Journal of Molecular Evolution

, Volume 72, Issue 3, pp 283–295 | Cite as

Monomer Abundance Distribution Patterns as a Universal Biosignature: Examples from Terrestrial and Digital Life

  • Evan D. Dorn
  • Kenneth H. Nealson
  • Christoph AdamiEmail author


Organisms leave a distinctive chemical signature in their environment because they synthesize those molecules that maximize their fitness. As a result, the relative concentrations of related chemical monomers in life-bearing environmental samples reflect, in part, those compounds’ adaptive utility. In contrast, rates of molecular synthesis in a lifeless environment are dictated by reaction kinetics and thermodynamics, so concentrations of related monomers in abiotic samples tend to exhibit specific patterns dominated by small, easily formed, low-formation-energy molecules. We contend that this distinction can serve as a universal biosignature: the measurement of chemical concentration ratios that belie formation kinetics or equilibrium thermodynamics indicates the likely presence of life. We explore the features of this biosignature as observed in amino acids and carboxylic acids, using published data from numerous studies of terrestrial sediments, abiotic (spark, UV, and high-energy proton) synthesis experiments, and meteorite bodies. We then compare these data to the results of experimental studies of an evolving digital life system. We observe the robust and repeatable evolution of an analogous biosignature in a digital lifeform, suggesting that evolutionary selection necessarily constrains organism composition and that the monomer abundance biosignature phenomenon is universal to evolved biosystems.


Artificial life Amino acids Carboxylic acids Astrobiology Exobiology Evolution Meteorites 



The research described in this work was carried out in part at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration (NASA), with support from the Director’s Research and Development Fund (DRDF) and from the National Science Foundation under contract Nos. DEB-9981397, FIBR-0527023 and NSF’s BEACON Center for Evolution in Action, under contract No. DBI-0939454. We thank Claus Wilke, Ronald V. Dorn III, and Diana Sherman for discussions. Finally, we are grateful to three anonymous reviewers for extensive and constructive comments on the manuscript.


  1. Abelson PH (1965) Abiogenic synthesis in martian environment. Proc Natl Acad Sci USA 54:1490–1494PubMedCrossRefGoogle Scholar
  2. Abelson PH, Hare PE (1969) Recent amino acids in the gunflint chert. Carnegie Inst Wash Yearb 69:208–210Google Scholar
  3. Adami C (1998) Introduction to artificial life. Springer, New YorkGoogle Scholar
  4. Adami C (2006) Digital genetics: unravelling the genetic basis of evolution. Nat Rev Genet 7:109–118Google Scholar
  5. Adami C, Ofria C, Collier TC (2000) Evolution of biological complexity. Proc Natl Acad Sci USA 97:4463–4468PubMedCrossRefGoogle Scholar
  6. Amend JP, Shock EL (1998) Energetics of amino acid synthesis in hydrothermal ecosystems. Science 281:1659–1662PubMedCrossRefGoogle Scholar
  7. Anders E, Hayatsu R, Studier MH (1973) Organic compounds in meteorites. Science 182:781–790PubMedCrossRefGoogle Scholar
  8. Baath E, Frostegard A, Fritze H (1992) Soil bacterial biomass, activity, phospholipid fatty-acid pattern, and ph tolerance in an area polluted with alkaline dust deposition. Appl Environ Microbiol 58:4026–4031PubMedGoogle Scholar
