Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor

  • Marjorie D. Cantine
  • Gregory P. FournierEmail author


Extensive fundamental molecular and biological evolution took place between the prebiotic origins of life and the state of the Last Universal Common Ancestor (LUCA). Considering the evolutionary innovations between these two endpoints from the perspective of environmental adaptation, we explore the hypothesis that LUCA was temporally, spatially, and environmentally distinct from life’s earliest origins in an RNA world. Using this lens, we interpret several molecular biological features as indicating an environmental transition between a cold, radiation-shielded origin of life and a mesophilic, surface-dwelling LUCA. Cellularity provides motility and permits Darwinian evolution by connecting genetic material and its products, and thus establishing heredity and lineage. Considering the importance of compartmentalization and motility, we propose that the early emergence of cellularity is required for environmental dispersal and diversification during these transitions. Early diversification and the emergence of ecology before LUCA could be an important pre-adaptation for life’s persistence on a changing planet.


Origin of life Last universal common ancestor (LUCA) Environmental adaptation 



The authors acknowledge funding from the Simons Foundation through the Simons Collaboration on the Origins of Life (Award #339603) and the NASA Astrobiology Institute (supplement to award #MIT/NNA13AA90A) M. D. Cantine was supported by a Whiteman Fellowship through MIT. The authors thank two anonymous reviewers for their feedback on the manuscript.


  1. Abramov O, Mojzsis SJ (2009) Microbial habitability of the Hadean Earth during the late heavy bombardment. Nature 459(7245):419–422PubMedCrossRefGoogle Scholar
  2. Akoopie A, Müller UF (2016) Lower temperature optimum of a smaller, fragmented triphosphorylation ribozyme. Phys Chem Chem Phys 18:20118–20125PubMedCrossRefGoogle Scholar
  3. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the Early Archaean era of Australia. Nature 441(7094):714–718PubMedCrossRefGoogle Scholar
  4. Atomi H, Matsumi R, Imanaka T (2004) Reverse gyrase is not a prerequisite for hyperthermophilic life. J Microbiol 186(14):4829–4833Google Scholar
  5. Attwater J, Wochner A, Pinheiro VB, Coulson A, Holliger P (2010) Ice as a protocellular medium for RNA replication. Nat Commun 1:76PubMedCrossRefGoogle Scholar
  6. Attwater J, Wochner A, Holliger P (2013) In-ice evolution of RNA polymerase ribozyme activity. Nat Chem 5(12):1011–1018PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bada JL, Bigham C, Miller SL (1994) Impact melting of frozen oceans on the early Earth: implications for the origin of life. P Natl Acad Sci USA 91(4):1248–1250CrossRefGoogle Scholar
  8. Badro J, Siebert J, Nimmo F (2016) An early geodynamo driven by exsolution of mantle components from Earth’s core. Nature 536(7616):326–328PubMedPubMedCentralCrossRefGoogle Scholar
  9. Barboni M, Boehnke P, Keller B, Kohl IE, Schoene B, Young ED, McKeegan KD (2017) Early formation of the Moon 4.51 billion years ago. Sci Adv 3(1):e1602365PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bargar KE, Fournier RO (1988) Effects of glacial ice on subsurface temperatures of hydrothermal systems in Yellowstone National Park, Wyoming: Fluid-inclusion evidence. Geology 16(12):1077–1080CrossRefGoogle Scholar
