Hostname: page-component-797576ffbb-xg4rj Total loading time: 0 Render date: 2023-12-03T01:37:44.943Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "useRatesEcommerce": true } hasContentIssue false

Fossils and astrobiology: new protocols for cell evolution in deep time

Published online by Cambridge University Press:  07 September 2012

Martin D. Brasier
Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK
David Wacey*
Department of Earth Sciences and Centre for Geobiology, Allegaten 41, University of Bergen, N-5007, Norway Centre for Core to Crust Fluid Systems, Centre for Microscopy Characterisation and Analysis, and School of Earth and Environment, The University of Western Australia, 35 Stirling Highway, WA 6009, Australia


The study of life remote in space has strong parallels with the study of life remote in time. Both are dependent on decoding those historic phenomena called ‘fossils’, here taken to include biogenic traces of activity and waste products. There is the shared problem of data restoration from incomplete data sets; the importance of contextual analysis of potentially viable habitats; the centrality of cell theory; the need to reject the null hypothesis of an abiogenic origin for candidate cells via morphospace analysis; the need to demonstrate biology-like behaviour (e.g., association with biofilm-like structures; tendency to form clusters and ‘mats’; and a preference for certain substrates), and of metabolism-like behaviour (e.g., within the candidate cell wall; within surrounding ‘waste products’; evidence for syntrophy and metabolic cycles; and evidence for metabolic tiers). We combine these ideas into a robust protocol for demonstrating ancient or extra-terrestrial life, drawing examples from Earth's early geological record, in particular from the earliest known freshwater communities of the 1.0 Ga Torridonian of Scotland, from the 1.9 Ga Gunflint Chert of Canada, from the 3.4 Ga Strelley Pool sandstone of Australia, and from the 3.46 Ga Apex Chert also of Australia.

Research Article
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Allison, P.A. & Bottjer, D. (eds) (2011). Taphonomy: Process and Bias through Time, 2nd edn, p. 599. Springer, Dordrecht.Google Scholar
Allwood, A.C., Walter, M.R., Kamber, B.S., Marshal, C.P. & Burch, I.W. (2006). Stromatolite reef from the Early Archean era of Australia. Nature 441, 714718.Google Scholar
Anbar, A.D. (2004). Iron stable isotopes: beyond biosignatures. Earth Planet. Sci. Lett. 217, 223236.Google Scholar
Antcliffe, J.B. & McLoughlin, N. (2009). Deciphering Fossil Evidence for the origins of life and the origins of animals: common challenges in different worlds. In From Fossils to Astrobiology. Records of Life on Earth and the Search for Extraterrestrial Biosignatures, ed. Seckbach, J. & Walsh, M., pp. 211232. Springer, Dordrecht.Google Scholar
Archer, C. & Vance, D. (2006). Coupled Fe and S isotope evidence for Archean microbial Fe(III) and sulfate reduction. Geology 34, 153156.Google Scholar
Armstrong, H.A. & Brasier, M.D. (2004). Microfossils, 2nd edn, p. 304. Blackwell Publishing, Oxford.Google Scholar
Awramik, S., Schopf, J. & Walter, M. (1983). Filamentous fossil bacteria from the Archean of Western Australia. Precambrian Res. 20, 357374.Google Scholar
Bak, P. (1997). How nature works. The Science of Self-organized Criticality, p. 212. Oxford University Press, New York.Google Scholar
