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

Abstract

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.

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References

  1. Abelson PH (1965) Abiogenic synthesis in martian environment. Proc Natl Acad Sci USA 54:1490–1494

    PubMed  Article  CAS  Google Scholar 

  2. Abelson PH, Hare PE (1969) Recent amino acids in the gunflint chert. Carnegie Inst Wash Yearb 69:208–210

    Google Scholar 

  3. Adami C (1998) Introduction to artificial life. Springer, New York

    Google Scholar 

  4. Adami C (2006) Digital genetics: unravelling the genetic basis of evolution. Nat Rev Genet 7:109–118

    Google Scholar 

  5. Adami C, Ofria C, Collier TC (2000) Evolution of biological complexity. Proc Natl Acad Sci USA 97:4463–4468

    PubMed  Article  CAS  Google Scholar 

  6. Amend JP, Shock EL (1998) Energetics of amino acid synthesis in hydrothermal ecosystems. Science 281:1659–1662

    PubMed  Article  CAS  Google Scholar 

  7. Anders E, Hayatsu R, Studier MH (1973) Organic compounds in meteorites. Science 182:781–790

    PubMed  Article  CAS  Google 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 58:4026–4031

    PubMed  CAS  Google Scholar 

  9. Bell G (2001) Neutral macroecology. Science 293:2413–2418

    PubMed  Article  CAS  Google 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 32:143–163

    PubMed  Article  CAS  Google 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 19:1645–1655

    PubMed  CAS  Google Scholar 

  12. Chow SS, Wilke CO, Ofria C, Lenski RE, Adami C (2004) Adaptive radiation from resource competition in digital organisms. Science 305:84–86

    PubMed  Article  CAS  Google 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 25:211–225

    Article  CAS  Google 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 29:933–945

    Article  CAS  Google 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 56:1963–1978

    Article  CAS  Google Scholar 

  16. Cronin JR, Moore CB (1976) Amino-acids of Nogoya and Mokoia carbonaceous chondrites. Geochim Cosmochim Acta 40:853–857

    Article  CAS  Google Scholar 

  17. Cronin JR, Pizzarello S, Moore CB (1979) Amino-acids in an antarctic carbonaceous chondrite. Science 206:335–337

    PubMed  Article  CAS  Google Scholar 

  18. Cronin JR, Moore CB, Pizzarello S (1980) Amino-acids in six CM2 chondrites. Meteoritics 15:277–278

    Google 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 17:265–272

    PubMed  Article  CAS  Google 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 91–97

  21. Dauwe B, Middelburg JJ (1998) Amino acids and hexosamines as indicators of organic matter degradation state in north sea sediments. Limnol Oceanogr 43:782–798

    Article  CAS  Google Scholar 

  22. Davies PCW, Benner SA, Cleland CE, Lineweaver CH, McKay CP, Wolfe-Simon F (2009) Signatures of a shadow biosphere. Astrobiology 9:241–249

    PubMed  Article  Google 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, Knoxville

    Google 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 166:403–409

    Article  CAS  Google Scholar 

  25. Elster H, Emanuel G, Weiner S (1991) Amino acid racemization of fossil bone. J Archaeol Sci 18:605–617

    Article  Google Scholar 

  26. Engel MH, Macko SA (1997) Isotopic evidence for extraterrestrial non-racemic amino acids in the Murchison meteorite. Nature 389:265–268

    PubMed  Article  CAS  Google Scholar 

  27. Engel MH, Nagy B (1982) Distribution and enantiomeric composition of amino-acids in the Murchison meteorite. Nature 296:837–840

    Article  CAS  Google Scholar 

  28. Engel MH, Macko SA, Silfer JA (1990) Carbon isotope composition of individual amino-acids in the Murchison meteorite. Nature 348:47–49

    PubMed  Article  CAS  Google Scholar 

  29. Gebicki JM, Hicks M (1976) Preparation and properties of vesicles enclosed by fatty acid membranes. Chem Phys Lipids 16:142–160