  9. Bell G (2001) Neutral macroecology. Science 293:2413–2418PubMedCrossRefGoogle Scholar
  10. Botta O, Glavin DP, Kminek G, Bada JL (2002) Relative amino acid concentrations as a signature for parent body processes of carbonaceous chondrites. Orig Life Evol Biosph 32:143–163PubMedCrossRefGoogle Scholar
  11. 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 19:1645–1655PubMedGoogle Scholar
  12. Chow SS, Wilke CO, Ofria C, Lenski RE, Adami C (2004) Adaptive radiation from resource competition in digital organisms. Science 305:84–86PubMedCrossRefGoogle Scholar
  13. Colombo JC, Silverberg N, Gearing JN (1996) Lipid biogeochemistry in the laurentian trough 1. Fatty acids, sterols and aliphatic hydrocarbons in rapidly settling particles. Org Geochem 25:211–225CrossRefGoogle Scholar
  14. Colombo JC, Silverberg N, Gearing JN (1998) Amino acid biogeochemistry in the laurentian trough: vertical fluxes and individual reactivity during early diagenesis. Org Geochem 29:933–945CrossRefGoogle Scholar
  15. Cowie GL, Hedges JI, Calvert SE (1992) Sources and relative reactivities of amino-acids, neutral sugars, and lignin in an intermittently anoxic marine-environment. Geochim Cosmochim Acta 56:1963–1978CrossRefGoogle Scholar
  16. Cronin JR, Moore CB (1976) Amino-acids of Nogoya and Mokoia carbonaceous chondrites. Geochim Cosmochim Acta 40:853–857CrossRefGoogle Scholar
  17. Cronin JR, Pizzarello S, Moore CB (1979) Amino-acids in an antarctic carbonaceous chondrite. Science 206:335–337PubMedCrossRefGoogle Scholar
  18. Cronin JR, Moore CB, Pizzarello S (1980) Amino-acids in six CM2 chondrites. Meteoritics 15:277–278Google Scholar
  19. Cronin JR, Gandy WE, Pizzarello S (1981) Amino-acids of the Murchison meteorite 1. 6 carbon acyclic primary alpha-amino alkanoic acids. J Mol Evol 17:265–272PubMedCrossRefGoogle Scholar
  20. Cronin JR, Cooper GW, Pizzarello S (1994) Characteristics and formation of amino-acids and hydroxy-acids of the Murchison meteorite. In: Life sciences and space research XXV (4), Pergamon Press Ltd., Oxford, vol 15 of advances in space research, pp 91–97Google Scholar
  21. Dauwe B, Middelburg JJ (1998) Amino acids and hexosamines as indicators of organic matter degradation state in north sea sediments. Limnol Oceanogr 43:782–798CrossRefGoogle Scholar
  22. Davies PCW, Benner SA, Cleland CE, Lineweaver CH, McKay CP, Wolfe-Simon F (2009) Signatures of a shadow biosphere. Astrobiology 9:241–249PubMedCrossRefGoogle Scholar
  23. Deamer DW (1999) How did it all begin? The self-assembly of organic molecules and the origin of cellular life. In: Scotchmoor J, Springer DA (eds) Evolution: investigating the evidence, vol 9. The Paleontological Society, KnoxvilleGoogle Scholar
  24. Dorn ED, McDonald GD, Storrie-Lombardi MC, Nealson KH (2003) Principal component analysis and neural networks for detection of amino acid biosignatures. Icarus 166:403–409CrossRefGoogle Scholar
  25. Elster H, Emanuel G, Weiner S (1991) Amino acid racemization of fossil bone. J Archaeol Sci 18:605–617CrossRefGoogle Scholar
  26. Engel MH, Macko SA (1997) Isotopic evidence for extraterrestrial non-racemic amino acids in the Murchison meteorite. Nature 389:265–268PubMedCrossRefGoogle Scholar
  27. Engel MH, Nagy B (1982) Distribution and enantiomeric composition of amino-acids in the Murchison meteorite. Nature 296:837–840CrossRefGoogle Scholar