Ball, P. (1999). The self-made tapestry. Pattern Formation in Nature, p. 287. Oxford University Press, New York.Google Scholar
Ball, P. (2009). Branches. Nature's Patterns: A Tapestry in Three Parts, p. 221. Oxford University Press, New York.Google Scholar
Bailey, J.V., Raub, T.D., Meckler, A.N., Harrison, B.K., Rauub, T.M.D., Green, A.M. & Orphan, V.J. (2010). Pseudofossils in relict methane seep carbonates resemble endemic microbial consortia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 285, 131142.Google Scholar
Barghoorn, E.S. & Tyler, S.A. (1965). Microorganisms from the Gunflint Chert. Science 147, 563577.Google Scholar
Brasier, A.T. (2011). Searching for travertines, calcretes and speleothems in deep time: processes, appearances, predictions and the impact of plants. Earth Sci. Rev. 104, 213239.Google Scholar
Brasier, M.D. (1980). Microfossils, p. 193. Unwin Hyman, London.Google Scholar
Brasier, M.D. (2009). Darwin's Lost World. The Hidden History of Animal Life, p. 304. Oxford University Press, New York.Google Scholar
Brasier, M.D. (2010). Towards a null hypothesis for stromatolites. In Earliest Life on Earth. Habitats, Environments and Methods of Detection, ed. Golding, S.D. & Glikson, M., pp. 115125. Springer, Dordrecht.Google Scholar
Brasier, M.D. (2012). Secret Chambers: The Inside Story of Cells and Complex Life, p. 256. Oxford University Press, New York.Google Scholar
Brasier, M.D., Green, O.R., Jephcoat, A.P., Kleppe, A.K., Van Kranendonk, M.J., Lindsay, J.F., Steele, A., Grassineau, N.V. (2002). Questioning the evidence for Earth's oldest fossils. Nature 416, 7681.Google Scholar
Brasier, M.D., Green, O.R. & Mcloughlin, N. (2004). Characterization and critical testing of potential microfossils from the early Earth: the Apex ‘microfossil debate’ and its lessons for Mars sample return. Int. J. Astrobiol. 3, 112.Google Scholar
Brasier, M.D., Green, O.R., Lindsay, J.F., McLoughlin, N., Steele, A. & Stoakes, C. (2005). Critical testing of Earth's oldest putative fossil assemblage from the ∼3.5 Ga Apex Chert, Chinaman Creek Western Australia. Precambrian Res. 140, 55102.Google Scholar
Brasier, M.D., McLoughlin, N., Green, O.R. & Wacey, D. (2006). A fresh look at the fossil evidence for early Archaean cellular life. Philos. Trans. R. Soc. B 361, 887902.Google Scholar
Brasier, M.D., Callow, R.H.T., Menon, L. & Liu, A. (2010). Osmotrophic biofilms: from modern to ancient. In Microbial Mats. Modern and Ancient Microorganisms in Stratified Systems, ed. Seckbach, J. & Oren, A., pp. 131148. Springer, Dordrecht.Google Scholar
Brasier, M.D., Wacey, D. & McLoughlin, N. (2011a). Taphonomy in temporally unique settings: a traverse in search of the earliest life on Earth. In Taphonomy: Process and Bias Through Time, Topics in Geobiology 32, ed. Allison, P.A. & Bottjer, D.J., pp. 487518. Springer, Dordrecht.Google Scholar
Brasier, M.D., Matthewman, R., McMahon, S. & Wacey, D. (2011b). Pumice as a remarkable substrate for the origin of life. Astrobiology 11, 725735.Google Scholar
Brasier, M.D., Green, O.R., Lindsay, J.F., McLoughlin, N., Stoakes, C., Brasier, A. & Wacey, D. (2011c). Geology and putative microfossil assemblage of the c. 3460 Ma ‘Apex Chert’, Chinaman Creek, Western Australia – a field and petrographic guide. Geological Survey of Western Australia, Record 2011/7, 60.Google Scholar
