Origins of Life and Evolution of Biospheres

, Volume 42, Issue 6, pp 587–609 | Cite as

Preservation and Evolution of Organic Matter During Experimental Fossilisation of the Hyperthermophilic Archaea Methanocaldococcus jannaschii

  • François OrangeEmail author
  • Jean-Robert Disnar
  • Pascale Gautret
  • Frances Westall
  • Nadège Bienvenu
  • Nathalie Lottier
  • Daniel Prieur
Microbial Fossils


Identification of the earliest traces of life is made difficult by the scarcity of the preserved microbial remains and by the alteration and potential contamination of the organic matter (OM) content of rocks. These factors can confuse interpretations of the biogenicity and syngenicity of fossilised structures and organic molecules found in ancient rocks. In order to improve our knowledge of the fossilisation processes and their effects at the molecular level, we made a preliminary study of the fate of OM during experimental fossilisation. Changes in the composition and quantity of amino acids, monosaccharides and fatty acids were followed with HPLC, GC and GC-MS analyses during 1 year of silicification of the hyperthermophilic Archaea Methanocaldococcus jannaschii. Although the cells themselves did not fossilise and the accompanying extracellular polymeric substances (EPS) did, our analyses showed that the OM initially present in both cells and EPS was uniformly preserved in the precipitated silica, with amino acids and fatty acids being the best preserved compounds. This study thus completes previous data obtained by electron microscopy investigations of simulated microbial fossilisation and can help better identification and interpretation of microbial biosignatures in both ancient rocks and in recent hydrothermal formations and sediments.


Archaea Methanocaldococcus jannaschii Fossilisation Amino acids Monosaccharides Fatty acids 



This study was financially supported by the CNRS and CNES. The authors would like to warmly thank Annie Richard for technical assistance with the electronic microscopy, and the two anonymous reviewers for their helpful comments on this manuscript.


  1. Akça E, Claus H, Schultz N, Karbach G, Schlott B, Debaerdemaeker T, Declercq JP, König H (2002) Genes and derived amino acid sequences of S-Layer proteins from mesophilic, thermophilic, and extremely thermophilic methanococci. Extremophiles 6:351–358. doi: 10.1007/s00792-001-0264-1 PubMedCrossRefGoogle Scholar
  2. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the early Archaean era of Australia. Nature 441:714–718. doi: 10.1038/nature04764 PubMedCrossRefGoogle Scholar
  3. Allwood AC, Grotzinger JP, Knoll AH, Burch IW, Andreson MS, Colemans ML, Kanik I (2009) Controls on development and diversity of early Archaean stromatolites. P Natl Acad Sci USA 106:9548–9555. doi: 10.1073/pnas.0903323106 CrossRefGoogle Scholar
  4. Antón J, Meseguer I, Rodríguez-Valera F (1988) Production of an extracellular polysaccharide by Haloferax mediterranei. Appl Environ Microb 54:2381–2386Google Scholar
  5. Balch WE, Wolfe RS (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl Environ Microb 32:781–791Google Scholar
  6. Bartley JK (1996) Actualistic taphonomy of cyanobacteria: implications for the Precambrian fossil record. Palaios 11:571–586CrossRefGoogle Scholar
  7. Benning LG, Phoenix VR, Yee N, Tobin MJ (2004a) Molecular characterization of cyanobacterial silicification using synchrotron infrared micro-spectroscopy. Geochim Cosmochim Ac 68:729–741. doi: 10.1016/S0016-7037(03)00489-7 CrossRefGoogle Scholar