  28. Engel MH, Macko SA, Silfer JA (1990) Carbon isotope composition of individual amino-acids in the Murchison meteorite. Nature 348:47–49PubMedCrossRefGoogle Scholar
  29. Gebicki JM, Hicks M (1976) Preparation and properties of vesicles enclosed by fatty acid membranes. Chem Phys Lipids 16:142–160PubMedCrossRefGoogle Scholar
  30. Gorban AN, Zinovyev AY, Popova TG (2003) Seven clusters in genomic triplet distributions. In Silico Biol 3:471–482PubMedGoogle Scholar
  31. Hargreaves WR, Deamer DW (1978) Liposomes from ionic, single-chain amphiphiles. Biochemistry 17Google Scholar
  32. Hayatsu R, H SM, Anders E (1971) Origin of organic matter in early solar system iv. Amino acids: confirmation of catalytic synthesis by mass spectrometry. Geochim Cosmochim Acta 35:939–951CrossRefGoogle Scholar
  33. Hedges JI, Oades JM (1997) Comparative organic geochemistries of soils and marine sediments. Org Geochem 27:319–361CrossRefGoogle Scholar
  34. Hedges JI, Mayorga E, Tsamakis E, McClain ME, Aufdenkampe A, Quay P, Richey JE, Benner R, Opsahl S, Black B, Pimentel T, Quintanilla J, Maurice L (2000) Organic matter in bolivian tributaries of the amazon river: a comparison to the lower mainstream. Limnol Oceanogr 45:1449–1466CrossRefGoogle Scholar
  35. Horsfall IM, Wolff GA (1997) Hydrolysable amino acids in sediments from the porcupine abyssal plain, northeast atlantic ocean. Org Geochem 26:311–320CrossRefGoogle Scholar
  36. Keil RG, Fogel ML (2001) Reworking of amino acid in marine sediments: stable carbon isotopic composition of amino acids in sediments along the washington coast. Limnol Oceanogr 46:14–23CrossRefGoogle Scholar
  37. Keil RG, Tsamakis E, Giddings JC, Hedges JI (1998) Biochemical distributions (amino acids, neutral sugars, and lignin phenols) among size-classes of modern marine sediments from the washington coast. Geochim Cosmochim Acta 62:1347–1364CrossRefGoogle Scholar
  38. Khare BN, Sagan C, Ogino H, Nagy B, Er C, Schram KH, Arakawa ET (1986) Amino-acids derived from Titan tholins. Icarus 68:176–184PubMedCrossRefGoogle Scholar
  39. Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98CrossRefGoogle Scholar
  40. Kvenvolden KA, Lawless J, Pering K, Peterson E, Flores J, Ponnamperuma C, Kaplan IR, Moore C (1970) Evidence for extraterrestrial amino-acids and hydrocarbons in Murchison meteorite. Nature 228:923–926PubMedCrossRefGoogle Scholar
  41. Lawless JG, Yuen GU (1979) Quantification of monocarboxylic acids in the Murchison carbonaceous meteorite. Nature 282:396–398CrossRefGoogle Scholar
  42. Lenski RE, Ofria C, Collier TC, Adami C (1999) Genome complexity, robustness and genetic interactions in digital organisms. Nature 400:661–664PubMedCrossRefGoogle Scholar
  43. Lenski RE, Ofria C, Pennock RT, Adami C (2003) The evolutionary origin of complex features. Nature 423:139–144PubMedCrossRefGoogle Scholar
  44. Lerner NR, Peterson E, Chang S (1993) The strecker synthesis as a source of amino-acids in carbonaceous chondrites—deuterium retention during synthesis. Geochim Cosmochim Acta 57:4713–4723PubMedCrossRefGoogle Scholar
  45. Lovelock JE (1965) A physical basis for life detection experiments. Nature 207:568–570PubMedCrossRefGoogle Scholar
  46. McCollom TM, Ritter G, Simoneit BRT (1999) Lipid synthesis under hydrothermal conditions by fischer-tropsh-type reactions. Orig Life Evol Biosph 29:153–166PubMedCrossRefGoogle Scholar
  47. McDonald GD, Khare BN, Thompson WR, Sagan C (1991) CH4/NH3/H2O spark tholin—chemical-analysis and interaction with jovian aqueous clouds. Icarus 94:354–367PubMedCrossRefGoogle Scholar
