 Ma shallow-water microbial consortium: Presumptive evidence of Earth's Paleoarchean anoxic atmosphere. Precambrian Res 299:309–318.
Sergeev VN (2009) The distribution of microfossil assemblages in Proterozoic rocks. Precambrian Res 173:212–222.
Sergeev VN, Schopf JW, and Kudryavtsev AB (2020) Global microfossil changes through the Precambrian-Cambrian phosphogenic event: the Shabakta Formation of the phosphorite-bearing Maly Karatau Range, South Kazakhstan. Precambrian Res 349:105386.
Shkolyar S, Eshelman EJ, Farmer JD, et al. (2018) Detecting kerogen as a biosignature using colocated UV time-gated Raman and fluorescence spectroscopy. Astrobiology 18:431–453.
Sinninghe Damsté JS, Eglinton TI, De Leeuw JW, et al. (1989) Organic sulphur in macromolecular sedimentary organic matter: I. Structure and origin of sulphur-containing moieties in kerogen, asphaltene and coal as revealed by flash pyrolysis. Geochim Cosmochim Acta 53:873–889.
Song JJ, Chung DDL, Eklund PC, et al. (1976) Raman scattering in graphite intercalation compounds. Solid State Commun 20:1111–1115.
Steele A, McCubbin FM, and Fries MD (2016) The provenance, formation, and implications of reduced carbon phases in Martian meteorites. Meteorit Planet Sci 51:2203–2225.
Steele A, Benning LG, Wirth R, et al. (2022) Organic synthesis associated with serpentinization and carbonation on early Mars. Science 375:172–177.
Stoker CR, Zent A, Catling DC, et al. (2010) Habitability of the Phoenix landing site. J Geophys Res Planet 115:1–24.
Strauss H and Moore TB (1992) Abundances and isotopic compositions of carbon and sulfur species in whole rock and kerogen samples. In The Proterozoic Biosphere: A Multidisciplinary Study, edited by J.W. Schopf and C. Klein, Cambridge University Press, Cambridge, pp 709–798.
Sugitani K, Grey K, Allwood A, et al. (2007) Diverse microstructures from Archaean chert from the Mount Goldsworthy-Mount Grant area, Pilbara Craton, Western Australia: microfossils, dubiofossils, or pseudofossils?. Precambrian Res 158:228–262.
Summons RE, Amend JP, Bish D, et al. (2011) Preservation of Martian organic and environmental records: final report of the Mars biosignature working group. Astrobiology 11:157–181.
Sumner DY and Bowring SA (1996) U-Pb geochronologic constraints on deposition of the Campbellrand Subgroup, Transvaal Supergroup, South Africa. Precambrian Res 79:25–35.
Tarcea N, Harz M, Rösch P, et al. (2007) UV Raman spectroscopy—a technique for biological and mineralogical in situ planetary studies. Spectrochim Acta A Mol Biomol Spectrosc 68:1029–1035.
Tarnas JD, Mustard JF, Lin H, et al. (2019) Orbital identification of hydrated silica in Jezero crater, Mars. Geophys Res Lett 46:12771–12782.
Tuinstra F and Koenig JL (1970) Raman spectrum of graphite. J Chem Phys 53:1126–1130.
Uckert K, Bhartia R, Beegle LW, et al. (2021) Calibration of the SHERLOC deep ultraviolet fluorescence–Raman spectrometer on the perseverance Rover. Appl Spectrosc 75:763–773.
Vandenbroucke M and Largeau C (2007) Kerogen origin, evolution and structure. Org Geochem 38:719–833.
Vidano RP, Fischbach DB, Willis LJ, et al. (1981) Observation of Raman band shifting with excitation wavelength for carbons and graphites. Solid State Commun 39:341–344.
Vrazo MB, Diefendorf AF, Crowley BE, et al. (2018) Late Cretaceous marine arthropods relied on terrestrial organic matter as a food source: geochemical evidence from the Coon Creek Lagerstätte in the Mississippi Embayment. Geobiology 16:160–178.
Wada H and Suzuki K (1983) Carbon isotopic thermometry calibrated by dolomite-calcite solvus temperatures. Geochim Cosmochim Acta 47:697–706.
Walter MR and Des Marais DJ (1993) Preservation of biological information in thermal spring deposits: developing a strategy for the search for fossil life on Mars. Icarus 101:129–143.
Wang Y, Alsmeyer DC, and McCreery RL (1990) Raman spectroscopy of carbon materials: structural basis of observed spectra. Chem Mater 2:557–563.
Westall F (1999) The nature of fossil bacteria: a guide to the search for extraterrestrial life. J Geophys Res Planet 104:16437–16451.
Westall F, Foucher F, Bost N, et al. (2015) Biosignatures on Mars: what, where, and how? Implications for the search for Martian life. Astrobiology 15:998–1029.
Williford KH, Farley KA, Stack KM, et al. (2018) The NASA Mars 2020 Rover mission and the search for extraterrestrial life. In From Habitability to Life on Mars, edited by N.A. Cabrol and E.A. Grin, Elsevier, Amsterdam, pp 275–308.
Wopenka B and Pasteris JD (1993) Structural characterization of kerogens to granulite-facies graphite: Applicability of Raman microprobe spectroscopy. Am Mineral 78:533–557.
Wray JJ, Ehlmann BL, Squyres SW, et al. (2008) Compositional stratigraphy of clay-bearing layered deposits at Mawrth Vallis, Mars. Geophys Res Lett 35: L12202.
Xu L, Yang J, Li Y, et al. (2004) Behavior of organic sulfur model compounds in pyrolysis under coal-like environment. Fuel Process Technol 85:1013–1024.
Zhang Z (1997) A new Palaeoproterozoic clastic-facies microbiota from the Changzhougou Formation, Changcheng Group Jixian, north China. Geol Mag 134:145–150.
Zolotov M and Shock E (1999) Abiotic synthesis of polycyclic aromatic hydrocarbons on Mars. J Geophys Res Planets 104:14033–14049.
Associate Editor: Christopher McKay