Buick, R., Thornett, J.R., McNaughton, N.J., Smith, J.B., Barley, M.E. & Savage, M. (1995). Record of emergent continental crust ∼3.5 billion years ago in the Pilbara craton of Australia. Nature 375, 574577.Google Scholar
Callow, R.H.T., Battison, L. & Brasier, M.D. (2011). Diverse microbially induced sedimentary structures from 1 Ga lakes of the Diabaig Formation, northwest Scotland. Sediment. Geol. 239, 117128.Google Scholar
Corsetti, F.A. & Storrie-Lombardie, M.C. (2003). Lossless compression of stromatolite images: a biogenicity index. Astrobiology 3, 649655.Google Scholar
Darwin, C. (1871). On the Origin of Species, 1871 edn.John Murray, London.Google Scholar
Deamer, D., Dworkin, J.P., Sandford, S.A., Bernstein, M.P. & Allamandola, L.J. (2002). The first cell membranes. Astrobiology 2, 371381.Google Scholar
De Gregorio, B.T. & Sharp, T.G. (2006). The structure and distribution of carbon in 3.5 Ga Apex chert: implications for the biogenicity of Earth's oldest putative microfossils. Am. Mineral.t 91, 784789.Google Scholar
Dick, S.J. & Strick, J.E. (2005). The Living Universe. NASA and the Development of Astrobiology, p. 308. Rutgers University Press, New Brunswick.Google Scholar
Donoghue, P.C.J., Bengtson, S., Dong, X., Gostling, N.J., Huldtgren, T., Cunningham, J.A., Yin, C., Yue, Z., Peng, F. & Stampanoni, M. (2006). Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680683.Google Scholar
Doolittle, W.F. (2000). Uprooting the tree of life. Sci. Am. 282, 9095.Google Scholar
Furnes, H., Staudigel, H., Thorseth, I.H., Torsvik, T., Muehlenbachs, K. & Tumyr, O. (2001). Bioalteration of basaltic glass in the oceanic crust, G3, 2, 2000GC000150.Google Scholar
Furnes, H., Banerjee, N.R., Staudigel, H., Muehlenbachs, K., McLoughlin, N., de Wit, M. & Van Kranendonk, M. (2007). Comparing petrographic signatures of bioalteration in recent to Mesoarchean pillow lavas: tracing subsurface life in oceanic igneous rocks. Precambrian Res. 158, 156176.Google Scholar
Garcia-Ruiz, J.M., Hyde, S.T., Carnerup, A.M., Christy, A.G., Van Kranendonk, M.J. & Welham, N.J. (2003). Self assembled silica-carbonate structures and detection of ancient microfossils. Science 302, 11941197.Google Scholar
Gilmour, I. (2003). Understanding Mars, p. 167. The Open University, Milton Keynes.Google Scholar
Hardin, J., Bertoni, G. & Kleinsmith, L.J. (2011). Becker's World of the Cell, 8th edn, p. 793. Pearson Benjamin Cummings, Boston, USA.Google Scholar
Hofmann, H.J. (1971). Precambrian fossils, pseudofossils and problematica in Canada. Bull. Geol. Surv. Canada 189, 146.Google Scholar
Hopkinson, L., Roberts, S., Herrington, R. & Wilkinson, J. (1998). Self-organization of submarine hydrothermal siliceous deposits: evidence from the TAG hydrothermal mound, 26°N Mid Atlantic Ridge. Geology 26, 347350.Google Scholar
Hoover, R. (2011). Fossils of cyanobacteria in CI1 carbonaceous meteorites; and commentary No 9, by martin brasier life in C11 carbonaceous chondrites? J. Cosmol. 13, Scholar
House, C.H., Schopf, J.W., McKeegan, K.D., Coath, C.D., Harrison, T.M. & Stetter, K.O. (2000). Carbon isotopic composition of individual Precambrian microfossils. Geology 28, 707710.Google Scholar
Jannasch, H.W. & Mottl, M.J. (1985). Geomicrobiology of deep-sea hydrothermal vents. Science 229, 717725.Google Scholar
Javaux, E., Marshall, C.P. & Bekker, A. (2010). Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934939.Google Scholar