  11. Beckstead AA, Zhang Y, de Vries MS, Kohler B (2016) Life in the light: nucleic acid photoproperties as a legacy of chemical evolution. Phys Chem Chem Phys 18(35):24228–24238PubMedCrossRefGoogle Scholar
  12. Bernal JD (1951) The physical basis of life. Routledge and Paul, LondonGoogle Scholar
  13. Bernhardt HS (2012) The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others) Biol. Direct 7(1):1CrossRefGoogle Scholar
  14. Bernstein H (1977) Germ line recombination may be primarily a manifestation of DNA repair processes. J Theor Biol 69(2):371–380PubMedCrossRefGoogle Scholar
  15. Bianconi G, Zhao K, Chen IA, Nowak MA (2013) Selection for replicases in protocells. PLoS Comput Biol 9(5):e1003051PubMedPubMedCentralCrossRefGoogle Scholar
  16. Biondi E, Branciamore S, Maurel MC, Gallori E (2007) Montmorillonite protection of an UV-irradiated hairpin ribozyme: evolution of the RNA world in a mineral environment. BMC Evol Biol 7(2):S2PubMedPubMedCentralCrossRefGoogle Scholar
  17. Boehnke P, Harrison TM (2016) Illusory Late Heavy Bombardments. Proc Natl Acad Sci U S A 113(39):10802–10806PubMedPubMedCentralCrossRefGoogle Scholar
  18. Boussau B, Blanquart S, Necsulea A, Lartillot N, Gouy M (2008) Parallel adaptations to high temperatures in the Archaean eon. Nature 456(7224):942–945PubMedCrossRefGoogle Scholar
  19. Bowring SA, Williams IS (1999) Priscoan (4.00–4.03 Ga) orthogneisses from northwestern Canada. Contrib Mineral Petrol 134(1):3–16CrossRefGoogle Scholar
  20. Brochier-Armanet C, Forterre P (2006) Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2(2):83–93PubMedCentralCrossRefGoogle Scholar
  21. Brooks DJ, Fresco JR, Lesk AM, Singh M (2002) Evolution of amino acid frequencies in proteins over deep time: inferred order of introduction of amino acids into the genetic code. Mol Biol Evol 19(10):1645–1655PubMedCrossRefGoogle Scholar
  22. Brown M (2006) Duality of thermal regimes is the distinctive characteristic of plate tectonics since the Neoarchean. Geology 34(11):961–964CrossRefGoogle Scholar
  23. Brown ME, Hand KP (2013) Salts and radiation products on the surface of Europa. Astron J 145(4):110CrossRefGoogle Scholar
  24. Budin I, Debnath A, Szostak JW (2012) Concentration-driven growth of model protocell membranes. J Am Chem Soc 134(51):20812–20819PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cabrol NA, Wettergreen D, Warren-Rhodes K, Grin EA, Moersch J, Diaz, GC, et al (2007) Life in the Atacama: Searching for life with rovers (science overview). J Geophys Res-Biogeo 112(G04S02). doi: 10.1029/2006JG000298
  26. Chen IA, Roberts RW, Szostak JW (2004) The emergence of competition between model protocells. Science 305(5689):1474–1476PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chyba CF, Hand KP (2001) Life without photosynthesis. Science 292(5524):2026–2027PubMedCrossRefGoogle Scholar
  28. Chyba CF, Phillips CB (2001) Possible ecosystems and the search for life on Europa. Proc Natl Acad Sci U S A 98(3):801–804PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cnossen I, Sanz-Forcada J, Favata F, Witasse O, Zegers T, Arnold NF (2007) Habitat of early life: Solar X-ray and UV radiation at Earth's surface 4–3.5 billion years ago. J Geol Res E 112(E02008). doi: 10.1029/2006JE002784
  30. Cockell CS (1998) Biological effects of high ultraviolet radiation on early Earth—a theoretical evaluation. J Theor Biol 193(4):717–729PubMedCrossRefGoogle Scholar
