Autocatalytic Sets and RNA Secondary Structure

Abstract

The dominant paradigm in origin of life research is that of an RNA world. However, despite experimental progress towards the spontaneous formation of RNA, the RNA world hypothesis still has its problems. Here, we introduce a novel computational model of chemical reaction networks based on RNA secondary structure and analyze the existence of autocatalytic sub-networks in random instances of this model, by combining two well-established computational tools. Our main results are that (i) autocatalytic sets are highly likely to exist, even for very small reaction networks and short RNA sequences, and (ii) sequence diversity seems to be a more important factor in the formation of autocatalytic sets than sequence length. These findings could shed new light on the probability of the spontaneous emergence of an RNA world as a network of mutually collaborative ribozymes.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Ashkenasy G, Jegasia R, Yadav M, Ghadiri MR (2004) Design of a directed molecular network. PNAS 101(30):10872–10877

  2. Bagley RJ, Farmer JD (1991) Spontaneous emergence of a metabolism. In: Langton CG, Taylor C, Farmer JD, Rasmussen S (eds) Artificial life II. Addison-Wesley, Redwood City, pp 93–140

  3. Bagley RJ, Farmer JD, Fontana W (1991) Evolution of a metabolism. In: Langton CG, Taylor C, Farmer JD, Rasmussen S (eds) Artificial life II. Addison-Wesley, pp 141–158

  4. Bartel DP, Szostak JW (1993) Isolation of new ribozymes from a large pool of random sequences. Science 261(5127):1411–1418

    CAS  Article  PubMed  Google Scholar 

  5. Benner SA, Kim HJ, Yang Z (2012) Setting the stage: the history, chemistry, and geobiology behind RNA. Cold Spring Harb Perspect Biol 4(a003):541

    Google Scholar 

  6. Farmer JD, Kauffman SA, Packard NH (1986) Autocatalytic replication of polymers. Phys D 22:50–67

    Article  Google Scholar 

  7. Filisetti A, Graudenzi A, Serra R, Villani M, Lucrezia DD, Füchslin RM, Kauffman SA, Packard N, Poli I (2011) A stochastic model of the emergence of autocatalytic cycles. J Syst Chem 2:2

    CAS  Article  Google Scholar 

  8. Gilbert W (1986) The RNA world. Nature 319:618

    Article  Google Scholar 

  9. Hayden EJ, Lehman N (2006) Self-assembly of a group I intron from inactive oligonucleotide fragments. Chem Biol 13:909–918

    CAS  Article  PubMed  Google Scholar 

  10. Higgs PG, Lehman N (2015) The RNA world: molecular cooperation at the origins of life. Nat Rev Genet 16:7–17

    CAS  Article  PubMed  Google Scholar 

  11. Hordijk W, Steel M (2004) Detecting autocatalytic, self-sustaining sets in chemical reaction systems. J Theor Biol 227(4):451–461

    CAS  Article  PubMed  Google Scholar 

  12. Hordijk W, Steel M (2013) A formal model of autocatalytic sets emerging in an RNA replicator system. J Syst Chem 4:3

    CAS  Article  Google Scholar 

  13. Hordijk W, Steel M (2014) Conditions for evolvability of autocatalytic sets: a formal example and analysis. Orig Life Evol Biosph 44(2):111–124

    CAS  Article  PubMed  Google Scholar 

  14. Hordijk W, Steel M (2017) Chasing the tail: the emergence of autocatalytic networks. BioSyst 152:1–10

    CAS  Article  Google Scholar 

  15. Hordijk W, Steel M, Kauffman S (2012) The structure of autocatalytic sets: evolvability, enablement, and emergence. Acta Biotheor 60(4):379–392

    Article  PubMed  Google Scholar 

  16. Hordijk W, Steel M, Kauffman S (2013) Autocatalytic sets: the origin of life, evolution, and functional organization. In: Pontarotti P (ed) Evolutionary biology: exobiology and evolutionary mechanisms. Springer, Berlin, pp 49–60

  17. Hordijk W, Vaidya N, Lehman N (2014) Serial transfer can aid the evolution of autocatalytic sets. J Syst Chem 5:4

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hordijk W, Smith JI, Steel M (2015) Algorithms for detecting and analysing autocatalytic sets. Algorithms Mol Biol 10:15

