Trimetaphosphate Activates Prebiotic Peptide Synthesis across a Wide Range of Temperature and pH

Abstract

The biochemical activation of amino acids by adenosine triphosphate (ATP) drives the synthesis of proteins that are essential for all life. On the early Earth, before the emergence of cellular life, the chemical condensation of amino acids to form prebiotic peptides or proteins may have been activated by inorganic polyphosphates, such as tri metaphosphate (TP). Plausible volcanic and other potential sources of TP are known, and TP readily activates amino acids for peptide synthesis. But de novo peptide synthesis also depends on pH, temperature, and processes of solvent drying, which together define a varied range of potential activating conditions. Although we cannot replay the tape of life on Earth, we can examine how activator, temperature, acidity and other conditions may have collectively shaped its prebiotic evolution. Here, reactions of two simple amino acids, glycine and alanine, were tested, with or without TP, over a wide range of temperature (0–100 °C) and acidity (pH 1–12), while open to the atmosphere. After 24 h, products were analyzed by HPLC and mass spectrometry. In the absence of TP, glycine and alanine readily formed peptides under harsh near-boiling temperatures, extremes of pH, and within dry solid residues. In the presence of TP, however, peptides arose over a much wider range of conditions, including ambient temperature, neutral pH, and in water. These results show how polyphosphates such as TP may have enabled the transition of peptide synthesis from harsh to mild early Earth environments, setting the stage for the emergence of more complex prebiotic chemistries.

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References

  1. Basiuk VA, Gromovoy TY, Golovaty VG, Glukhoy AM (1990) Mechanisms of amino acid polycondensation on silica and alumina surfaces. Orig Life Evol Biosph 20:483–498

    Article  Google Scholar 

  2. Bhunia S, Singh A, Ojhaa AK (2016) Un-catalyzed peptide bond formation between two monomers of glycine, alanine, serine, threonine, and aspartic acid in gas phase: a density functional theory study. Eur Phys J D 70

  3. Bird RB, Stewart WE, Lightfoot EN (1960) Transport phenomena. John Wiley and Sons, New York

    Google Scholar 

  4. Borsook H (1953) Peptide bond formation. In: Adv Protein Chem, vol 8. Elsevier, pp 127–174

  5. Eigen M (1971) Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523

    CAS  Article  Google Scholar 

  6. Fernandez-Garcia C, Coggins AJ, Powner MW (2017) A Chemist's perspective on the role of phosphorus at the origins of life. Life (Basel) 7. https://doi.org/10.3390/life7030031

    Article  Google Scholar 

  7. Ferris JP, Hill AR, Liu RH, Orgel LE (1996) Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381:59–61

    CAS  Article  Google Scholar 

  8. Fitz D, Jakschitz T, Rode BM (2008) The catalytic effect of L- and D-histidine on alanine and lysine peptide formation. J Inorg Biochem 102:2097–2102. https://doi.org/10.1016/j.jinorgbio.2008.07.010

    CAS  Article  PubMed  Google Scholar 

  9. Forsythe JG, Yu SS, Mamajanov I, Grover MA, Krishnamurthy R, Fernandez FM, Hud NV (2015) Ester-mediated amide bond formation driven by wet-dry cycles: a possible path to polypeptides on the prebiotic earth. Angew Chem Int Ed Engl 54:9871–9875. https://doi.org/10.1002/anie.201503792

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Forsythe JG, Petrov AS, Millar WC, Yu SS, Krishnamurthy R, Grover MA, Hud NV, Fernández FM (2017) Surveying the sequence diversity of model prebiotic peptides by mass spectrometry. Proc Natl Acad Sci U S A 114:E7652–E7659. https://doi.org/10.1073/pnas.1711631114

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Gallego I, Grover MA, Hud NV (2015) Folding and imaging of DNA nanostructures in anhydrous and hydrated deep-eutectic solvents. Angew Chem Int Ed Engl 54:6765–6769. https://doi.org/10.1002/anie.201412354

    CAS  Article  PubMed  Google Scholar 

  12. Gánti T (2003) The principles of life. Oxford University Press

  13. Gao X, Deng H, Tang G, Liu Y, Xu P, Zhao Y (2011) Intermolecular phosphoryl transfer of N-phosphoryl amino acids. Eur J Org Chem 2011(17):3220–3228

    Article  Google Scholar 

  14. Gibard C, Bhowmik S, Karki M, Kim E-K, Krishnamurthy R (2018) Phosphorylation, oligomerization and self-assembly in water under potential prebiotic conditions. Nat Chem 10:212