  31. Deamer D, Dworkin JP, Sandford SA, Bernstein MP, Allamandola LJ (2002) The first cell membranes. Astrobiology 2(4):371–381PubMedCrossRefGoogle Scholar
  32. DeChaine EG, Bates AE, Shank TM, Cavanaugh CM (2006) Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents. Environ Microbiol 8(11):1902–1912PubMedCrossRefGoogle Scholar
  33. Draganić Z, Draganić I, Shimoyama A, Ponnamperuma C (1977) Evidence for amino acids in hydrolysates of compounds formed by ionizing radiations. Origins Life 8(4):371–376CrossRefGoogle Scholar
  34. Engelhart, AE, Adamala KP, Szostak JW (2016) A simple physical mechanism enables homeostasis in primitive cells. Nat Chem 8(5):448-53Google Scholar
  35. Feulner G (2012) The faint young Sun problem. Rev Geophys 50(RG2006). doi: 10.1029/2011RG000375
  36. Forterre P (1996) A hot topic: the origin of hyperthermophiles. Cell 85(6):789–792PubMedCrossRefGoogle Scholar
  37. Forterre P (2002) A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet 18(5):236–237PubMedCrossRefGoogle Scholar
  38. Forterre P, Confalonier F, Charbonnier F, Duguet M (1995) Speculations on the origin of life and thermophily: review of available information on reverse gyrase suggests that hyperthermophilic procaryotes are not so primitive. Origins Life Evol B 25(1–3):235–249CrossRefGoogle Scholar
  39. Fournier GP, Alm EJ (2015) Ancestral reconstruction of a pre-LUCA aminoacyl-tRNA synthetase ancestor supports the late addition of Trp to the genetic code. J Mol Evol 80(3–4):171–185PubMedCrossRefGoogle Scholar
  40. Fournier GF, Gogarten JP (2010) Rooting the ribosomal tree of life. Mol Biol Evol 27(8):1792–1801PubMedCrossRefGoogle Scholar
  41. Fournier GP, Andam CP, Alm EJ, Gogarten JP (2011) Molecular evolution of aminoacyl tRNA synthetase proteins in the early history of life. Origins Life Evol B 41(6):621–632CrossRefGoogle Scholar
  42. Fournier GP, Andam CP, Gogarten JP (2015) Ancient horizontal gene transfer and the last common ancestors. BMC Evol Biol 15(1):1CrossRefGoogle Scholar
  43. Galtier N, Tourasse N, Gouy M (1999) A nonhyperthermophilic common ancestor to extant life forms. Science 283(5399):220–221PubMedCrossRefGoogle Scholar
  44. Ganesan A, Hanawalt P (2016) Photobiological Origins of the Field of Genomic Maintenance. Photochem Photobiol 92(1):52–60PubMedCrossRefGoogle Scholar
  45. Garzón L, Garzón ML (2001) Radioactivity as a significant energy source in prebiotic synthesis. Origins Life Evol B 31(1):3–13CrossRefGoogle Scholar
  46. Gillon M et al (2017) Seven temperate terrestrial planets around the nearby ultracool dwarf star TRAPPIST-1. Nature 542(7642):456–460PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gogarten JP, Taiz L (1992) Evolution of proton pumping ATPases: rooting the tree of life. Photosynth Res 33(2):137–146PubMedCrossRefGoogle Scholar
  48. Gogarten JP et al (1989) Evolution of the vacuolar H+−ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci U S A 86(17):6661–6665PubMedPubMedCentralCrossRefGoogle Scholar
  49. Gogarten JP, Starke T, Kibak H, Fishman J, Taiz L (1992) Evolution and isoforms of V-ATPase subunits. J Exp Biol 172(1):137–147PubMedGoogle Scholar
  50. Grotzinger JP et al (2014) A habitable fluvio-lacustrine environment at Yellowknife Bay, Gale Crater, Mars. Science 343(6169):1242777PubMedCrossRefGoogle Scholar
