Advertisement

Biological Theory

, Volume 14, Issue 4, pp 224–246 | Cite as

A History of Autocatalytic Sets

A Tribute to Stuart Kauffman
  • Wim HordijkEmail author
Historical Essay

Abstract

This year we celebrated Stuart Kauffman’s 80th birthday. Kauffman has contributed many original ideas to science. One of them is that of autocatalytic sets in the context of the origin of life. An autocatalytic set is a self-sustaining chemical reaction network in which all the molecules mutually catalyze each other’s formation from a basic food source. This notion is often seen as a “counterargument” against the dominant genetics-first view of the origin of life, focusing more on metabolism instead. The original notion was introduced back in 1971, but it has taken several decades for this idea to really catch on. Thanks to theoretical as well as experimental progress in more recent research on autocatalytic sets, especially over the past 15 years, the idea now seems to be gaining significant interest and support. In this tribute to Kauffman’s work and ideas, a brief history of research on autocatalytic sets is presented.

Keywords

Autocatalytic sets Stuart Kauffman Origin of life 

Notes

Acknowledgments

I would like to thank the Konrad Lorenz Institute for Evolution and Cognition Research (Klosterneuburg, Austria) and the European Union’s Horizon 2020 ATTRACT program for financial support, Mike Steel for the longstanding and highly productive collaboration (and for commenting on an earlier version of this manuscript), and Stuart Kauffman for being a friend, colleague, and mentor.

Compliance with Ethical Standards

Conflict of interest

The author explicitly and intentionally declares a conflict of interest with the RNA world hypothesis for the origin of life.