Kempe, A., Wirth, R., Altermann, W., Stark, R.W., Schopf, J.W. & Heckl, W.M. (2005). Focussed ion beam preparation and in situ nanoscopic study of Precambrian acritarchs. Precambrian Res. 140, 3654.Google Scholar
Kilburn, M.R. & Wacey, D. (2011). Elemental and isotopic analysis by NanoSIMS: insights for the study of stromatolites and early life on Earth. In Stromatolites: Cellular Origin, Life in Extreme Habitats and Astrobiology, ed. Seckbach, J. & Tewari, V. pp. 463493. Springer.Google Scholar
Knoll, A.H. (2003). Life on a Young Planet: The First Three Billion Years of Evolution on Earth, p. 277. Princeton University Press.Google Scholar
Knoll, A.H., Canfield, D.E. & Konhauser, K.O. (eds) (2012). Fundamentals of Geobiology, p. 456. Wiley-Blackwell, Chichester.Google Scholar
Konhauser, K. (2007). Introduction to Geomicrobiology, p. 423. Blackwell, Oxford.Google Scholar
Krumbein, W., Paterson, D.M. & Zavarzin, G.A. (eds) (2003). Fossil and Recent Biofilms: A Natural History of Life on Earth, p. 482. Kluwer, Dordrecht.Google Scholar
Lemelle, L., Labrot, P., Salome, M., Simionovici, A., Viso, M. & Westall, F. (2008). In situ imaging of organic sulfur in 700–800 My-old Neoproterozoic microfossils using X-ray spectromicroscopy at the S K-edge. Org. Geochem. 39, 188202.Google Scholar
Lepot, K., Benzerara, K., Brown, G.E. Jr. & Philippot, P. (2008). Microbially influenced formation of 2724-million-year-old stromatolites. Nature Geosci. 1, 118121.Google Scholar
Martin, W. & Russell, M.J. (2007). On the origin of biochemistry at an alkaline hydrothermal vent. Philos. Trans. R. Soc. B 362, 18871926.Google Scholar
Marshall, C.P., Emry, J.R. & Olcott Marshall, A. (2011). Haematite pseudomicrofossils present in the 3.5-billion-year-old Apex Chert. Nature Geosci. 4, 240243.Google Scholar
McKay, D., Gibson, E.K. Jr, Thomas-Keprta, K.L., Vali, H., Romanek, C.S., Clemett, S.J., Chillier, X.D.F., Maechling, C.R. & Zare, R.N. (1996). Search for past life on Mars: possible relic biogenic activity in Martian meteorite ALH84001. Science 273, 924930.Google Scholar
McLoughlin, N., Brasier, M.D., Wacey, D., Green, O.R. & Perry, R. (2007). On biogenicity criteria for endolithic microborings on early Earth and beyond. Astrobiology 7, 1026.Google Scholar
McLoughlin, N., Wilson, L.A. & Brasier, M.D. (2008). Growth of synthetic stromatolites and wrinkle structures in the absence of microbes: implications for the early fossil record. Geobiology 6, 95105.Google Scholar
Mulkidjanian, A.Y., Bychkov, A.Yu., Dibrova, D.V., Galperin, M.Y. & Koonin, E.V. (2012). Origin of first cells at terrestrial anoxic geothermal fields. Proc. Nat. Acad. Sci. U.S.A. 109, E821830.Google Scholar
Noffke, N. (2010). Geobiology: Microbial Mats in Sandy Deposits from the Archean Era to Today, p. 194. Springer, Dordrecht.Google Scholar
Noffke, N., Eriksson, K.A., Hazen, R.M. & Simpson, E.L. (2006). A new window into early Archean life: microbial mats in Earth's oldest siliciclastic tidal deposits (3.2 Ga Moodies group, South Africa). Geology 34, 253256.Google Scholar
Oehler, D.Z., Robert, F., Mostefaoui, S., Meibom, A., Selo, M. & McKay, D.S. (2006). Chemical mapping of Proterozoic organic matter at submicron spatial resolution. Astrobiology 6, 838850.Google Scholar
Oehler, D.Z., Robert, F., Walter, M.R., Sugitani, K., Allwood, A., Meibom, A., Mostefaoui, S., Selo, M., Thomen, A. & Gibson, E.K. (2009). NanoSIMS: insights to biogenicity and syngeneity of Archaean carbonaceous structures. Precambrian Res. 173, 7078.Google Scholar