  51. Groussin M, Boussau B, Charles S, Blanquart S, Gouy M (2013) The molecular signal for the adaptation to cold temperature during early life on Earth. Biol Lett 9(5):20130608PubMedPubMedCentralCrossRefGoogle Scholar
  52. Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13(3):407–412PubMedPubMedCentralCrossRefGoogle Scholar
  53. Heijde M, Zabulon G, Corellou F, Ishikawa T, Brazard J, Usman A, Todo T (2010) Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes. Plant Cell Environ 33(10):1614–1626PubMedCrossRefGoogle Scholar
  54. Heine M, Chandra SB (2009) The linkage between reverse gyrase and hyperthermophiles: a review of their invariable association. J Microbiol 47(3):229–234PubMedCrossRefGoogle Scholar
  55. Hilario E, Gogarten JP (1993) Horizontal transfer of ATPase genes—the tree of life becomes a net of life. Biosystems 31(2–3):111–119PubMedCrossRefGoogle Scholar
  56. Hoeppner MP, Gardner PP, Poole AM (2012) Comparative analysis of RNA families reveals distinct repertoires for each domain of life. PLoS Comput Biol 8(11):e1002752PubMedPubMedCentralCrossRefGoogle Scholar
  57. Horneck G (1993) Responses of Bacillus subtilis spores to space environment: Results from experiments in space. Origins Life Evol B 23(1):37–52CrossRefGoogle Scholar
  58. Hren MT, Tice MM, Chamberlain CP (2009) Oxygen and hydrogen isotope evidence for a temperate climate 3.42 billion years ago. Nature 462(7270):205–208PubMedCrossRefGoogle Scholar
  59. Hughes AR, Inouye BD, Johnson MT, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11(6):609–623PubMedCrossRefGoogle Scholar
  60. Islas S, Velasco AM, Becerra A, Delaye L, Lazcano A (2003) Hyperthermophily and the origin and earliest evolution of life. Int Microbiol 6(2):87–94PubMedCrossRefGoogle Scholar
  61. Iwabe N, Kuma KI, Hasegawa M, Osawa S, Miyata T (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A 86(23):9355–9359PubMedPubMedCentralCrossRefGoogle Scholar
  62. Jackson JB (2016) Natural pH Gradients in Hydrothermal Alkali Vents Were Unlikely to Have Played a Role in the Origin of Life. J Mol Evol 83(1–2):1–11PubMedPubMedCentralCrossRefGoogle Scholar
  63. Jangir Y, French S, Momper LM, Moser DP, Amend JP, El-Naggar MY (2016) Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species. Front Microbiol. 7(756). doi: 10.3389/fmicb.2016.00756
  64. Jékely G (2006) Did the last common ancestor have a biological membrane? Biol Direct 1(1):35PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kanai S, Kikuno R, Toh H, Ryo H, Todo T (1997) Molecular evolution of the photolyase–blue-light photoreceptor family. J Mol Evol 45(5):535–548PubMedCrossRefGoogle Scholar
  66. Kawamura K, Nagahama M, Kuranoue K (2005) Chemical evolution of RNA under hydrothermal conditions and the role of thermal copolymers of amino acids for the prebiotic degradation and formation of RNA. Adv Space Res 35(9):1626–1633PubMedCrossRefGoogle Scholar
  67. Kienert H, Feulner G, Petoukhov V (2012) Faint young Sun problem more severe due to ice-albedo feedback and higher rotation rate of the early Earth. Geophys Res Lett 39(L23710). doi: 10.1029/2012GL054381
  68. Kikuchi A, Asai K (1984) Reverse gyrase-a topoisomerase which introduces positive superhelical turns into DNA. Nature 309:677–681PubMedCrossRefGoogle Scholar
  69. Kladwang W, Hum J, Das R (2012) Ultraviolet shadowing of RNA causes substantial non-Poissonian chemical damage in seconds. Sci Rep 2012;2:517. doi:  10.1038/srep00517.
