Excess Mutual Catalysis Is Required for Effective Evolvability

It is widely accepted that autocatalysis constitutes a crucial facet of effective replication and evolution (e.g., in Eigen's hypercycle model). Other models for early evolution (e.g., by Dyson, Gánti, Varela, and Kauffman) invoke catalytic networks, where cross-catalysis is more apparent. A key question is how the balance between auto- (self-) and cross- (mutual) catalysis shapes the behavior of model evolving systems. This is investigated using the graded autocatalysis replication domain (GARD) model, previously shown to capture essential features of reproduction, mutation, and evolution in compositional molecular assemblies. We have performed numerical simulations of an ensemble of GARD networks, each with a different set of lognormally distributed catalytic values. We asked what is the influence of the catalytic content of such networks on beneficial evolution. Importantly, a clear trend was observed, wherein only networks with high mutual catalysis propensity (pmc) allowed for an augmented diversity of composomes, quasi-stationary compositions that exhibit high replication fidelity. We have reexamined a recent analysis that showed meager selection in a single GARD instance and for a few nonstationary target compositions. In contrast, when we focused here on compotypes (clusters of composomes) as targets for selection in populations of compositional assemblies, appreciable selection response was observed for a large portion of the networks simulated. Further, stronger selection response was seen for high pmc values. Our simulations thus demonstrate that GARD can help analyze important facets of evolving systems, and indicate that excess mutual catalysis over self-catalysis is likely to be important for the emergence of molecular systems capable of evolutionlike behavior.

[1]  K. Kaneko Kinetic Origin of Heredity in a Replicating System with a Catalytic Network , 2002, Journal of biological physics.

[2]  Eric J. Hayden,et al.  Systems chemistry on ribozyme self-construction: evidence for anabolic autocatalysis in a recombination network. , 2008, Angewandte Chemie.

[3]  J. Brookfield Evolution and evolvability: celebrating Darwin 200 , 2009, Biology Letters.

[4]  Eörs Szathmáry,et al.  Lack of evolvability in self-sustaining autocatalytic networks constraints metabolism-first scenarios for the origin of life , 2010, Proceedings of the National Academy of Sciences.

[5]  F. Anet The place of metabolism in the origin of life. , 2004, Current opinion in chemical biology.

[6]  T. Gánti Organization of chemical reactions into dividing and metabolizing units: the chemotons. , 1975, Bio Systems.

[7]  D. Lancet,et al.  Compositional genomes: prebiotic information transfer in mutually catalytic noncovalent assemblies. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Higgs,et al.  Compositional Inheritance: Comparison of Self-assembly and Catalysis , 2008, Origins of Life and Evolution of Biospheres.

[9]  G. F. Joyce The antiquity of RNA-based evolution , 2002, Nature.

[10]  Irene A Chen,et al.  From self-assembled vesicles to protocells. , 2010, Cold Spring Harbor perspectives in biology.

[11]  D. Lancet,et al.  Mutations and Lethality in Simulated Prebiotic Networks , 2009, Journal of Molecular Evolution.

[12]  Peter F. Stadler,et al.  In Silico Evolution of Early Metabolism , 2011, Artificial Life.

[13]  Douglas Steinley,et al.  K-means clustering: a half-century synthesis. , 2006, The British journal of mathematical and statistical psychology.

[14]  Lipidia: An Artificial Chemistry of Self-Replicating Assemblies of Lipid-like Molecules , 2004 .

[15]  L W Buss,et al.  What would be conserved if "the tape were played twice"? , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[16]  B. Ganem RNA world , 1987, Nature.

[17]  L. Orgel,et al.  Prebiotic chemistry and the origin of the RNA world. , 2004, Critical reviews in biochemistry and molecular biology.

[18]  Keith J. Laidler The development of theories of catalysis , 1986 .

[19]  Y. Pilpel,et al.  Graded Autocatalysis Replication Domain (GARD): Kinetic Analysis of Self-Replication in Mutually Catalytic Sets , 1998, Origins of life and evolution of the biosphere.

[20]  P. Stadler,et al.  Dynamics of autocatalytic reaction networks. IV: Inhomogeneous replicator networks. , 1991, Bio Systems.

[21]  M. Bedau An Aristotelian account of minimal chemical life. , 2010, Astrobiology.

[22]  Moshe Sipper,et al.  Lipidia : An Artificial Chemistry of Self-Replicating Assemblies of Lipid-like Molecules , 2004 .

[23]  T. Gánti Biogenesis itself. , 1997, Journal of theoretical biology.

[24]  M. Eigen,et al.  The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. , 1977, Die Naturwissenschaften.

[25]  E. Szathmáry,et al.  A classification of replicators and lambda-calculus models of biological organization , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  D. Deamer,et al.  The Lipid World , 2001, Origins of life and evolution of the biosphere.

[27]  P. Luisi,et al.  Lipid vesicles as possible intermediates in the origin of life , 1999 .