    PubMed  Article  CAS  Google Scholar 

  30. Gorban AN, Zinovyev AY, Popova TG (2003) Seven clusters in genomic triplet distributions. In Silico Biol 3:471–482

    PubMed  CAS  Google Scholar 

  31. Hargreaves WR, Deamer DW (1978) Liposomes from ionic, single-chain amphiphiles. Biochemistry 17

  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 35:939–951

    Article  CAS  Google Scholar 

  33. Hedges JI, Oades JM (1997) Comparative organic geochemistries of soils and marine sediments. Org Geochem 27:319–361

    Article  CAS  Google 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 45:1449–1466

    Article  CAS  Google Scholar 

  35. Horsfall IM, Wolff GA (1997) Hydrolysable amino acids in sediments from the porcupine abyssal plain, northeast atlantic ocean. Org Geochem 26:311–320

    Article  CAS  Google 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 46:14–23

    Article  CAS  Google 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 62:1347–1364

    Article  CAS  Google Scholar 

  38. Khare BN, Sagan C, Ogino H, Nagy B, Er C, Schram KH, Arakawa ET (1986) Amino-acids derived from Titan tholins. Icarus 68:176–184

    PubMed  Article  CAS  Google Scholar 

  39. Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98

    Article  CAS  Google 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 228:923–926

    PubMed  Article  CAS  Google Scholar 

  41. Lawless JG, Yuen GU (1979) Quantification of monocarboxylic acids in the Murchison carbonaceous meteorite. Nature 282:396–398

    Article  CAS  Google Scholar 

  42. Lenski RE, Ofria C, Collier TC, Adami C (1999) Genome complexity, robustness and genetic interactions in digital organisms. Nature 400:661–664

    PubMed  Article  CAS  Google Scholar 

  43. Lenski RE, Ofria C, Pennock RT, Adami C (2003) The evolutionary origin of complex features. Nature 423:139–144

    PubMed  Article  CAS  Google 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 57:4713–4723

    PubMed  Article  CAS  Google Scholar 

  45. Lovelock JE (1965) A physical basis for life detection experiments. Nature 207:568–570

    PubMed  Article  CAS  Google Scholar 

  46. McCollom TM, Ritter G, Simoneit BRT (1999) Lipid synthesis under hydrothermal conditions by fischer-tropsh-type reactions. Orig Life Evol Biosph 29:153–166

    PubMed  Article  CAS  Google 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 94:354–367

    PubMed  Article  CAS  Google Scholar 

  48. McDonald GD, Thompson WR, Heinrich M, Khare BN, Sagan C (1994) Chemical investigation of Titan and Triton tholins. Icarus 108:137–145

    PubMed  Article  CAS  Google Scholar 

  49. McKay CP (2002) Planetary protection for a europa surface sample return: the ice clipper mission. Adv Space Res 30:1601–1605

    Article  Google Scholar 

  50. McKay CP (2004) What is life—and how do we search for it in other worlds? PLOS Biol 2:1260–1263

    Article  CAS  Google Scholar 

  51. Miller SL (1953) A production of amino acids under possible primitive Earth conditions. Science 117:528–529

    PubMed  Article  CAS  Google Scholar 

  52. Miller SL (1955) Production of some organic compounds under possible primitive Earth conditions. J Am Chem Soc 77:2351–2361

    Article  CAS  Google Scholar 

  53. Miller SL, Urey HC (1959) Organic compound synthesis on the primitive Earth. Science 130:245–251

    PubMed  Article  CAS  Google 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 416:403–406

    PubMed  Article  CAS  Google Scholar 

  55. Nagy B, Bitz SMC (1963) Long-chain fatty acids from the orgueil meteorite. Arch Biochem Biophys 101:240

    Article  CAS  Google Scholar 

  56. Naraoka H, Shimoyama A, Harada K (1996) Molecular distribution of monocarboxylic acids in asuka carbonaceous chondrites from antarctica. Orig Life Evol Biosph 29:187–201