    Article  PubMed  PubMed Central  Google Scholar 

  19. Horning DP, Joyce GF (2016) Amplification of RNA by an RNA polymerase ribozyme. PNAS 113:9786–9791

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Jain S, Krishna S (2001) A model for the emergence of cooperation, interdependence, and structure in evolving networks. PNAS 98(2):543–547

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Jain S, Krishna S (2002) Large extinctions in an evolutionary model: The role of innovation and keystone species. PNAS 99(4):2055–2060

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Joyce GF (2002) The antiquity of RNA-based evolution. Nature 418:214–221

    CAS  Article  PubMed  Google Scholar 

  23. Kauffman SA (1971) Cellular homeostasis, epigenesis and replication in randomly aggregated macromolecular systems. J Cybernet 1(1):71–96

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  25. Kauffman SA (1993) The origins of order. Oxford University Press, New York

  26. Kim DE, Joyce GF (2004) Cross-catalytic replication of an RNA ligase ribozyme. Chem Biol 11:1505–1512

    CAS  Article  PubMed  Google Scholar 

  27. Li L, Francklyn C, Carter CW (2013) Aminoacylating urzymes challenge the RNA world hypothesis. J Biol Chem 288:26856–26863

  28. Lincoln TA, Joyce GE (2009) Self-sustained replication of an RNA enzyme. Science 323:1229–1232

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Lorenz R, Bernhart SH, Höner zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL (2011) ViennaRNA Package 2.0. Algorithms Mol Biol 6:26

  30. Mossel E, Steel M (2005) Random biochemical networks: the probability of self-sustaining autocatalysis. J Theor Biol 233(3):327–336

    CAS  Article  PubMed  Google Scholar 

  31. Nghe P, Hordijk W, Kauffman SA, Walker SI, Schmidt FJ, Kemble H, Yeates JAM, Lehman N (2015) Prebiotic network evolution: six key parameters. Mol BioSyst 11:3206–3217

    CAS  Article  PubMed  Google Scholar 

  32. Polyansky AA, Hlevnjak M, Zagrovic B (2013) Proteome-wide analysis reveals clues of complementary interactions between mRNAs and their cognate proteins as the physicochemical foundation of the genetic code. RNA Biol 10(8):1248–1254

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239–242

    CAS  Article  PubMed  Google Scholar 

  34. Sievers D, von Kiedrowski G (1994) Self-replication of complementary nucleotide-based oligomers. Nature 369:221–224

    CAS  Article  PubMed  Google Scholar 

  35. Smith J, Steel M, Hordijk W (2014) Autocatalytic sets in a partitioned biochemical network. J Syst Chem 5:2

    Article  PubMed  PubMed Central  Google Scholar 

  36. Sousa FL, Hordijk W, Steel M, Martin WF (2015) Autocatalytic sets in E. coli metabolism. J Syst Chem 6:4

    Article  PubMed  PubMed Central  Google Scholar 

  37. Steel M (2000) The emergence of a self-catalysing structure in abstract origin-of-life models. Appl Math Lett 3:91–95

    Article  Google Scholar 

  38. Szostak JW (2012) The eightfold path to non-enzymatic RNA replication. J Syst Chem 3:2

    CAS  Article  Google Scholar 

  39. Tanaka S, Fellermann H, Rasmussen S (2014) Structure and selection in an autocatalytic binary polymer model. EPL 107(28):004

    Google Scholar 

  40. Vaidya N, Manapat ML, Chen IA, Xulvi-Brunet R, Hayden EJ, Lehman N (2012) Spontaneous network formation among cooperative RNA replicators. Nature 491:72–77

    CAS  Article  PubMed  Google Scholar 

  41. Vasas V, Fernando C, Santos M, Kauffman S, Sathmáry E (2012) Evolution before genes. Biol Direct 7:1

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wills PR, Henderson L (2000) Self-organisation and information-carrying capacity of collectively autocatalytic sets of polymers: ligation systems. In: Bar-Yam Y (ed) Unifying themes in complex systems: proceedings of the first international conference on complex systems. Perseus Books, pp 613–623

Download references

Acknowledgements

The author thanks the KLI Klosterneuburg for financial support in the form of a fellowship, and two anonymous reviewers for helpful suggestions to improve the original manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Wim Hordijk.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hordijk, W. Autocatalytic Sets and RNA Secondary Structure. J Mol Evol 84, 153–158 (2017). https://doi.org/10.1007/s00239-017-9787-7

Download citation

Keywords

  • Origin of life
  • RNA world
  • Autocatalytic sets
  • RNA secondary structure