  70. Koeberl C (2006) Impact processes on the early Earth. Elements 2(4):211–216CrossRefGoogle Scholar
  71. Koga Y, Kyuragi T, Nishihara M, Sone N (1998) Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent. J Mol Evol 46(1):54–63PubMedCrossRefGoogle Scholar
  72. Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1(2):127–136PubMedCrossRefGoogle Scholar
  73. Koonin EV, Martin W (2005) On the origin of genomes and cells within inorganic compartments. Trends Genet 21(12):647–654PubMedCrossRefGoogle Scholar
  74. Kua J, Bada JL (2011) Primordial ocean chemistry and its compatibility with the RNA world. Origins Life Evol B 41(6):553–558CrossRefGoogle Scholar
  75. Lanier KA, Athavale SS, Petrov AS, Wartell R, Williams LD (2016) Imprint of Ancient Evolution on rRNA Folding. Biochemistry 55(33):4603–4613PubMedCrossRefGoogle Scholar
  76. Lanier KA, Roy P, Schneider DM, Williams LD (2017) Ancestral Interactions of Ribosomal RNA and Ribosomal Proteins. Biophys J. doi: 10.1016/j.bpj.2017.04.007
  77. Lazcano A (1995) Cellular evolution during the early Archean: what happened between the progenote and the cenancestor? Microbiol SEM 11:185–198Google Scholar
  78. Lazcano A, Guerrero R, Margulis L, Oro J (1988) The evolutionary transition from RNA to DNA in early cells. J Mol Evol 27(4):283–290PubMedCrossRefGoogle Scholar
  79. Levy M, Miller SL (1998) The stability of the RNA bases: implications for the origin of life. P Natl A Sci USA 95(14):7933–7938CrossRefGoogle Scholar
  80. Levy M, Miller SL, Brinton K, Bada JL (2000) Prebiotic synthesis of adenine and amino acids under Europa-like conditions. Icarus 145(2):609–613PubMedCrossRefGoogle Scholar
  81. Lipenkov VY, Ekaykin AA, Polyakova EV, Raynaud D (2016) Characterization of subglacial Lake Vostok as seen from physical and isotope properties of accreted ice. Phil Trans R Soc A 374(2059):20140303PubMedCrossRefGoogle Scholar
  82. Lombard J, López-García P, Moreira D (2012) The early evolution of lipid membranes and the three domains of life. Nat Rev Microbiol 10(7):507–515PubMedCrossRefGoogle Scholar
  83. Lyons TW, Reinhard CT, Planavsky NJ (2014) The rise of oxygen in Earth's early ocean and atmosphere. Nature 506(7488):307–315PubMedCrossRefGoogle Scholar
  84. Mansy SS, Szostak JW (2008) Thermostability of model protocell membranes. P Natl A Sci USA 105(36):13351–13355CrossRefGoogle Scholar
  85. Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162(3):346–361PubMedCrossRefGoogle Scholar
  86. Margulis L (1981) Symbiosis in cell evolution: Life and its environment on the early earth. WH Freeman & Co, San FranciscoGoogle Scholar
  87. Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos T Roc Soc B 358(1429):59–85CrossRefGoogle Scholar
  88. Martin W, Baross J, Kelley D, Russell MJ (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol 6(11):805–814PubMedCrossRefGoogle Scholar
  89. McCollom TM (2013) Miller-Urey and beyond: what have we learned about prebiotic organic synthesis reactions in the past 60 years? Annu Rev Earth Pl Sc 41:207–229CrossRefGoogle Scholar
  90. McKay CP, Anbar AD, Porco C, Tsou P (2014) Follow the plume: The habitability of Enceladus. Astrobiology 14(4):352–355PubMedCrossRefGoogle Scholar
  91. McLoughlin N, Grosch EG, Kilburn MR, Wacey D (2012) Sulfur isotope evidence for a Paleoarchean subseafloor biosphere, Barberton, South Africa. Geology 40(11):1031–1034CrossRefGoogle Scholar
  92. Mirkin BG, Fenner TI, Galperin MY, Koonin EV (2003) Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol Biol 3(1):1CrossRefGoogle Scholar
  93. Miyakawa S, Cleaves JH, Miller SL (2002) The cold origin of life: B Implications based on pyrimidines and purines produced from frozen ammonium cyanide solutions. Origins Life Evol B 32(3):209–218CrossRefGoogle Scholar
  94. Mojzsis SJ, Harrison TM, Pidgeon RT (2001) Oxygen-isotope evidence from ancient zircons for liquid water at the Earth's surface 4,300 Myr ago. Nature 409(6817):178–181PubMedCrossRefGoogle Scholar