References

  1. Ameta S, Arsène S, Foulon S, Saudemont B, Clifton BE, Griffiths AD, Nghe P (2019) Darwinian properties and their trade-offs in autocatalytic RNA networks. bioRxiv.  https://doi.org/10.1101/726497 CrossRefGoogle Scholar
  2. Arsène S, Ameta S, Lehman N, Griffiths AD, Nghe P (2018) Coupled catabolism and anabolism in autocatalytic RNA sets. Nucleic Acids Res 46(18):9660–9666Google Scholar
  3. Ashkenasy G, Jegasia R, Yadav M, Ghadiri MR (2004) Design of a directed molecular network. PNAS 101(30):10872–10877Google Scholar
  4. Bagley RJ (1990) The functional self-organization of autocatalytic networks in a model of the evolution of biogenesis. PhD thesis, University of California, San DiegoGoogle Scholar
  5. 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, Boston, pp 93–140Google Scholar
  6. 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, Boston, pp 141–158Google Scholar
  7. Cazzolla Gatti R, Hordijk W, Kauffman S (2017) Biodiversity is autocatalytic. Ecol Model 346:70–76Google Scholar
  8. Cazzolla Gatti R, Fath B, Hordijk W, Kauffman S, Ulanowicz R (2018) Niche emergence as an autocatalytic process in the evolution of ecosystems. J Theor Biol 454:110–117Google Scholar
  9. COOLscience Club (2019) The origin and early evolution of life (2019) https://coolscience.club. Accessed 22 Sept 2019
  10. Damer B, Deamer DW (2015) Coupled phases and combinatorial selection in fluctuating hydrothermal pools: a scenario to guide experimental approaches to the origin of cellular life. Life 5:872–887Google Scholar
  11. Darzi Y, Letunic I, Bork P, Yamada T (2018) iPath3.0: interactive pathways explorer v3. Nucleic Acids Res 46:W510–W513Google Scholar
  12. Deamer DW (2019) Assembling life: how can life begin on earth and other habitable planets? Oxford University Press, OxfordGoogle Scholar
  13. Dittrich P, Speroni di Fenizio P (2007) Chemical organization theory. Bull Math Biol 69(4):1199–1231Google Scholar
  14. Dyson FJ (1982) A model for the origin of life. J Mol Evol 18:344–350Google Scholar
  15. Dyson FJ (1985) Origins of life. Cambridge University Press, CambridgeGoogle Scholar
  16. Eigen M (1971) Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58(10):465–523Google Scholar
  17. Eigen M (1992) Steps towards life. Oxford University Press, OxfordGoogle Scholar
  18. Eigen M, Schuster P (1979) The hypercycle: a principle of natural self-organization. Springer, BerlinGoogle Scholar
  19. Erdős P, Rényi A (1959) On random graphs. Publ Math 6:290–297Google Scholar
  20. Erdős P, Rényi A (1960) On the evolution of random graphs. Publ Math Inst Hung Acad Sci 5:17–61Google Scholar
  21. Farmer JD, Kauffman SA, Packard NH (1986) Autocatalytic replication of polymers. Physica D 22:50–67Google Scholar
  22. Fellermann H, Tanaka S, Rasmussen S (2017) Sequence selection by dynamical symmetry breaking in an autocatalytic binary polymer model. Phys Rev E 96:062407Google Scholar
  23. Filisetti A, Graudenzi A, Serra R, Villani M, De Lucrezia D, Fuchslin RM, Kauffman SA, Packard N, Poli I (2011) A stochastic model of the emergence of autocatalytic cycles. J Syst Chem 2:2Google Scholar
  24. Filisetti A, Villani M, Damiani C, Graudenzi A, Roli A, Hordijk W, Serra R (2014) On RAF sets and autocatalytic cycles in random reaction networks. Commun Comput Inf Sci 445:113–126Google Scholar
  25. Fontana W, Buss LW (1994a) The arrival of the fittest: toward a theory of biological organization. Bull Math Biol 56:1–64Google Scholar
  26. Fontana W, Buss LW (1994b) What would be conserved if the tape were played twice? PNAS 91:757–761Google Scholar
  27. Gabora L, Steel M (2017) Autocatalytic networks in cognition and the origin of culture. J Theor Biol 431:87–95Google Scholar
  28. Gilbert W (1986) The RNA world. Nature 319:618Google Scholar
  29. Gillespie DT (1976) A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J Comput Phys 22:403–434Google Scholar
  30. Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81(25):2340–2361Google Scholar
  31. Giri V, Jain S (2012) The origin of large molecules in primordial autocatalytic reaction networks. PLoS ONE 7(1):e29546Google Scholar
  32. Hanel R, Kauffman SA, Thurner S (2005) Phase transition in random catalytic networks. Phys Rev E 72:036117Google Scholar
  33. Hanel R, Kauffman SA, Thurner S (2007) Towards a physics of evolution: critical diversity dynamics at the edges of collapse and bursts of diversification. Phys Rev E 76:036110Google Scholar
  34. Hordijk W (2013) Autocatalytic sets: from the origin of life to the economy. BioScience 63(11):877–881Google Scholar