  48. McDonald GD, Thompson WR, Heinrich M, Khare BN, Sagan C (1994) Chemical investigation of Titan and Triton tholins. Icarus 108:137–145PubMedCrossRefGoogle Scholar
  49. McKay CP (2002) Planetary protection for a europa surface sample return: the ice clipper mission. Adv Space Res 30:1601–1605CrossRefGoogle Scholar
  50. McKay CP (2004) What is life—and how do we search for it in other worlds? PLOS Biol 2:1260–1263CrossRefGoogle Scholar
  51. Miller SL (1953) A production of amino acids under possible primitive Earth conditions. Science 117:528–529PubMedCrossRefGoogle Scholar
  52. Miller SL (1955) Production of some organic compounds under possible primitive Earth conditions. J Am Chem Soc 77:2351–2361CrossRefGoogle Scholar
  53. Miller SL, Urey HC (1959) Organic compound synthesis on the primitive Earth. Science 130:245–251PubMedCrossRefGoogle Scholar
  54. Munoz-Caro GM, Meierhenrich UJ, Schutte WA, Barbier B, Segovia AA, Rosenbauer H, Thiemann WHP, Brack A, Greenberg JM (2002) Amino acids from ultraviolet irradiation of interstellar ice analogues. Nature 416:403–406PubMedCrossRefGoogle Scholar
  55. Nagy B, Bitz SMC (1963) Long-chain fatty acids from the orgueil meteorite. Arch Biochem Biophys 101:240CrossRefGoogle Scholar
  56. Naraoka H, Shimoyama A, Harada K (1996) Molecular distribution of monocarboxylic acids in asuka carbonaceous chondrites from antarctica. Orig Life Evol Biosph 29:187–201CrossRefGoogle Scholar
  57. Ofria C, Adami C, Collier TC (2002) Design of evolvable computer languages. IEEE Trans Evol Comput 6:420–424CrossRefGoogle Scholar
  58. Ofria C, Adami C, Collier TC (2003) Selective pressures on genomes in molecular evolution. J Theor Biol 222:477–483PubMedGoogle Scholar
  59. Ofria C, Wilke CO (2004) Avida: a software platform for research in computation evolutionary biology. Artif Life 10:191–229PubMedCrossRefGoogle Scholar
  60. Pace NR (2001) The universal nature of biochemistry. Proc Natl Acad Sci USA 98:805–808PubMedCrossRefGoogle Scholar
  61. Ray TS (1992) An approach to the synthesis of life. In: Langton CG, Farmer JD, Rasmussen S (eds) Artificial life II. Addison-Wesley, Redwood City, pp 371–408Google Scholar
  62. Ring D, Wolman Y, Miller SL, Friedmann N (1972) Prebiotic synthesis of hydrophobic and protein amino-acids. Proc Natl Acad Sci USA 69:765–768Google Scholar
  63. Rushdi AI, Simoneit BRT (2001) Lipid formation by aqueous fischer-tropsch-type synthesis over a temperature range of 100 to 400°C. Orig Life Evol Biosph 31:103–118PubMedCrossRefGoogle Scholar
  64. Schlesinger G, Miller SL (1986) Prebiotic syntheses of pantoic acid and the other components of coenzyme-a. Orig Life Evol Biosph 16:307–307CrossRefGoogle Scholar
  65. Schultes EA, Hraber PT, LaBean TH (1997) Global similarities in nucleotide base composition among disparate functional classes of single-stranded RNA imply adaptive evolutionary convergence. RNA 3:792–806PubMedGoogle Scholar
  66. Schultes EA, Hraber PT, LaBean TH (1999) Estimating the contributions of selection and self-organization in rna secondary structure. J Mol Evol 49:76–83PubMedCrossRefGoogle Scholar
  67. Shapiro R SMD (2009) The search for alien life in our solar system: Strategies and priorities. Astrobiology 9:335–343PubMedCrossRefGoogle Scholar
  68. Shimoyama A, Ponnamperuma C, Yanai K (1979) Amino-acids in the Yamato carbonaceous chondrite from Antarctica. Nature 282:394–396CrossRefGoogle Scholar