  95. Monnard PA, Apel CL, Kanavarioti A, Deamer DW (2002) Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: Implications for a prebiotic aqueous medium. Astrobiology 2(2):139–152PubMedCrossRefGoogle Scholar
  96. Moulton V, Gardner PP, Pointon RF, Creamer LK, Jameson GB, Penny D (2000) RNA folding argues against a hot-start origin of life. J Mol Evol 51(4):416–421PubMedCrossRefGoogle Scholar
  97. Myers JS (2001) Protoliths of the 3.8–3.7 Ga Isua greenstone belt, west Greenland. Precambrian Res 105(2):129–141CrossRefGoogle Scholar
  98. Nagel GM, Doolittle RF (1995) Phylogenetic analysis of the aminoacyl-tRNA synthetases. J Mol Evol 40(5):487–498PubMedCrossRefGoogle Scholar
  99. O’Malley-James JT, Kaltenegger L (2017) UV surface habitability of the TRAPPIST-1 system. Mon Not R Astron 469(1):L26–L30CrossRefGoogle Scholar
  100. Ohtomo Y, Kakegawa T, Ishida A, Nagase T, Rosing MT (2014) Evidence for biogenic graphite in early Archaean Isua metasedimentary rocks. Nat Geosci 7(1):25–28CrossRefGoogle Scholar
  101. Peterson G, Allen CR, Holling CS (1998) Ecological resilience, biodiversity, and scale. Ecosystems 1(1):6–18CrossRefGoogle Scholar
  102. Petit C, Sancar A (1999) Nucleotide excision repair: from E. coli to man. Biochimie 81(1):15–25PubMedCrossRefGoogle Scholar
  103. Petrov AS et al (2015) History of the ribosome and the origin of translation. Proc Natl Acad Sci U S A 112(50):15396–15401PubMedPubMedCentralCrossRefGoogle Scholar
  104. Poole AM, Jeffares DC, Penny D (1998) The path from the RNA world. J Mol Evol 46(1):1–17PubMedCrossRefGoogle Scholar
  105. Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459(7244):239–242PubMedCrossRefGoogle Scholar
  106. Price PB (2007) Microbial life in glacial ice and implications for a cold origin of life. FEMS Microbiol Ecol 59(2):217–231PubMedCrossRefGoogle Scholar
  107. Rambler MB, Margulis L (1980) Bacterial resistance to ultraviolet irradiation under anaerobiosis: implications for pre-phanerozoic evolution. Science 210(4470):638–640PubMedCrossRefGoogle Scholar
  108. Ranea JA, Sillero A, Thornton JM, Orengo CA (2006) Protein superfamily evolution and the last universal common ancestor. (LUCA). J Mol Evol 63(4):513–525PubMedCrossRefGoogle Scholar
  109. Ranjan S, Sasselov DD (2016) Influence of the UV Environment on the Synthesis of Prebiotic Molecules. Astrobiology 16(1):68–88PubMedCrossRefGoogle Scholar
  110. Ravanat JL, Douki T (2016) UV and ionizing radiations induced DNA damage, differences and similarities. Radiat Phys Chem 128:92–102CrossRefGoogle Scholar
  111. Reusch TB, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA Proceedings of the National Academy of Sciences of the United States of America 102(8):2826–2831PubMedCrossRefGoogle Scholar
  112. Ritson D, Sutherland JD (2012) Prebiotic synthesis of simple sugars by photoredox systems chemistry. Nat Chem 4(11):895–899PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409(6823):1092–1101PubMedCrossRefGoogle Scholar
  114. Russell MJ, Hall AJ (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc Lond 154(3):377–402CrossRefGoogle Scholar
  115. Sagan C (1957) Radiation and the origin of the gene. Evolution 11(1):40-55Google Scholar
  116. Schopf JW (1993) Microfossils of the Early Archean Apex chert: new evidence of the antiquity of life. Science 260(5108):640–646PubMedCrossRefGoogle Scholar
  117. Shimada H, Yamagishi A (2011) Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochemistry 50(19):4114–4120PubMedCrossRefGoogle Scholar
  118. Sluijs A, Schouten S, Pagani M, Woltering M, Brinkhuis H, Damsté JSS et al (2006) Subtropical Arctic Ocean temperatures during the Palaeocene/Eocene thermal maximum. Nature 441(7093):610–613PubMedCrossRefGoogle Scholar
  119. Sparks WB, Schmidt BE, McGrath MA, Hand KP, Spencer JR, Cracraft M, Deustua SE (2017) Active Cryovolcanism on Europa? Astrophys J Lett 839(2):L18CrossRefGoogle Scholar