    CAS  Article  Google Scholar 

  15. Huber C, Wächtershäuser G (1998) Peptides by activation of amino acids with CO on (Ni,Fe)S surfaces: implications for the origin of life. Science 281:670–672

    CAS  Article  Google Scholar 

  16. Hulshof J, Ponnamperuma C (1976) Prebiotic condensation reactions in an aqueous medium: a review of condensing agents. Orig Life 7:197–124

    CAS  Article  Google Scholar 

  17. Imai E, Honda H, Hatori K, Matsuno K (1999) Autocatalytic synthesis of Oligoglycine in a simulated submarine hydrothermal system. Orig Life Evol Biosph 29:249–259

    CAS  Article  Google Scholar 

  18. Kauffman SA (1986) Autocatalytic sets of proteins. J Theor Biol 119:1–24

    CAS  Article  Google Scholar 

  19. Kauffman SA (1993) The origins of order: self-organization and selection in evolution. Oxford University Press, Oxford

    Google Scholar 

  20. Kitadai N, Maruyama S (2017) Origins of building blocks of life: a review. Geosci Front 9:1117–1153

    Article  Google Scholar 

  21. Kura G, Nakashima T, Oshima F (1987) Study of the acidic hydrolysis of cyclic trimetaphosphate by liquid chromatography. J Chromatogr A 219:385–391

    Article  Google Scholar 

  22. Lahav N, White D, Chang S (1978) Peptide formation in the prebiotic era: thermal condensation of Glycine in fluctuating clay environments. Science 201:67–69

    CAS  Article  Google Scholar 

  23. Lambert J-F (2008) Adsorption and polymerization of amino acids on mineral surfaces: a review. Orig Life Evol Biosph 38:211–242

    CAS  Article  Google Scholar 

  24. Lane N (2015) The vital question: energy, evolution, and the origins of complex life. W.W. In: Norton & company. New York, London

    Google Scholar 

  25. Lohrmann R, Ranganathan R, Sawai H, Orgel LE (1975) Prebiotic peptide-formation in the solid state. I. Reactions of benzoate ion and glycine with adenosine 5′-phosphorimidazolide. J Mol Evol 5:57–73

    CAS  Article  Google Scholar 

  26. Meyerhof O, Shatas R, Kaplan A (1953) Heat of hydrolysis of trimetaphosphate. Biochim Biophys Acta 12:121–127

    CAS  Article  Google Scholar 

  27. Napier J, Yin J (2006) Formation of peptides in the dry state. Peptides 27:607–610

    CAS  Article  Google Scholar 

  28. Osterberg R, Orgel L (1972) Polyphosphate and trimetaphosphate formation under potentially prebiotic conditions. J Mol Evol 1:241–248

    CAS  Article  Google Scholar 

  29. Pascal R, Pross A, Sutherland JD (2013) Towards an evolutionary theory of the origin of life based on kinetics and thermodynamics. Open Biol 3:130156. https://doi.org/10.1098/rsob.130156

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Pasek MA (2008) Rethinking early earth phosphorus geochemistry. Proc Natl Acad Sci U S A 105:853–858. https://doi.org/10.1073/pnas.0708205105

    Article  PubMed  PubMed Central  Google Scholar 

  31. Patel BH, Percivalle C, Ritson DJ, Duffy CD, Sutherland JD (2015) Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nat Chem 7:301–307

    CAS  Article  Google Scholar 

  32. Plankensteiner K, Righi A, Rode BM (2002) Glycine and diglycine as possible catalytic factors in the prebiotic evolution of peptides. Orig Life Evol Biosph 32:225–236

    CAS  Article  Google Scholar 

  33. Rabinowitz J (1970) Peptide and amide bond formation in aqueous solutions of cyclic and linear polyphosphates as a possible prebiotic process. Helv Chim Acta 53:1350–1355

    CAS  Article  Google Scholar 

  34. Rabinowitz J, Flores J, Kresbach R, Rogers G (1969) Peptide formation in the presence of linear or cyclic polyphosphates. Nature 224:795–796

    CAS  Article  Google Scholar 

  35. Rishpon J, O'Hara PJ, Lahav N, Lawless JG (1982) Interaction between ATP, metal ions, glycine, and several minerals. J Mol Evol 18:179–184

    CAS  Article  Google Scholar 

  36. Rode BM (1999) Peptides and the origin of life. Peptides 20:773–786

    CAS  Article  Google Scholar 

  37. Rode BM, Fitz D, Jakschitz T (2007) The first steps of chemical evolution towards the origin of life. Chem Biodivers 4:2674–2702. https://doi.org/10.1002/cbdv.200790220

