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      Replication of Simulated Prebiotic Amphiphilic Vesicles in a Finite Environment Exhibits Complex Behavior That Includes High Progeny Variability and Competition

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      1, , 2 , 3 , 2 ,
      Astrobiology
      Mary Ann Liebert, Inc.

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          Abstract

          We studied the simulated replication and growth of prebiotic vesicles composed of 140 phospholipids and cholesterol using our R-GARD (Real Graded Autocatalysis Replication Domain) formalism that utilizes currently extant lipids that have known rate constants of lipid-vesicle interactions from published experimental data. R-GARD normally modifies kinetic parameters of lipid-vesicle interactions based on vesicle composition and properties. Our original R-GARD model tracked the growth and division of one vesicle at a time in an environment with unlimited lipids at a constant concentration. We explore here a modified model where vesicles compete for a finite supply of lipids. We observed that vesicles exhibit complex behavior including initial fast unrestricted growth, followed by intervesicle competition for diminishing resources, then a second growth burst driven by better-adapted vesicles, and ending with a final steady state. Furthermore, in simulations without kinetic parameter modifications (“invariant kinetics”), the initial replication was an order of magnitude slower, and vesicles' composition variability at the final steady state was much lower. The complex kinetic behavior was not observed either in the previously published R-GARD simulations or in additional simulations presented here with only one lipid component. This demonstrates that both a finite environment (inducing selection) and multiple components (providing variation for selection to act upon) are crucial for portraying evolution-like behavior. Such properties can improve survival in a changing environment by increasing the ability of early protocellular entities to respond to rapid environmental fluctuations likely present during abiogenesis both on Earth and possibly on other planets. This in silico simulation predicts that a relatively simple in vitro chemical system containing only lipid molecules might exhibit properties that are relevant to prebiotic processes. Key Words: Phospholipid vesicles—Prebiotic compartments—Prebiotic vesicle competition—Prebiotic vesicle variability. Astrobiology 18, 419–430.

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          The antiquity of RNA-based evolution.

          All life that is known to exist on Earth today and all life for which there is evidence in the geological record seems to be of the same form--one based on DNA genomes and protein enzymes. Yet there are strong reasons to conclude that DNA- and protein-based life was preceded by a simpler life form based primarily on RNA. This earlier era is referred to as the 'RNA world', during which the genetic information resided in the sequence of RNA molecules and the phenotype derived from the catalytic properties of RNA.
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            Experimental models of primitive cellular compartments: encapsulation, growth, and division.

            The clay montmorillonite is known to catalyze the polymerization of RNA from activated ribonucleotides. Here we report that montmorillonite accelerates the spontaneous conversion of fatty acid micelles into vesicles. Clay particles often become encapsulated in these vesicles, thus providing a pathway for the prebiotic encapsulation of catalytically active surfaces within membrane vesicles. In addition, RNA adsorbed to clay can be encapsulated within vesicles. Once formed, such vesicles can grow by incorporating fatty acid supplied as micelles and can divide without dilution of their contents by extrusion through small pores. These processes mediate vesicle replication through cycles of growth and division. The formation, growth, and division of the earliest cells may have occurred in response to similar interactions with mineral particles and inputs of material and energy.
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              Coupled Growth and Division of Model Protocell Membranes

              The generation of synthetic forms of cellular life requires solutions to the problem of how biological processes such as cyclic growth and division could emerge from purely physical and chemical systems. Small unilamellar fatty acid vesicles grow when fed with fatty acid micelles and can be forced to divide by extrusion, but this artificial division process results in significant loss of protocell contents during each division cycle. Here we describe a simple and efficient pathway for model protocell membrane growth and division. The growth of large multilamellar fatty acid vesicles fed with fatty acid micelles, in a solution where solute permeation across the membranes is slow, results in the transformation of initially spherical vesicles into long thread-like vesicles, a process driven by the transient imbalance between surface area and volume growth. Modest shear forces are then sufficient to cause the thread-like vesicles to divide into multiple daughter vesicles without loss of internal contents. In an environment of gentle shear, protocell growth and division are thus coupled processes. We show that model protocells can proceed through multiple cycles of reproduction. Encapsulated RNA molecules, representing a primitive genome, are distributed to the daughter vesicles. Our observations bring us closer to the laboratory synthesis of a complete protocell consisting of a self-replicating genome and a self-replicating membrane compartment. In addition, the robustness and simplicity of this pathway suggests that similar processes might have occurred under the prebiotic conditions of the early Earth.
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                Author and article information

                Journal
                Astrobiology
                Astrobiology
                ast
                Astrobiology
                Mary Ann Liebert, Inc. (140 Huguenot Street, 3rd FloorNew Rochelle, NY 10801USA )
                1531-1074
                1557-8070
                01 April 2018
                01 April 2018
                01 April 2018
                : 18
                : 4
                : 419-430
                Affiliations
                [ 1 ]Institute for Genomic Biology, University of Illinois at Urbana-Champaign , Urbana, Illinois, USA.
                [ 2 ]Department of Cell Biology and Neuroscience, University of California , Riverside, California, USA.
                [ 3 ]Department of Molecular Genetics, Weizmann Institute of Science , Rehovot, Israel.
                Author notes
                Address correspondence to: Raphael Zidovetzki, Department of Molecular, Cell and Systems Biology, University of California 900 University Ave, Riverside, CA 92521, E-mail: raphael.zidovetzki@ 123456ucr.edu
                Article
                10.1089/ast.2016.1615
                10.1089/ast.2016.1615
                5910049
                29634319
                96c1c2d3-b760-4d70-a8f1-48b96217fccc
                © Don L. Armstrong et al., 2018; Published by Mary Ann Liebert, Inc.

                This Open Access article is distributed under the terms of the Creative Commons License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.

                History
                : 28 October 2016
                : 03 November 2017
                Page count
                Figures: 11, Tables: 2, References: 47, Pages: 12
                Categories
                Research Articles

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