  8. Benning LG, Phoenix VR, Yee N, Konhauser KO (2004b) The dynamics of cyanobacterial silicification: an infrared micro-spectroscopic investigation. Geochim Cosmochim Ac 68:743–757. doi: 10.1016/S0016-7037(03)00488-5 CrossRefGoogle Scholar
  9. Bethge O, Holmström C, Juhlin S (1966) Quantitative gas chromatography of mixtures of simple sugar. Svenk Papperstid 69:60–63Google Scholar
  10. Birnbaum SJ, Wireman JW, Borowski R (1989) Silica precipitation by the anaerobic sulphate reducing bacterium Desulfovibrio desulfuricans: effects upon cell morphology and implications for preservation. In: Crick RE (ed) Origin, evolution, and modern aspects of biomineralization in plants and animals. Plenum Press, New York, pp 507–516Google Scholar
  11. Brasier MD, Green OR, Jephcoat AP, Kleppe AK, Van Kranendonk MJ, Lindsay JF, Steele A, Grassineau NV (2002) Questioning the evidence for Earth’s oldest fosils. Nature 416:76–81. doi: 10.1038/416076a PubMedCrossRefGoogle Scholar
  12. Brocks JJ (2011) Millimeter-scale concentration gradients of hydrocarbons in Archean shales: live-oil escape or fingerprint of contamination? Geochim Cosmochim Ac 75:3196–3213CrossRefGoogle Scholar
  13. Brocks JJ, Pearson A (2005) Building the biomarker tree of life. Rev Mineral Geochem 59:233–258. doi: 10.2138/rmg.2005.59.10 CrossRefGoogle Scholar
  14. Cambilleau C, Claverie JM (2000) Structural and genomic correlates of hyperthermostability. J Biol Chemistry 275:32383–32386. doi: 10.1074/jbc.C000497200 CrossRefGoogle Scholar
  15. Camoin G, Gautret P, Montaggioni L, Cabioch G (1999) Nature and environmental significance of microbialites in quaternary reefs: the Tahiti paradox. Sediment Geol 126:271–304. doi: 10.1016/S0037-0738(99)00045-7 CrossRefGoogle Scholar
  16. Carballeira NM, Reyes M, Sostre A, Huang H, Verhagen MF, Adams MW (1997) Unusual fatty acid compositions of the hyperthermophilic Archaeon Pyrococcus furiosus and the Bacterium Thermotoga maritima. J Bacteriol 179:2766–2768PubMedGoogle Scholar
  17. Chakravarty S, Varadarajan R (2000) Elucidation of determinants of protein stability through genome sequence analysis. FEBS Lett 470:65–69. doi: 10.1016/S0014-5793(00)01267-9 PubMedCrossRefGoogle Scholar
  18. Claus H, Akça E, Debaerdemaeker T, Evrard C, Declercq JP, König H (2002) Primary structure of selected archaeal mesophilic and extremely thermophilic outer surface layer proteins. Syst Appl Microbiol 25:3–12. doi: 10.1078/0723-2020-00100 PubMedCrossRefGoogle Scholar
  19. Comont L, Laggoun-Défarge F, Disnar JR (2006) Evolution of organic matter indicators in response tomajor environmental changes: the case of a formerly cut-over peat bog (Le Russey, Jura Mountains, France). Org Geochem 37:1736–1751. doi: 10.1016/j.orggeochem.2006.08.005 CrossRefGoogle Scholar
  20. Das R, Gerstein M (2000) The stability of thermophilic proteins: a study based on comprehensive genome comparison. Funct Integr Genomic 1:76–88. doi: 10.1007/s101420050009 Google Scholar
  21. de Leeuw JW, Largeau C (1993) A review of macromolecular compounds that comprise living organisms and their role in kerogen, coal and petroleum formation. In: Engel MH, Macko SA (eds) Organic geochemistry – principles and applications. Plenum Press, New York, pp 23–72CrossRefGoogle Scholar
  22. Decho AW, Visscher PT, Reid RP (2005) Production and cycling of natural microbial exopolymers (EPS) within a marine stromatolite. Palaeogeogr Palaeocl 219:71–86. doi: 10.1016/j.palaeo.2004.10.015 CrossRefGoogle Scholar