Oehler, D.Z., Robert, F., Walter, M.R., Sugitani, K., Meibom, M., Mostefaoui, S. & Gibson, E.K. (2010). Diversity in the Archean biosphere: new insights from NanoSIMS. Astrobiology 10, 413424.Google Scholar
Olcott Marshall, A., Emry, J.R. & Marshall, C.P. (2012). Multiple generations of carbon in the Apex Chert and implications for preservation of microfossils. Astrobiology 12, 160166.Google Scholar
Orphan, V.J. & House, C.H. (2009). Geobiological investigations using secondary ion mass spectrometry: microanalysis of extant and paleo-microbial processes. Geobiology 7, 360372.Google Scholar
Pasteris, J.D., Wopenka, B. (2003). Necessary, but not sufficient: Raman identification of disordered carbon as a signature of ancient life. Astrobiology 3, 727738.Google Scholar
Perry, R.S. et al. (2007). Defining biominerals and organominerals: direct and indirect indicators of life. Sed. Geol. 201, 157179.Google Scholar
Philippot, P., van Zuilen, M., Thomazo, C., Farquhar, J. & Van Kranendonk, M.J. (2007). Early Archaean microorganisms preferred elemental sulfur, not sulfate. Science 317, 15341537.Google Scholar
Pinti, D.L., Mineau, R. & Clement, V. (2009). Hydrothermal alteration and microfossil artefacts of the 3465-million-year-old Apex chert. Nature Geosci. 2, 640643.Google Scholar
Reitner, J., Queric, N-V. & Arp, G. (eds) (2011). Advances in Stromatolite Geobiology, Lecture Notes in Earth Sciences, p. 559. Springer, Dordrecht.Google Scholar
Rickards, D. (2012). Sedimentary Sulfides. Elsevier, Amsterdam (In press).Google Scholar
Riding, R. (2011). The nature of stromatolites: 3500 million years of history and a century of research. In Advances in Stromatolite Geobiology, Lecture Notes in Earth Sciences, ed. Reitner, J., Queric, N-V. & Arp, G., pp. 2974. Springer, Dordrecht.Google Scholar
Rose, E., McLoughlin, N. & Brasier, M.D. (2006). Ground truth: the epistemology of searching for the earliest life on Earth. In Life As We Know It. Cellular Origin, Life in Extreme Habitats and Astrobiology, ed. Seckbach, J., Vol. 10, pp. 259286. Springer-Verlag, Berlin.Google Scholar
Schopf, J.W. (1993). Microfossils of the Early Archaean Apex Chert: new evidence for the antiquity of life. Science 260, 640646.Google Scholar
Schopf, J.W. (1999). The Cradle of Life, p. 367. Princeton University Press, New York.Google Scholar
Schopf, J.W. & Kudryavtsev, A.B. (2005). Three-dimensional Raman imagery of Precambrian microscopic organisms. Geobiol. 3, 112.Google Scholar
Schopf, J.W. & Kudryavtsev, A.B. (2009). Confocal laser scanning microscopy and Raman imaging of ancient microscopic fossils. Precambrian Res. 173, 3949.Google Scholar
Schopf, J.W., Kudryavtsev, A.B., Agresti, D.G., Wdowiak, T.J. & Czaja, A.D. (2002). Laser-Raman imagery of Earth's earliest fossils. Nature 416, 7376.Google Scholar
Schopf, J.W., Kudryavtsev, A.B., Agresti, D.G., Czaja, A.D. & Wdowiak, T. J. (2005). Raman imagery: a new approach to assess the geochemical maturity and biogenicity of permineralized Precambrian fossils. Astrobiology 5, 333371.Google Scholar
Schopf, J.W., Kudyatsev, A.B., Sugitani, K. & Walter, M.R. (2010). Precambrian microbe-like pseudofossils: a promising solution to the problem. Precambrian Res. 179, 191205.Google Scholar