  35. Hordijk W (2016) Evolution of autocatalytic sets in computational models of chemical reaction networks. Orig Life Evol Biosph 46:233–245Google Scholar
  36. Hordijk W (2017) Autocatalytic confusion clarified. J Theor Biol 435:22–28Google Scholar
  37. Hordijk W, Steel M (2004) Detecting autocatalytic, self-sustaining sets in chemical reaction systems. J Theor Biol 227(4):451–461Google Scholar
  38. Hordijk W, Steel M (2013) A formal model of autocatalytic sets emerging in an RNA replicator system. J Syst Chem 4:3Google Scholar
  39. Hordijk W, Steel M (2014) Conditions for evolvability of autocatalytic sets: a formal example and analysis. Orig Life Evol Biosph 44(2):111–124Google Scholar
  40. Hordijk W, Steel M (2015) Autocatalytic sets and boundaries. J Syst Chem 6:1Google Scholar
  41. Hordijk W, Steel M (2016) Autocatalytic sets in polymer networks with variable catalysis distributions. J Math Chem 54(10):1997–2021Google Scholar
  42. Hordijk W, Steel M (2017) Chasing the tail: the emergence of autocatalytic networks. BioSystems 152:1–10Google Scholar
  43. Hordijk W, Kauffman SA, Steel M (2011) Required levels of catalysis for emergence of autocatalytic sets in models of chemical reaction systems. Int J Mol Sci 12(5):3085–3101Google Scholar
  44. Hordijk W, Steel M, Kauffman S (2012) The structure of autocatalytic sets: evolvability, enablement, and emergence. Acta Biotheor 60(4):379–392Google Scholar
  45. Hordijk W, Vaidya N, Lehman N (2014a) Serial transfer can aid the evolution of autocatalytic sets. J Syst Chem 5:4Google Scholar
  46. Hordijk W, Wills PR, Steel M (2014b) Autocatalytic sets and biological specificity. Bull Math Biol 76(1):201–224Google Scholar
  47. Hordijk W, Smith JI, Steel M (2015) Algorithms for detecting and analysing autocatalytic sets. Algorithms Mol Biol 10:15Google Scholar
  48. Hordijk W, Naylor J, Krasnogor N, Fellermann H (2018a) Population dynamics of autocatalytic sets in a compartmentalized spatial world. Life 8:33Google Scholar
  49. Hordijk W, Shichor S, Ashkenasy G (2018b) The influence of modularity, seeding, and product inhibition on peptide autocatalytic network dynamics. ChemPhysChem 19:2437–2444Google Scholar
  50. Hordijk W, Steel M, Dittrich P (2018c) Autocatalytic sets and chemical organizations: modeling self-sustaining reaction networks at the origin of life. New J Phys 20:015011Google Scholar
  51. Hordijk W, Steel M, Kauffman SA (2019) Molecular diversity required for the formation of autocatalytic sets. Life 9:23Google Scholar
  52. Jain S, Krishna S (1998) Autocatalytic sets and the growth of complexity in an evolutionary model. Phys Rev Lett 81(25):5684–5687Google Scholar
  53. Jain S, Krishna S (2001) A model for the emergence of cooperation, interdependence, and structure in evolving networks. PNAS 98(2):543–547Google Scholar
  54. Jain S, Krishna S (2002) Large extinctions in an evolutionary model: The role of innovation and keystone species. PNAS 99(4):2055–2060Google Scholar
  55. Jaramillo S, Honorato-Zimmer R, Pereira U, Contreras D, Reynaert B, Hernández V, Soto-Andrade J, Cárdenas ML, Cornish-Bowden A, Letelier JC (2010) (M, R) systems and RAF sets: common ideas, tools and projections. In: Proceedings of the ALife XII Conference, Odense, pp 94–100Google Scholar
  56. Kauffman SA (1971) Cellular homeostasis, epigenesis and replication in randomly aggregated macromolecular systems. J Cybern 1(1):71–96Google Scholar
  57. Kauffman SA (1986) Autocatalytic sets of proteins. J Theor Biol 119:1–24Google Scholar
  58. Kauffman SA (1993) The origins of order. Oxford University Press, OxfordGoogle Scholar
  59. Kauffman SA (1995) At home in the universe. Oxford University Press, OxfordGoogle Scholar
  60. Kauffman SA (2011) Economics and the collectively autocatalytic structure of the real economy. NPR 137 blog (21 November)Google Scholar
  61. Kauffman SA (2019) A world beyond physics. Oxford University Press, OxfordGoogle Scholar
  62. Kim DE, Joyce GF (2004) Cross-catalytic replication of an RNA ligase ribozyme. Chem Biol 11:1505–1512Google Scholar
  63. Lancet D, Zidovetzki R, Markovitch O (2018) Systems protobiology: origin of life in lipid catalytic networks. J R Soc Interface 15:20180159Google Scholar
  64. Lifson S (1997) On the crucial stages in the origin of animate matter. J Mol Evol 44:1–8Google Scholar
  65. Lincoln TA, Joyce GE (2009) Self-sustained replication of an RNA enzyme. Science 323:1229–1232Google Scholar
  66. Luisi PL (2003) Autopoiesis: a review and a reappraisal. Naturwissenschaften 90:49–59Google Scholar