    CAS  Article  PubMed  Google Scholar 

  38. Rodriguez-Garcia M, Surman AJ, Cooper GJ, Suarez-Marina I, Hosni Z, Lee MP, Cronin L (2015) Formation of oligopeptides in high yield under simple programmable conditions. Nat Commun 6:8385. https://doi.org/10.1038/ncomms9385

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Sakata K, Kitadai N, Yokoyama T (2010) Effects of pH and temperature on dimerization rate of glycine: evaluation of favorable environmental conditions for chemical evolution of life. Geochim Cosmochim Acta 74:6841–6851

    CAS  Article  Google Scholar 

  40. Sawai H, Lohrmann R, Orgel L (1975) Prebiotic peptide-formation in the solid state. J Mol Evol 6:165–184

    CAS  Article  Google Scholar 

  41. Schwendinger MG, Rode BM (1989) Possible role of copper and sodium-chloride in prebiotic evolution of peptides. Anal Sci 5:411–414

    CAS  Article  Google Scholar 

  42. Shimoyama A, Ogasawara R (2002) Dipeptides and diketopiperazines in the Yamato-791198 and Murchison carbonaceous chondrites. Orig Life Evol Biosph 32:165–179

    CAS  Article  Google Scholar 

  43. Sibilska IK, Chen B, Li L, Yin J (2017) Effects of Trimetaphosphate on abiotic formation and hydrolysis of peptides. Life (Basel) 7. https://doi.org/10.3390/life7040050

    Article  Google Scholar 

  44. Steen H, Mann M (2004) The ABC's (and XYZ's) of peptide sequencing. Nat Rev Mol Cell Biol 5:699–711. https://doi.org/10.1038/nrm1468

    CAS  Article  PubMed  Google Scholar 

  45. Weber A, Caroon J, Warden J, Lemmon R, Calvin M (1977) Simultaneous peptide and oligonucleotide formation in mixtures of amino acid, nucleoside triphosphate, imidazole, and magnesium ion. Biosystems 8:277–286

    CAS  Article  Google Scholar 

  46. Yamagata Y, Watanabe H, Saitoh M, Namba T (1991) Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature 352:516–519. https://doi.org/10.1038/352516a0

    CAS  Article  PubMed  Google Scholar 

  47. Ying J, Lin R, Xu P, Wu Y, Liu Y, Zhao Y (2018) Prebiotic formation of cyclic dipeptides under potentially early earth conditions. Sci Rep 8:936

    Article  Google Scholar 

  48. Zamaraev KI, Romannikov VN, Salganik RI, Wlassoff WA, Khramtsov VV (1997) Modelling of the prebiotic synthesis of oligopeptides: silicate catalysts help to overcome the critical stage. Orig Life Evol Biosph 27:325–337

    CAS  Article  Google Scholar 

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Acknowledgements

D. Baum, A. Donnelly, K. Schloss, and K. Vetsigian provided helpful discussions and feedback. This work was funded in part by the Vilas Distinguished Achievement Professorship (L.L. and J.Y.), the Office of the Vice Chancellor for Research and Graduate Education (L.L. and J.Y.), the Wisconsin Institute for Discovery (J.Y.), the Janis Apinis Professorship (L.L.) at the School of Pharmacy, all at the University of Wisconsin-Madison; a Robert Draper Technology Innovation Fund grant (L.L.), shared instrument grant (L.L.), and Accelerator Fund grant (J.Y.) from the Wisconsin Alumni Research Foundation (WARF); and grants R01DK071801 (L.L.), R01AI091646 (J.Y.), U19AI0104317 (J.Y.), and a shared instrument grant NCRR S10RR029531 (L.L.) for the Orbitrap instruments, from the U.S. National Institutes of Health.

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I.S. and J.Y. conceived the project and wrote the manuscript, Y.F. and L.L. contributed to the writing. Y.F. performed the MS/MS analyses. I.S. carried out the experiments, collected the data, and performed the analysis. All authors discussed the results and contributed to the manuscript.

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Correspondence to John Yin.

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The authors declare no competing financial interests exist.

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The data that support the findings of this study are available from J.Y. upon reasonable request.

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Sibilska, I., Feng, Y., Li, L. et al. Trimetaphosphate Activates Prebiotic Peptide Synthesis across a Wide Range of Temperature and pH. Orig Life Evol Biosph 48, 277–287 (2018). https://doi.org/10.1007/s11084-018-9564-7

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Keywords

  • Trimetaphosphate
  • Prebiotic
  • Alanine
  • Glycine
  • de novo peptides
  • Drying-induced condensation