  23. Disnar JR, Jacob J, Morched-Issa M, Lottier N, Arnaud F (2008) Assessment of peat quality by molecular and bulk geochemical analysis; application to the Holocene record of the Chautagne marsh (Haute Savoie, France). Chem Geol 254:101–112. doi: 10.1016/j.chemgeo.2008.06.004 CrossRefGoogle Scholar
  24. Eichler J (2003) Facing extremes: archaeal surface-layer (glyco)proteins. Microbiology 149:3347–3351. doi: 10.1099/mic.0.26591-0 PubMedCrossRefGoogle Scholar
  25. Ferris FG, Fyfe WS, Beveridge TJ (1988) Metallic ion binding by Bacillus subtilis: implications for the fossilization of microorganisms. Geology 16:149–152CrossRefGoogle Scholar
  26. Francis S, Margulis L, Barghoorn ES (1978) On the experimental silicification of microorganisms. II. On the time of appearance of eukaryotic organisms in the fossil record. Precambrian Res 6:65–100CrossRefGoogle Scholar
  27. Gautret P, Trichet J (2005) Automicrites in modern cyanobacterial stromatolitic deposits of Rangiroa, Tuamotu Archipelago, French Polynesia: biogeochemical parameters underlaying their formation. Sediment Geol 178:55–73. doi: 10.1016/j.sedgeo.2005.03.012 CrossRefGoogle Scholar
  28. Hall-Stoodley L, Costerton JW, Stoodley P (2005) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. doi: 10.1038/nrmicro821 CrossRefGoogle Scholar
  29. Handley KM, Turner SJ, Campbell KA, Mountain BW (2008) Silicifying biofilm exopolymers on a hot-spring microstromatolite: templating nanometer-thick laminae. Astrobiology 8:747–770. doi: 10.1089/ast.2007.0172 PubMedCrossRefGoogle Scholar
  30. Haney PJ, Badger JH, Buldak GL, Reich CI, Woese CR, Olsen CR (1999) Thermal adaptation analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococcus species. P Natl Acad Sci USA 96:3578–3583. doi: 10.1073/pnas.96.7.3578 CrossRefGoogle Scholar
  31. Hedges JI, Keil RG (1995) Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar Chem 49:81–115. doi: 10.1016/0304-4203(95)00008-F Google Scholar
  32. Jeanthon C (2000) Molecular ecology of hydrothermal vent microbial communities. Antonie Leeuwenhoek 77:117–133. doi: 10.1023/A:1002463825025 PubMedCrossRefGoogle Scholar
  33. Johnson MR, Montero CI, Conners SB, Schockley KR, Bridger SL, Kelly RM (2005) Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga maritima. Mol Microbiol 55:664–674. doi: 10.1111/j.1365-2958.2004.04419.x PubMedCrossRefGoogle Scholar
  34. Jones WJ, Leigh JA, Mayer F, Woese CR, Wolfe RS (1983) Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch Microbiol 136:254–261. doi: 10.1007/BF00425213 CrossRefGoogle Scholar
  35. Kandler O, König H (1998) Cell wall polymers in Archaea (Archaebacteria). Cell Mol Life Sci 54:305–308. doi: 10.1007/s000180050156 PubMedCrossRefGoogle Scholar
  36. Kaur G, Mountain BW, Pancost RD (2008) Microbial membrane lipids in active and inactive sinters from Champagne Pool, New Zealand: elucidating past geothermal chemistry and microbiology. Org Geochem 39:1024–1028. doi: 10.1016/j.orggeochem.2008.04.016 CrossRefGoogle Scholar
  37. Klock JH, Wieland A, Seifert R, Michaelis W (2007) Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Mar Biol 152:1077–1085. doi: 10.1007/s00227-007-0754-5 CrossRefGoogle Scholar
  38. Knicker H, Hatcher PG (1997) Survival of protein in an organic-rich sediment: possible protection by encapsulation in organic matter. Naturwissenschaften 84:231–234. doi: 10.1007/s001140050384 CrossRefGoogle Scholar
  39. Knicker H, Hatcher PG (2001) Sequestration of organic nitrogen in the sapropel from Mangrovre Lake, Bermuda. Org Geochem 32:733–744. doi: 10.1016/S0146-6380(01)00005-5 CrossRefGoogle Scholar