  67. Martin WF, Russell MJ (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Philos Trans R Soc B 362:1887–1925Google Scholar
  68. Miras HN, Mathis C, Xuan W, Long DL, Pow R, Cronin L (2019) Spontaneous formation of autocatalytic sets with self-replicating inorganic metal oxide clusters. ChemRxiv.  https://doi.org/10.26434/chemrxiv.9598442.v1 CrossRefGoogle Scholar
  69. Mossel E, Steel M (2005) Random biochemical networks: the probability of self-sustaining autocatalysis. J Theor Biol 233(3):327–336Google Scholar
  70. Naylor J, Fellermann H, Ding Y, Mohammed WK, Jakubovics NS, Mukherjee J, Biggs CA, Wright PC, Krasnogor N (2017) Simbiotics: a multiscale integrative platform for 3D modeling of bacterial populations. ACS Synth Biol 6(7):1194–1210Google Scholar
  71. Nghe P, Hordijk W, Kauffman SA, Walker SI, Schmidt FJ, Kemble H, Yeates JAM, Lehman N (2015) Prebiotic network evolution: six key parameters. Mol BioSystems 11:3206–3217Google Scholar
  72. Patzke V, von Kiedrowski G (2007) Self replicating systems. Arkivoc 2007(5):293–310Google Scholar
  73. Piedrafita G, Monnard PA, Mavelli F, Ruiz-Mirazo K (2017) Permeability-driven selection in a semi-empirical protocell model: the roots of prebiotic systems evolution. Sci Rep 7:3141Google Scholar
  74. Rosen R (1991) Life itself. Columbia University Press, New YorkGoogle Scholar
  75. Segré D, Lancet D, Kedem O, Pilpel Y (1998a) Graded autocatalysis replication domain (GARD): kinetic analysis of self-replication in mutually catalytic sets. Orig Life Evol Biosph 28:501–514Google Scholar
  76. Segré D, Pilpel Y, Lancet D (1998b) Mutual catalysis in sets of prebiotic organic molecules: evolution through computer simulated chemical kinetics. Physica A 249:558–564Google Scholar
  77. Serra R, Villani M (2017) Modelling protocells. Springer, BerlinGoogle Scholar
  78. Serra R, Villani M (2019) Sustainable growth and synchronization in protocell models. Life 9(3):68Google Scholar
  79. Serra R, Filisetti A, Villani M, Graudenzi A, Damiani C, Panini T (2014) A stochastic model of catalytic reaction networks in protocells. Nat Comput 13(3):367–377Google Scholar
  80. Sievers D, von Kiedrowski G (1994) Self-replication of complementary nucleotide-based oligomers. Nature 369:221–224Google Scholar
  81. Sousa FL, Hordijk W, Steel M, Martin WF (2015) Autocatalytic sets in E. coli metabolism. J Syst Chem 6:4Google Scholar
  82. Stadler PF, Fontana W, Miller JH (1993) Random catalytic reaction networks. Physica D 63:378–392Google Scholar
  83. Steel M (2000) The emergence of a self-catalysing structure in abstract origin-of-life models. Appl Math Lett 3:91–95Google Scholar
  84. Steel M, Hordijk W, Smith J (2013) Minimal autocatalytic networks. J Theor Biol 332:96–107Google Scholar
  85. Szathmáry E (2013) On the propagation of a conceptual error concerning hypercycles and cooperation. J Syst Chem 4:1Google Scholar
  86. Tanaka S, Fellermann H, Rasmussen S (2014) Structure and selection in an autocatalytic binary polymer model. EPL 107:28004Google Scholar
  87. Vaidya N, Manapat ML, Chen IA, Xulvi-Brunet R, Hayden EJ, Lehman N (2012) Spontaneous network formation among cooperative RNA replicators. Nature 491:72–77Google Scholar
  88. Vasas V, Szathmáry E, Santos M (2010) Lack of evolvability in self-sustaining autocatalytic networks constraints metabolism-first scenarios for the origin of life. PNAS 107(4):1470–1475Google Scholar
  89. Vasas V, Fernando C, Santos M, Kauffman S, Sathmáry E (2012) Evolution before genes. Biol Direct 7:1Google Scholar
  90. Villani M, Filisetti A, Graudenzi A, Damiani C, Carletti T, Serra R (2014) Growth and division in a dynamic protocell model. Life 4:837–864Google Scholar
  91. Wills P, Henderson L (1997) Self-organisation and information-carrying capacity of collectively autocatalytic sets of polymers: ligation systems. In: Bar-Yam Y (ed) Proceedings of the International Conference on Complex Systems, New England Complex Systems Institute, NashuaGoogle Scholar
  92. Wills P, 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, vol 1. Westview Press, Boulder, pp 613–623Google Scholar
  93. Xavier JC, Hordijk W, Kauffman SA, Steel M, Martin WF (2019) Autocatalytic chemical networks preceded proteins and RNA in evolution. bioRxiv.  https://doi.org/10.1101/693879 CrossRefGoogle Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2019

Authors and Affiliations

  1. 1.Konrad Lorenz Institute for Evolution and Cognition ResearchKlosterneuburgAustria

Personalised recommendations