[28]  Jacquelyn A. Thomas,et al.  The Influence of Environmental Conditions, Lipid Composition, and Phase Behavior on the Origin of Cell Membranes , 2007, Origins of Life and Evolution of Biospheres.

[29]  U. Alon Network motifs: theory and experimental approaches , 2007, Nature Reviews Genetics.

[30]  Robert Shapiro,et al.  A simpler origin for life. , 2007, Scientific American.

[31]  M. Pigliucci Is evolvability evolvable? , 2008, Nature Reviews Genetics.

[32]  Doron Lancet,et al.  Early Systems Biology and Prebiotic Networks , 2005, Trans. Comp. Sys. Biology.

[33]  E. Seidemann,et al.  Probability model for molecular recognition in biological receptor repertoires: significance to the olfactory system. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Gillespie,et al.  Master equations for random walks with arbitrary pausing time distributions , 1977 .

[35]  D. Lancet,et al.  Polymer Gard: Computer Simulation of Covalent Bond Formation in Reproducing Molecular Assemblies , 2005, Origins of Life and Evolution of Biospheres.

[36]  Freeman J. Dyson,et al.  A model for the origin of life , 2005, Journal of Molecular Evolution.

[37]  Yohei Yokobayashi,et al.  Emergence of symbiosis in peptide self-replication through a hypercyclic network , 1997, Nature.

[38]  H. Maturana,et al.  Autopoiesis: the organization of living systems, its characterization and a model. , 1974, Currents in modern biology.

[39]  Doron Lancet,et al.  Coevolution of compositional protocells and their environment , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  B. McMullin Remarks on Autocatalysis and Autopoiesis , 2000, Annals of the New York Academy of Sciences.

[41]  R. A. Hughes,et al.  The importance of prebiotic chemistry in the RNA world. , 2004, Current opinion in chemical biology.

[42]  M. Eigen,et al.  What is a quasispecies? , 2006, Current topics in microbiology and immunology.

[43]  Peter F. Stadler,et al.  Networks in molecular evolution , 2002 .

[44]  Steen Rasmussen,et al.  Protocells : bridging nonliving and living matter , 2008 .

[45]  L. Orgel,et al.  A Simpler Nucleic Acid , 2000, Science.

[46]  D. Lancet,et al.  Spontaneous chiral symmetry breaking in early molecular networks , 2010, Biology Direct.

[47]  Doron Lancet,et al.  Test of a statistical model for molecular recognition in biological repertoires. , 2002, Journal of theoretical biology.

[48]  D. Gillespie A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions , 1976 .

[49]  Eörs Szathmáry,et al.  Evolutionary Potential and Requirements for Minimal Protocells , 2005 .

[50]  John Maynard Smith,et al.  From replicators to reproducers: the first major transitions leading to life. , 1997, Journal of theoretical biology.

[51]  Stuart A. Kauffman,et al.  The origins of order , 1993 .

[52]  José F Fontanari,et al.  The information capacity of hypercycles. , 2008, Journal of theoretical biology.

[53]  Doron Lancet,et al.  Compositional complementarity and prebiotic ecology in the origin of life , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[54]  P. A. P. Moran,et al.  Random processes in genetics , 1958, Mathematical Proceedings of the Cambridge Philosophical Society.

[55]  Doron Lancet,et al.  Question 7: The First Units of Life Were Not Simple Cells , 2007, Origins of Life and Evolution of Biospheres.

[56]  D. Lancet,et al.  The molecular roots of compositional inheritance. , 2001, Journal of theoretical biology.

[57]  Ian S. Williams,et al.  Pb, U and Th diffusion in natural zircon , 1997, Nature.

[58]  Béla Barabás,et al.  Stochastic aspects of asymmetric autocatalysis and absolute asymmetric synthesis , 2010 .

[59]  U. Müller,et al.  Re-creating an RNA world , 2006, Cellular and Molecular Life Sciences CMLS.

[60]  W. Gilbert Origin of life: The RNA world , 1986, Nature.

[61]  D. Lancet,et al.  Emergence of order in small autocatalytic sets maintained far from equilibrium : application of a probabilistic receptor affinity distribution (RAD) model , 1994 .

[62]  S. Lifson,et al.  A model of prebiotic replication: survival of the fittest versus extinction of the unfittest. , 1999, Journal of theoretical biology.

[63]  W. Stahel,et al.  Log-normal Distributions across the Sciences: Keys and Clues , 2001 .

[64]  A. Weber Sugars as the Optimal Biosynthetic Carbon Substrate of Aqueous Life Throughout the Universe , 2000, Origins of life and evolution of the biosphere.

[65]  S. Lifson On the Crucial Stages in the Origin of Animate Matter , 1997, Journal of Molecular Evolution.

[66]  R. Shapiro Small Molecule Interactions were Central to the Origin of Life , 2006, The Quarterly Review of Biology.

[67]  Pier Luigi Luisi,et al.  Autocatalytic self-replicating micelles as models for prebiotic structures , 1992, Nature.