  69. Shimoyama A, Naraoka H, Yamamoto H, Harada K (1986) Carboxylic acids in the Yamato-791198 carbonaceous chondrites from antarctica. Chem Lett 15:1561–1564CrossRefGoogle Scholar
  70. Shimoyama A, Komiya M, Harada K (1991) Low-molecular-weight monocarboxylic acids and gamma-lactones in neogene sediments of the shinjo basin. Geochem J 25:421–428Google Scholar
  71. Smith JM (1992) Evolutionary biology—byte-sized evolution. Nature 355:772–773PubMedCrossRefGoogle Scholar
  72. Shimoyama A, Ikeda H, Nomoto S, Harada K (1994) Formation of carboxylic-acids from elemental carbon and water by arc-discharge experiments. Bull Chem Soc Jpn 67:257–259CrossRefGoogle Scholar
  73. Sugisaki R, Mimura K (1994) Mantle hydrocarbons—abiotic or biotic. Geochim Cosmochim Acta 58:2527–2542PubMedCrossRefGoogle Scholar
  74. Summons R, Albrech P, McDonald G, Moldowan J (2008) Molecular biosignatures. Space Science Reviews 135:133–159CrossRefGoogle Scholar
  75. Sundh I, Nilsson M, Borga P (1997) Variation in microbial community structure in two boreal peatlands as determined by analysis of phospholipid fatty acid profiles. Appl Environ Microbiol 63:1476–1482PubMedGoogle Scholar
  76. Takano Y, Ohashi A, Kaneko T, Kobayashi K (2004) Abiotic synthesis of high-molecular-weight organics from an inorganic gas mixture of carbon monoxide, ammonia, and water by 3 mev proton irradiation. Appl Phys Lett 84:1410–1412CrossRefGoogle Scholar
  77. Wakeham SG (1999) Monocarboxylic, dicarboxylic and hydroxy acids released by sequential treatments of suspended particles and sediments of the black sea. Org Geochem 30:1059–1074CrossRefGoogle Scholar
  78. Wang XS, Poinar HN, Poinar GO, Bada JL (1995) Amino acids in the amber matrix and in entombed insects. In: Anderson KB, Crelling JC (eds) Amber, resinite, and fossil resins, American Chemical Society, Washington, vol 617 of ACS symposium series, pp 255–262Google Scholar
  79. White DC, Ringelberg DB, Macnaughton SJ, Alugupalli S, Schram D (1997) Signature lipid biomarker analysis for quantitative assessment in situ of environmental microbial ecology. In: Molecular markers in environmental geochemistry, American Chemical Society, vol 671 of ACS symposium series, pp 22–34Google Scholar
  80. Wilke CO, Adami C (2002) The biology of digital organisms. Trends Ecol Evol 17:528–532CrossRefGoogle Scholar
  81. Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C (2001) Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412:331–333PubMedCrossRefGoogle Scholar
  82. Yedid G, Bell G (2001) Microevolution in an electronic microcosm. Am Nat 157:465–487PubMedCrossRefGoogle Scholar
  83. Yuen GU, Lawless JG, Edelson EH (1981) Quantification of monocarboxylic acids from a spark discharge synthesis. J Mol Evol 17:43–47CrossRefGoogle Scholar
  84. Zelles L, Bai QY (1994) Fatty-acid patterns of phospholipids and lipopolysaccharides in environmental samples. Chemosphere 28:391–411CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Evan D. Dorn
    • 1
  • Kenneth H. Nealson
    • 2
  • Christoph Adami
    • 3
    • 4
    Email author
  1. 1.Digital Life Laboratory 136-93California Institute of TechnologyPasadenaUSA
  2. 2.Department of Earth SciencesUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Keck Graduate Institute of Applied Life ScienceClaremontUSA
  4. 4.BEACON Center for Evolution in Action, Michigan State UniversityEast LansingUSA

Personalised recommendations