    Article  Google Scholar 

  57. Ofria C, Adami C, Collier TC (2002) Design of evolvable computer languages. IEEE Trans Evol Comput 6:420–424

    Article  Google Scholar 

  58. Ofria C, Adami C, Collier TC (2003) Selective pressures on genomes in molecular evolution. J Theor Biol 222:477–483

    PubMed  CAS  Google Scholar 

  59. Ofria C, Wilke CO (2004) Avida: a software platform for research in computation evolutionary biology. Artif Life 10:191–229

    PubMed  Article  Google Scholar 

  60. Pace NR (2001) The universal nature of biochemistry. Proc Natl Acad Sci USA 98:805–808

    PubMed  Article  CAS  Google 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 371–408

    Google Scholar 

  62. Ring D, Wolman Y, Miller SL, Friedmann N (1972) Prebiotic synthesis of hydrophobic and protein amino-acids. Proc Natl Acad Sci USA 69:765–768

    Google 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 31:103–118

    PubMed  Article  CAS  Google Scholar 

  64. Schlesinger G, Miller SL (1986) Prebiotic syntheses of pantoic acid and the other components of coenzyme-a. Orig Life Evol Biosph 16:307–307

    Article  Google 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 3:792–806

    PubMed  CAS  Google Scholar 

  66. Schultes EA, Hraber PT, LaBean TH (1999) Estimating the contributions of selection and self-organization in rna secondary structure. J Mol Evol 49:76–83

    PubMed  Article  CAS  Google Scholar 

  67. Shapiro R SMD (2009) The search for alien life in our solar system: Strategies and priorities. Astrobiology 9:335–343

    PubMed  Article  Google Scholar 

  68. Shimoyama A, Ponnamperuma C, Yanai K (1979) Amino-acids in the Yamato carbonaceous chondrite from Antarctica. Nature 282:394–396

    Article  CAS  Google Scholar 

  69. Shimoyama A, Naraoka H, Yamamoto H, Harada K (1986) Carboxylic acids in the Yamato-791198 carbonaceous chondrites from antarctica. Chem Lett 15:1561–1564

    Article  Google 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 25:421–428

    CAS  Google Scholar 

  71. Smith JM (1992) Evolutionary biology—byte-sized evolution. Nature 355:772–773

    PubMed  Article  CAS  Google 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 67:257–259

    Article  CAS  Google Scholar 

  73. Sugisaki R, Mimura K (1994) Mantle hydrocarbons—abiotic or biotic. Geochim Cosmochim Acta 58:2527–2542

    PubMed  Article  CAS  Google Scholar 

  74. Summons R, Albrech P, McDonald G, Moldowan J (2008) Molecular biosignatures. Space Science Reviews 135:133–159

    Article  CAS  Google 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 63:1476–1482

    PubMed  CAS  Google 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 84:1410–1412

    Article  CAS  Google 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 30:1059–1074

    Article  CAS  Google 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 255–262

  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 22–34

  80. Wilke CO, Adami C (2002) The biology of digital organisms. Trends Ecol Evol 17:528–532

    Article  Google 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 412:331–333

    PubMed  Article  CAS  Google Scholar 

  82. Yedid G, Bell G (2001) Microevolution in an electronic microcosm. Am Nat 157:465–487

    PubMed  Article  CAS  Google Scholar 

  83. Yuen GU, Lawless JG, Edelson EH (1981) Quantification of monocarboxylic acids from a spark discharge synthesis. J Mol Evol 17:43–47

    Article  CAS  Google Scholar 

  84. Zelles L, Bai QY (1994) Fatty-acid patterns of phospholipids and lipopolysaccharides in environmental samples. Chemosphere 28:391–411

    Article  CAS  Google Scholar 

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Acknowledgments

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.

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Dorn, E.D., Nealson, K.H. & Adami, C. Monomer Abundance Distribution Patterns as a Universal Biosignature: Examples from Terrestrial and Digital Life. J Mol Evol 72, 283–295 (2011). https://doi.org/10.1007/s00239-011-9429-4

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Keywords

  • Artificial life
  • Amino acids
  • Carboxylic acids
  • Astrobiology
  • Exobiology
  • Evolution
  • Meteorites