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Yoshiya J. Matsubara

Publications and source records attributed to Yoshiya J. Matsubara.

6 recordsLinked to original sources

Conditions for Darwinian evolution in compartmentalized autocatalytic reaction networks

The first forms of life likely consisted of protocells endowed with metabolism, growth, and division. Such systems may have evolved due to variation and heredity in their chemical composition, even before the advent of genetics. However, whether compositional heredity is robust enough to sustain evolution by natural selection remains unknown, especially given that early compartmentalization cycles were likely imperfect, potentially disrupting stable inheritance across generations. Here, we show that multistable autocatalytic reaction networks can maintain heritable compositional states across a broad class of growth-division regimes, including continuous, serial, symmetric division, and multi-fragmentation cycles. We further identify parameter domains that preserve stable inheritance in the presence of stochastic variation, such that selection can operate efficiently. We finally demonstrate rudimentary forms of evolution by natural selection in populations of protocells with two heritable states, which we illustrate in an experimentally feasible setting. Our findings establish conditions for natural selection in compartmentalized autocatalytic systems and set the stage for understanding the minimal requirements for open-ended evolution.

physics.bio-ph↗

Suppression of errors in collectively coded information

Modern life largely transmits genetic information from mother to daughter through the duplication of single physically intact molecules that encode information. However, copying an extended molecule requires complex copying machinery and high fidelity that scales with the genome size to avoid the error catastrophe. Here, we explore these fidelity requirements in an alternative architecture, the virtual circular genome, in which no one physical molecule encodes the full genetic information. Instead, information is encoded and transmitted in a collective of overlapping and interacting segments. Using a model experimental system of a complex mixture of DNA oligomers that can partly anneal and extend off each other, we find that mutant oligomers are suppressed relative to a model without collective encoding. Through simulations and theory, we show that this suppression of mutants can be explained by competition for productive binding partners. As a consequence, information can be propagated robustly in a virtual circular genome even at mutation rates expected under prebiotic conditions.

q-bio.PE↗

Error Catastrophe Can Be Avoided by Proofreading Innate to Template-Directed Polymerization

An important issue for the origins of life is ensuring the accurate maintenance of information in replicating polymers in the face of inevitable errors. Here, we investigated how this maintenance depends on reaction kinetics by incorporating the elementary steps of polymerization into the population dynamics of polymers. We found that template-directed polymerization entails an inherent error-correction mechanism akin to kinetic proofreading, generating long polymers that are more tolerant to an error catastrophe. Because this mechanism does not require enzymes, it is likely to operate under broad prebiotic conditions.

physics.bio-ph↗

Horizontal transfer between loose compartments stabilizes replication of fragmented ribozymes

The emergence of replicases that can replicate themselves is a central issue in the origin of life. Recent experiments suggest that such replicases can be realized if an RNA polymerase ribozyme is divided into fragments short enough to be replicable by the ribozyme and if these fragments self-assemble into a functional ribozyme. However, the continued self-replication of such replicases requires that the production of every essential fragment be balanced and sustained. Here, we use mathematical modeling to investigate whether and under what conditions fragmented replicases achieve continued self-replication. We first show that under a simple batch condition, the replicases fail to display continued self-replication owing to positive feedback inherent in these replicases. This positive feedback inevitably biases replication toward a subset of fragments, so that the replicases eventually fail to sustain the production of all essential fragments. We then show that this inherent instability can be resolved by small rates of random content exchange between loose compartments (i.e., horizontal transfer). In this case, the balanced production of all fragments is achieved through negative frequency-dependent selection operating in the population dynamics of compartments. This selection mechanism arises from an interaction mediated by horizontal transfer between intracellular and intercellular symmetry breaking. The horizontal transfer also ensures the presence of all essential fragments in each compartment, sustaining self-replication. Taken together, our results underline compartmentalization and horizontal transfer in the origin of the first self-replicating replicases.

q-bio.CB↗

Optimal size for emergence of self-replicating polymer system

A biological system consists of a variety of polymers that are synthesized from monomers, by catalysis that exists only for some long polymers. It is important to elucidate the emergence and sustenance of such autocatalytic polymerization. We analyze here the stochastic polymerization reaction dynamics, to investigate the transition time from a state with almost no catalysts to a state with sufficient catalysts. We found an optimal volume that minimizes this transition time, which agrees with the inverse of the catalyst concentration at the unstable fixed point that separates the two states, as is theoretically explained. Relevance to the origin of life is also discussed.

physics.chem-ph↗

Kinetic Selection of Template Polymer with Complex Sequences

Emergence and maintenance of polymers with complex sequences is a major question in the study of origins of life. To answer this, we studied a model polymerization reaction, where polymers are synthesized by stepwise ligation from two types of monomers, catalyzed by a long polymer as a template. Direct stochastic simulation and dynamical systems analysis revealed that the most dominant polymer sequence in a population successively changes against the flow rate of monomer to the system. The slower the flow, the more is the complex sequence selected. We discuss the relevance of this kinetic selection of sequence by the non-equilibrium flow rate to the origin of complex polymers.

physics.bio-ph↗