  120. Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol 131(1):1–32CrossRefGoogle Scholar
  121. Stephenson JD, Freeland SJ (2013) Unearthing the root of amino acid similarity. J Mol Evol 77(4):159–169PubMedCrossRefGoogle Scholar
  122. Stern RJ (2005) Evidence from ophiolites, blueschists, and ultrahigh-pressure metamorphic terranes that the modern episode of subduction tectonics began in Neoproterozoic time. Geology 33(7):557–560CrossRefGoogle Scholar
  123. Sugitani K, Lepot K, Nagaoka T, Mimura K, Van Kranendonk M, Oehler DZ, Walter MR (2010) Biogenicity of morphologically diverse carbonaceous microstructures from the ca. 3400 Ma Strelley Pool Formation, in the Pilbara Craton. Western Australia Astrobiology 10(9):899–920Google Scholar
  124. Sutherland JD (2017) Opinion: Studies on the origin of life—the end of the beginning. Nat Rev Chem 1:0012CrossRefGoogle Scholar
  125. Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409(6818):387–390PubMedCrossRefGoogle Scholar
  126. Tang M, Chen K, Rudnick RL (2016) Archean upper crust transition from mafic to felsic marks the onset of plate tectonics. Science 351(6271):372–375PubMedCrossRefGoogle Scholar
  127. Tarduno JA, Cottrell RD, Smirnov AV (2006) The paleomagnetism of single silicate crystals: Recording geomagnetic field strength during mixed polarity intervals, superchrons, and inner core growth. Rev Geophys 44(RG1002). doi: 10.1029/2005RG000189
  128. Trinks H, Schröder W, Biebricher CK (2005) Ice and the origin of life. Origins Life Evol B 35(5):429–445CrossRefGoogle Scholar
  129. Ueno Y, Yamada K, Yoshida N, Maruyama S, Isozaki Y (2006) Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature 440(7083):516–519PubMedCrossRefGoogle Scholar
  130. Valley JW, Peck WH, King EM, Wilde SA (2002) A cool early Earth. Geology 30(4):351–354CrossRefGoogle Scholar
  131. Vincent WF, Mueller D, Van Hove P, Howard-Williams C (2004) Glacial periods on early Earth and implications for the evolution of life. In: Seckbach J (ed) Origins. Springer, Netherlands, pp 483–501CrossRefGoogle Scholar
  132. Wacey D (2010) Stromatolites in the ∼3400 Ma Strelley Pool Formation, Western Australia: examining biogenicity from the macro-to the nano-scale. Astrobiology 10(4):381–395PubMedCrossRefGoogle Scholar
  133. Westall F, De Ronde CE, Southam G, Grassineau N, Colas M, Cockell C, Lammer H (2006) Implications of a 3472–3333 Gyr-old subaerial microbial mat from the Barberton greenstone belt, South Africa for the UV environmental conditions on the early Earth. Philosophical Philos T Roc Soc B 361(1474):1857–1876CrossRefGoogle Scholar
  134. Wienken CJ, Baaske P, Duhr S, Braun D (2011) Thermophoretic melting curves quantify the conformation and stability of RNA and DNA. Nucleic Acids Res 39(8):e52. doi: 10.1093/nar/gkr035
  135. Wilde SA, Valley JW, Peck WH, Graham CM (2001) Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago. Nature 409:175–118PubMedCrossRefGoogle Scholar
  136. Witkin EM (1969) Ultraviolet-induced mutation and DNA repair. Annu Rev Genet Review of Genetics 3(1):525–552Google Scholar
  137. Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221Google Scholar
  138. Wolf ET, Toon OB (2010) Fractal organic hazes provided an ultraviolet shield for early Earth. Science 328(5983):1266–1268PubMedCrossRefGoogle Scholar
  139. Zeldovich KB, Berezovsky IN, Shakhnovich EI (2007) Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput Biol 3(1):e5PubMedPubMedCentralCrossRefGoogle Scholar
  140. Zhu TF, Adamala K, Zhang N, Szostak JW (2012) Photochemically driven redox chemistry induces protocell membrane pearling and division. P Natl A Sci USA 25:9828–9832CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of Earth, Atmospheric and Planetary SciencesMassachusetts Institute of TechnologyCambridgeUSA

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