  40. Knoll AH, Strother PK, Rossi S (1988) Distribution and diagenesis of microfossils from the lower Proterozoic Duck Creek Dolomite, Western Australia. Precamb Res 38:257–279. doi: 10.1016/0301-9268(88)90005-8 CrossRefGoogle Scholar
  41. Konhauser KO, Jones B, Phoenix VR, Ferris G, Renaut RW (2004) The microbial role in hot spring silicification. Ambio 33:552–558. doi: 10.1579/0044-7447-33.8.552 PubMedGoogle Scholar
  42. Lalonde SV, Konhauser KO, Reysenbach AL, Ferris FG (2005) The experimental silicification of Aquificales and their role in hot spring formation. Geobiology 3:41–52. doi: 10.1111/j.1472-4669.2005.00042.x CrossRefGoogle Scholar
  43. LaPaglia C, Hartzell PL (1997) Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 63:3158–3163PubMedGoogle Scholar
  44. Maillard LC (1916) Synthèse des matières humiques par action des acides aminés sur les sucres réducteurs. Annales de Chimie, 9ème série 5:258–317Google Scholar
  45. Mayer LM (1994) Relationships between mineral surfaces and organic carbon concentrations in soils and sediments. Chem Geol 114:347–363. doi: 10.1016/0009-2541(94)90063-9 CrossRefGoogle Scholar
  46. McDonald JH, Grasso AM, Rejto LK (1999) Patterns of temperature adaptation in proteins from Methanococcus and Bacillus. Mol Biol Evol 16:1785–1790PubMedCrossRefGoogle Scholar
  47. Moers MEC, de Leeuw JW, Baas M (1994) Origin and diagenesis of carbohydrates in ancient sediments. Org Geochem 21:1093–1106. doi: 10.1016/0146-6380(94)90072-8 CrossRefGoogle Scholar
  48. Mojzsis SJ, Arrheinius G, McKeegan KD, Harrison TM, Nutman AP, Friend RL (1996) Evidence for life on Earth before 3.800 million years ago. Nature 384:55–59. doi: 10.1038/384055a0 PubMedCrossRefGoogle Scholar
  49. Mongenot T, Riboulleau A, Garcette-Lepecq A, Derenne S, Pouet Y, Baudin F, Largeau C (2001) Occurrence of proteinaceous moieties in S- and O-rich Late Tithonian kerogen (Kashpir oil shales, Russia). Org Geochem 32:199–203. doi: 10.1016/S0146-6380(00)00154-6 CrossRefGoogle Scholar
  50. Neuweiler F, Gautret P, Thiel V, Lange R, Michaelis W, Reitner J (2002) Petrology of lower cretaceous carbonate mud mounds (Albian, N. Spain): insights into organomineralic deposits of the geological record. Sedimentology 46:837–859. doi: 10.1046/j.1365-3091.1999.00255.x CrossRefGoogle Scholar
  51. Nguyen RT, Harvey HR (1998) Protein preservation during early diagenesis in marine waters and sediments. In: Stankiewicz BA, van Bergen PF (eds) Nitrogen-containing macromolecules in the bio- and geosphere. ACS Symposium Series 707., pp 89–112Google Scholar
  52. Nguyen RT, Harvey HR (2001) Preservation of proteins in marine systems: hydrophobic and other noncovalent associations as major stabilizing forces. Geochim Cosmochim Ac 65:1467–1480. doi: 10.1016/S0016-7037(00)00621-9 CrossRefGoogle Scholar
  53. Nguyen RT, Harvey HR (2003) Preservation via macromolecular associations during Botryococcus braunii decay: proteins in the Pula Kerogen. Org Geochem 34:1391–1403. doi: 10.1016/S0146-6380(02)00261-9 CrossRefGoogle Scholar
  54. Nishihira M, Nagahama S, Ohga M, Koga Y (2000) Straight-chain fatty alcohols in the hyperthermophilic archaeon Pyrococcus furiosus. Extremophiles 4:275–277. doi: 10.1007/s007920070013 CrossRefGoogle Scholar
  55. Oehler JH (1976) Experimental studies in Precambrian paleontology: structural and chemical changes in blue-green algae during simulated fossilization in synthetic chert. Geol Soc Am Bull 87:117–129CrossRefGoogle Scholar
  56. Oehler JH, Schopf JW (1971) Artificial microfossils: experimental studies of permineralization of blue-green algae in silica. Science 174:1229–1231PubMedCrossRefGoogle Scholar