Information & Authors


Published In

cover image Astrobiology
Volume 22Issue Number 10October 2022
Pages: 1239 - 1254
PubMed: 36194869


Published online: 3 October 2022
Published in print: October 2022
Published ahead of print: 16 September 2022
Accepted: 1 August 2022
Received: 17 August 2021


Request permissions for this article.




Department of Earth, Planetary, and Space Sciences, University of California, Los Angeles, California, USA.
Center for the Study of Evolution and the Origin of Life, University of California, Los Angeles, California, USA.
J. William Schopf
Department of Earth, Planetary, and Space Sciences, University of California, Los Angeles, California, USA.
Center for the Study of Evolution and the Origin of Life, University of California, Los Angeles, California, USA.
Anatoliy B. Kudryavtsev
Department of Earth, Planetary, and Space Sciences, University of California, Los Angeles, California, USA.
Center for the Study of Evolution and the Origin of Life, University of California, Los Angeles, California, USA.
Andrew D. Czaja
Department of Geology, University of Cincinnati, Cincinnati, Ohio, USA.
Kenneth H. Williford
Jet Propulsion Laboratory, California Institute of Technology, Pasadena, California, USA.


Address correspondence to: Jeffrey T. Osterhout, NASA Jet Propulsion Laboratory California Institute of Technology, 4800 Oak Grove Drive, Pasadena, CA 91109, USA [email protected]

Author Disclosure Statement

No competing financial interests exist.

Funding Information

This research was supported by the JPL (Jet Propulsion Laboratory) Visiting Student Researchers Program, and funding was provided by the UCLA Center for the Study of Evolution and the Origin of Life.

Metrics & Citations



Export citation

Select the format you want to export the citations of this publication.

View Options

Get Access

Access content

To read the fulltext, please use one of the options below to sign in or purchase access.

Society Access

If you are a member of a society that has access to this content please log in via your society website and then return to this publication.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options


View PDF/ePub

Full Text

View Full Text







Copy the content Link

Share on social media

Back to Top