Seckbach, J. & Oren, A. (eds) (2010). Microbial Mats. Modern and Ancient Microorganisms in Stratified Systems, p. 606. Springer, Dordrecht.Google Scholar
Strother, P.K., Battison, L., Brasier, M.D. & Wellman, C.H. (2011). Earth's earliest non-marine eukaryotes. Nature 473, 505509.Google Scholar
Templeton, A. & Knowles, E. (2009). Microbial transformations of minerals and metals: recent advances in geomicrobiology derived from synchrotron-based X-ray spectroscopy and X-ray microscopy. Annu. Rev. Earth Planet. Sci. 37, 367391.Google Scholar
Tyler, S.A. & Barghoorn, E.S. (1954). Occurrence of structurally preserved plants in Pre-Cambrian rocks of the Canadian Shield. Science 119, 606608.Google Scholar
Tyler, S.A. & Barghoorn, E.S. (1963). Ambient pyrite grains in Precambrian cherts. Am. J. Sci. 261, 424432.Google Scholar
Ueno, Y., Isozaki, Y., Yurimoto, H. & Maruyama, S. (2001). Carbon isotopic signatures of individual Archean microfossils(?) from Western Australia. Int. Geol. Rev. 43, 196212.Google Scholar
van Zuilen, M.A., Mathew, K., Wopenka, B., Lepland, A., Marti, K. & Arrhenius, G. (2005). Nitrogen and argon isotopic signatures in graphite from the 3.8-Ga-old Isua Supracrustal Belt, Southern West Greenland. Geochim. Cosmochim. Acta 69, 12411252.Google Scholar
Varnam, A.H. & Evans, M.G. (2000). Environmental Microbiology, p. 160. Manson Publishing, London.Google Scholar
Wacey, D. (2009). Early Life on Earth: A practical Guide, p. 285. Springer, Amsterdam.Google Scholar
Wacey, D., McLoughlin, N., Green, O.R., Parnell, J., Stoakes, C.A. & Brasier, M.D. (2006). The ∼3.4 billion year old Strelley Pool Sandstone: a new window into early life on Earth. Int. J. Astrobiol. 5, 333342.Google Scholar
Wacey, D., Kilburn, M.R., McLoughlin, N., Parnell, J., Stoakes, C.A. & Brasier, M.D. (2008). Using NanoSIMS in the search for early life on Earth: ambient inclusion trails in a c.3400 Ma sandstone. J. Geol. Soc. Lond. 165, 4353.Google Scholar
Wacey, D., McLoughlin, N., Whitehouse, M. & Kilburn, M.R. (2010a). Two co-existing sulfur metabolisms in a ∼3430 Ma sandstone. Geology 38, 11151118.Google Scholar
Wacey, D., McLoughlin, N., Stoakes, C.A., Kilburn, M.R., Green, O.R. & Brasier, M.D. (2010b). The 3426–3350 Ma Strelley Pool Formation in the East Strelley Greenstone Belt – A Field and Petrographic Guide. Geological Survey of Western Australia Record 2010/10, Perth, p. 71.Google Scholar
Wacey, D., Saunders, M., Brasier, M.D. & Kilburn, M.R. (2011a). Earliest microbially-mediated pyrite oxidation in ∼3.4 billion-year-old sediments. Earth Planet. Sci. Lett. 301, 393402.Google Scholar
Wacey, D., Kilburn, M., Saunders, M., Cliff, J. & Brasier, M.D. (2011b). Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nature Geosci. 4, 698702.Google Scholar
Wacey, D., Menon, S., Green, L., Gerstmann, D., Kong, C., McLoughlin, N., Saunders, M. & Brasier, M.D. (2012). Taphonomy of microfossils from the ∼3400 Ma Strelley Pool Formation and ∼1900 Ma Gunflint Formation: new insights using focused ion beam. Precambrian Res. (in press).Google Scholar
Walter, M.R. (1976). Stromatolites, p. 790. Elsevier, Amsterdam.Google Scholar
Walter, M.R. (1999). The Search for Life on Mars, p. 170. Perseus Publishing, Cambridge, MA.Google Scholar
Williams, D.B. & Carter, C.B. (2009). Transmission Electron Microscopy: A Textbook for Materials Science, 2nd edn, p. 832. Springer Science and Business Media, New York.Google Scholar