  57. Ogier S, Disnar JR, Albéric P, Bourdier G (2001) Neutral carbohydrate geochemistry of particulate material (trap and core sediments) in an eutrophic lake (Aydat, France). Org Geochem 32:151–162. doi: 10.1016/S0146-6380(00)00138-8 CrossRefGoogle Scholar
  58. Orange F, Westall F, Disnar JR, Prieur D, Bienvenu N, Le Romancer M, Défarge C (2009) Experimental silicification of the extremophilic Archaea Pyrococcus abyssi and Methanocaldococcus jannaschii. Applications in the search for evidence of life in early Earth and extraterrestrial rocks. Geobiology 7:403–418. doi: 10.1111/j.1472-4669.2009.00212.x PubMedCrossRefGoogle Scholar
  59. Orange F, Disnar JR, Westall F, Prieur D, Baillif P (2011) Metal cation binding by the hyperthermophilic microorganism, Archaea Methanocaldococcus jannaschii, and its effects on silicification. Palaeontology 54:954–964. doi: 10.1111/j.1475-4983.2011.01066.x CrossRefGoogle Scholar
  60. Pancost RD, Pressley S, Coleman JM, Benning LG, Mountain BW (2005) Lipid biomolecules in silica sinters: indicators of microbial biodiversity. Environ Microbiol 7:66–77. doi: 10.1111/j.1462-2920.2004.00686.x PubMedCrossRefGoogle Scholar
  61. Pancost RD, Pressley S, Coleman JM, Talbot HM, Kelly SP, Farrimond P, Schouten S, Benning LG, Mountain BW (2006) Composition and implications of diverse lipids in New Zealand geothermal sinters. Geobiology 4:71–92. doi: 10.1111/j.1472-4669.2006.00069.x CrossRefGoogle Scholar
  62. Patel GB, Sprott, GD (2006) Archaeal membrane lipids. In: ELS. John Wiley & Sons Ltd, Chichester. Accessed August 21 2011. doi: 10.1038/npg.els.0004316
  63. Pflug HD, Jaeschke-Boyer H (1979) Combined structural and chemical analysis of 3,800-Myr-old microfossils. Nature 280:483–486. doi: 10.1038/280483a0 CrossRefGoogle Scholar
  64. Phoenix VR, Adams DG, Konhauser KO (2000) Cyanobacterial viability during hydrothermal biomineralization. Chem Geol 169:329–338. doi: 10.1016/S0009-2541(00)00212-6 CrossRefGoogle Scholar
  65. Poinar HN, Stankiewicz BA (1999) Protein preservation and DNA retrieval from ancient tissues. P Natl Acad Sci USA 96:8426–8431CrossRefGoogle Scholar
  66. Poli A, Anzelmo G, Nicolaus B (2010) Bacterial exopolysaccharides from extreme marine habitats: production, characterization and biological activities. Mar Drugs 8:1779–1802. doi: 10.3390/md8061779 PubMedCrossRefGoogle Scholar
  67. Riboulleau A, Mongenot T, Baudin F, Derenne S, Largeau C (2002) Factors controlling the survival of protaneiceous material in Late Tithonian kerogens (Kashpri Oil Shales, Russia). Org Geochem 33:1127–1130. doi: 10.1016/S0146-6380(02)00081-5 CrossRefGoogle Scholar
  68. Rinker KD, Kelly RM (1996) Growth physiology of the hyperthermophilic Archaeon Thermococcus littoralis: development of a sulfur-free defined medium, characterization of an exopolysaccharide, and evidence of biofilm formation. Appl Environ Microbiol 62:4478–4485PubMedGoogle Scholar
  69. Salmon V, Derenne S, Lallier-Verges E, Largeau C, Beaudoin B (1998) Study of the role of the mineral matrix in sedimentary organic matter preservation (Cenomanian black shale, Central Italy). Mineral Mag 62A:1312–1313CrossRefGoogle Scholar
  70. Schopf JW (1993) Microfossils of the early Archaean Apex Chert: new evidence of the antiquity of life. Science 260:640–646. doi: 10.1126/science.260.5108.640 PubMedCrossRefGoogle Scholar
  71. Schopf S, Wanner G, Rachel R, Wirth R (2008) An archaeal bi-species formed by Pyrococcus furiosus and Methanopyrus kandleri. Arch Microbiol 190:371–377. doi: 10.1007/s00203-008-0371-9 PubMedCrossRefGoogle Scholar
  72. Schultze-Lam S, Ferris FG, Kohnauser KO, Wiese RG (1995) In situ silicification of an Icelandic microbial mat: implications for microfossil formation. Can J Earth Sci 32:2021–2026CrossRefGoogle Scholar
  73. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176. doi: 10.1023/A:1016125726789 CrossRefGoogle Scholar
  74. Sowers KR, Gunsalus RP (1988) Adaptation for growth at various saline concentration by the Archaebacterium Methanosarcina thermophila. J Bacteriol 170:998–1002PubMedGoogle Scholar
  75. Stefanova M, Disnar JR (2000) Composition and early diagenesis of fatty acids in lacustrine sediments, lake Aydat (France). Org Geochem 31:41–55. doi: 10.1016/S0146-6380(99)00134-5 CrossRefGoogle Scholar
  76. Tanoue E, Ishii M, Midorikawa T (1996) Discrete dissolved and particulate proteins in oceanic waters. Limnol Oceanogr 41:1334–1343CrossRefGoogle Scholar
  77. Tice MM, Lowe DR (2004) Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431:522–523. doi: 10.1038/nature02888 CrossRefGoogle Scholar
  78. Tice MM, Lowe DR (2007) Tectonic controls on atmospheric, climatic, and biological evolution 3.5–2.4 Ga. Precamb Res 158:177–197. doi: 10.1016/j.precamres.2007.04.008 CrossRefGoogle Scholar
  79. Toporski JKW, Steele A, Westall F, Thomas-Keprta KL, McKay DS (2002) The simulated silicification of bacteria – new clues to the modes and timing of bacterial preservation and implications for the search for extraterrestrialmicrofossils. Astrobiology 2:21–26CrossRefGoogle Scholar
  80. Tornabene TG, Langworthy TA (1979) Diphytanyl and dibiphytanyl glycerol ethers of methanogenic archaebacteria. Science 203:51–53. doi: 10.1126/science.758677 PubMedCrossRefGoogle Scholar
  81. Tornabene TG, Wolfe RS, Balch WE, Holzer G, Fox GE, Oro O (1978) Phytanylglycerol ethers and squalene in the archaebacterium Methanobacterium thermoautotrophicum. J Mol Evol 11:259–266. doi: 10.1007/BF01734487 PubMedCrossRefGoogle Scholar
  82. Underwood GJC, Paterson DM, Parkes RJ (1995) The measurement of microbial carbohydrate exopolymers from intertidal sediments. Limnol Oceanogr 40:1243–1253CrossRefGoogle Scholar
  83. van Zuilen MA, Lepland A, Arrhenius A (2002) Reassessing the evidence for the earliest traces of life. Nature 418:627–630. doi: 10.1038/nature00934 PubMedCrossRefGoogle Scholar
  84. Vandenbroucke M, Largeau C (2007) Kerogen origin, evolution and structure. Org Geochem 38:719–833. doi: 10.1016/j.orggeochem.2007.01.001 CrossRefGoogle Scholar
  85. Walsh MM (1992) Microfossils and possible microfossils from the early Archean Onverwacht Group, Barberton Mountain Land, South Africa. Precamb Res 54:271–293CrossRefGoogle Scholar
  86. Walsh MM (2004) Evaluation of early Archean volcanoclastic and volcanic flow rocks as possible sites for carbonaceous fossil microbes. Astrobiology 4:429–437PubMedCrossRefGoogle Scholar
  87. Westall F (1997) The influence of cell wall composition on the fossilization of bacteria and the implications for the search for early life forms. In: Cosmovici C, Bowyer S, Werthimer D (eds) Astronomical and biochemical origins and the search for life in the universe. Editori Compositrici, Bologna, pp 491–504Google Scholar
  88. Westall F (2011) Early life: nature, distribution and evolution. In: Gargaud M, López-García P, Martin H (eds) Origins and evolution of life, an astrobiological perspective. Cambridge University Press, Cambridge, pp 391–413CrossRefGoogle Scholar
  89. Westall F, Cavalazzi B (2011) Biosignatures in rocks. In: Reitner J, Volker T (eds) Encyclopedia of geobiology. Springer, Dordrecht, pp 189–201Google Scholar
  90. Westall F, Folk RL (2003) Exogenous carbonaceous microstructures in early Archaean cherts and BIFs from the Isua greenstone belt: implications for the search for life in ancient rocks. Precamb Res 126:313–330. doi: 10.1016/S0301-9268(03)00102-5 CrossRefGoogle Scholar
  91. Westall F, Southam G (2006) The early record of life. In: Benn K, Mareschal JC, Condie KC (eds) Archean geodynamics and environments, geophysical monograph series 164. American Geophysical Union, Washington, DC, pp 283–304CrossRefGoogle Scholar
  92. Westall F, Boni L, Guerzoni E (1995) The experimental silicification of microorganisms. Paleontology 38:495–528Google Scholar
  93. Westall F, Steele A, Toporski J, Walsh M, Allen C, Guidry S, McKay D, Gibson E, Chafetz H (2000) Polymeric substances and biofilms as biomarkers in terrestrial materials: implications for extraterrestrial samples. J Geophys Res 105:24511–24527. doi: 10.1029/2000JE001250 CrossRefGoogle Scholar
  94. Westall F, de Vries ST, Nijman W, Rouchon V, Orberger B, Pearson V, Watson J, Verchovsky A, Wright I, Rouzaud JN, Marchesini D, Severine A (2006a) The 3.466 Ga “Kitty’s Gap Chert”, an early Archean microbial ecosystem. Spec Pap Geol Soc Am 405:105–131. doi: 10.1130/2006.2405(07) Google Scholar
  95. Westall F, de Ronde CEJ, Southam G, Grassineau N, Colas M, Cockell C, Lammer H (2006b) Implication of a 3.472–3.333 Gyr-old subaerial microbial mat from the Barberton greenstone belt, South Africa for the UV environmental conditions on the early Earth. Phil Trans R Soc B 361:1857–1875. doi: 10.1098/rstb.2006.1896 PubMedCrossRefGoogle Scholar
  96. Westall F, Cavalazzi B, Lemelle L, Marrocchi Y, Rouzaud JN, Simionovici A, Salomé M, Mostefaoui S, Andreazza C, Foucher F, Toporski J, Jauss A, Thiel V, Southam G, MacLean L, Wirick S, Hofmann A, Meibom A, Robert F, Défarge C (2011) Implications of in situ calcification for photosynthesis in a ~3.3 Ga-old microbial biofilm from the Barberton greenstone belt, South Africa. Earth Planet Sc Lett 310:468–479. doi: 10.1016/j.epsl.2011.08.029 CrossRefGoogle Scholar
  97. Wicks RJ, Moran MA, Pittman LJ, Hodson RE (1991) Carbohydrates signatures of aquatic macrophytes and their dissolved degradation products as determined by sensitive high-performance ion chromatography method. Appl Environ Microb 57:3135–3143Google Scholar
  98. Zang X, van Heemst JDH, Dria KJ, Hatcher PG (2000) Encapsulation of protein in humic acid from a histosol as an explanation for the occurrence of organic nitrogen in soil and sediment. Org Geochem 31:679–695. doi: 10.1016/S0146-6380(00)00040-1 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • François Orange
    • 1
    • 2
    • 3
    • 4
    • 5
    Email author
  • Jean-Robert Disnar
    • 3
    • 4
    • 5
  • Pascale Gautret
    • 3
    • 4
    • 5
  • Frances Westall
    • 1
    • 2
  • Nadège Bienvenu
    • 6
  • Nathalie Lottier
    • 3
    • 4
    • 5
  • Daniel Prieur
    • 6
  1. 1.Centre de Biophysique Moléculaire – UPR 4301, CNRSOrléans Cedex 2France
  2. 2.Observatoire des Sciences de l’Univers en région Centre – UMS 3116Orléans Cedex 2France
  3. 3.Univ d’Orléans, ISTO, UMR 7327OrléansFrance
  4. 4.CNRS/INSU, ISTO, UMR 7327OrléansFrance
  5. 5.BRGM, ISTO, UMR 7327OrléansFrance
  6. 6.Université de Bretagne Occidentale, Institut Universitaire Européen de la Mer – UMR 6197, Technopôle Brest IroisePlouzanéFrance

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