The Influence of Environmental Conditions, Lipid Composition, and Phase Behavior on the Origin of Cell Membranes

At some point in life’s development, membranes formed, providing barriers between the environment and the interior of the ‘cell.’ This paper evaluates the research to date on the prebiotic origin of cell membranes and highlights possible areas of continuing study. A careful review of the literature uncovered unexpected factors that influence membrane evolution. The major stages in primitive membrane formation and the transition to contemporary cell membranes appear to require an exacting relationship between environmental conditions and amphiphile composition and phase behavior. Also, environmental and compositional requirements for individual stages are in some instances incompatible with one another, potentially stultifying the pathway to contemporary membranes. Previous studies in membrane evolution have noted the effects composition and environment have on membrane formation but the crucial dependence and interdependence on these two factors has not been emphasized. This review makes clear the need to focus future investigations away from proof-of-principle studies towards developing a better understanding of the roles that environmental factors and lipid composition and polymorphic phase behavior played in the origin and evolution of cell membranes.

[1]  G. Ourisson,et al.  Addendum: Origins of cellular life: Molecular foundations and new approaches , 1999 .

[2]  Irene A. Chen,et al.  The Emergence of Competition Between Model Protocells , 2004, Science.

[3]  D. Deamer,et al.  Self-assembling amphiphilic molecules: Synthesis in simulated interstellar/precometary ices. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Szostak,et al.  RNA Catalysis in Model Protocell Vesicles , 2005, Journal of the American Chemical Society.

[5]  H. Morowitz Beginnings of Cellular Life: Metabolism Recapitulates Biogenesis , 1992 .

[6]  D. Deamer,et al.  Role of lipids in prebiotic structures. , 1980, Bio Systems.

[7]  Martin M. Hanczyc,et al.  Experimental Models of Primitive Cellular Compartments: Encapsulation, Growth, and Division , 2003, Science.

[8]  P. Pohl,et al.  Changes of intrinsic membrane potentials induced by flip-flop of long-chain fatty acids. , 2000, Biochemistry.

[9]  Dale P. Cruikshank,et al.  Organic matter in carbonaceous chondrites, planetary satellites, asteroids and comets , 1988 .

[10]  S. Marčelja,et al.  Physical principles of membrane organization , 1980, Quarterly Reviews of Biophysics.

[11]  A. Khvorova,et al.  Binding and disruption of phospholipid bilayers by supramolecular RNA complexes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Pierre-Alain Monnard,et al.  Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium. , 2002, Astrobiology.

[13]  D. Deamer,et al.  Permeation of membranes by the neutral form of amino acids and peptides: Relevance to the origin of peptide translocation , 1994, Journal of Molecular Evolution.

[14]  M. Yarus,et al.  A membrane transporter for tryptophan composed of RNA. , 2004, RNA.

[15]  A. Vlassov How was Membrane Permeability Produced in an RNA World? , 2005, Origins of Life and Evolution of Biospheres.

[16]  David W. Deamer,et al.  Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions , 2005, Journal of Molecular Evolution.

[17]  WHEN DARWIN,et al.  The Origin of Life , 2019, Rethinking Evolution.

[18]  A. Rushdi,et al.  Abiotic Condensation Synthesis of Glyceride Lipids and Wax Esters Under Simulated Hydrothermal Conditions , 2006, Origins of Life and Evolution of Biospheres.

[19]  G. Lindblom,et al.  Cubic phases and isotropic structures formed by membrane lipids — possible biological relevance , 1989 .

[20]  F. Kamp,et al.  Dissociation of long and very long chain fatty acids from phospholipid bilayers. , 1996, Biochemistry.

[21]  J. Bada How life began on Earth: a status report , 2004 .

[22]  Katsuhiko Ariga,et al.  Monolayer studies of single-chain polyprenyl phosphates. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[23]  J. Oró,et al.  Cyanamide mediated synthesis under plausible primitive earth conditions , 1979, Journal of Molecular Evolution.

[24]  P. Walde,et al.  From decanoate micelles to decanoic acid/dodecylbenzenesulfonate vesicles. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[25]  D. Bartel,et al.  Synthesizing life , 2001, Nature.

[26]  A. Bangham,et al.  Diffusion of univalent ions across the lamellae of swollen phospholipids. , 1965, Journal of molecular biology.

[27]  A. Weber Origin of fatty acid synthesis: Thermodynamics and kinetics of reaction pathways , 2006, Journal of Molecular Evolution.

[28]  Pier Luigi Luisi,et al.  Growth and Transformation of Vesicles Studied by Ferritin Labeling and Cryotransmission Electron Microscopy , 2001 .

[29]  Pier Luigi Luisi,et al.  Matrix Effect in the Size Distribution of Fatty Acid Vesicles , 1998 .

[30]  D. Alford,et al.  Spontaneous fusion of phosphatidylcholine small unilamellar vesicles in the fluid phase. , 1987, Biochemistry.

[31]  D. Lasič,et al.  The mechanism of vesicle formation. , 1988, The Biochemical journal.

[32]  D. Deamer,et al.  Amphiphilic components of the murchison carbonaceous chondrite: Surface properties and membrane formation , 2005, Origins of life and evolution of the biosphere.

[33]  Pierre-Alain Monnard,et al.  Preparation of vesicles from nonphospholipid amphiphiles. , 2003, Methods in enzymology.

[34]  Martin M Hanczyc,et al.  Replicating vesicles as models of primitive cell growth and division. , 2004, Current opinion in chemical biology.

[35]  D. Gilbert,et al.  Membrane bilayer assembly in neural tissue of rat and squid as a critical phenomenon: Influence of temperature and membrane proteins , 2005, The Journal of Membrane Biology.

[36]  J. Oró,et al.  Cyanamide mediated syntheses under plausible primitive earth conditions , 1978, Journal of Molecular Evolution.

[37]  G. Ourisson,et al.  Towards Proto‐Cells: “Primitive” Lipid Vesicles Encapsulating Giant DNA and Its Histone Complex , 2001, Cellular & molecular biology letters.

[38]  A. Khvorova,et al.  RNAs that bind and change the permeability of phospholipid membranes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Fabio Mavelli,et al.  Matrix Effect in Oleate Micelles-Vesicles Transformation , 2004, Origins of life and evolution of the biosphere.

[40]  P. Luisi,et al.  Autopoietic Self-Reproduction of Fatty Acid Vesicles , 1994 .

[41]  Fabio Mavelli,et al.  A Possible Route to Prebiotic Vesicle Reproduction , 2004, Artificial Life.

[42]  K. Matsuno,et al.  Evolving lipid vesicles in prebiotic hydrothermal environments , 2005, Origins of Life and Evolution of Biospheres.

[43]  G. Ourisson,et al.  Membrane Properties of Branched Polyprenyl Phosphates, Postulated as Primitive Membrane Constituents , 2006, Chemistry & biodiversity.

[44]  S. Singer,et al.  The fluid mosaic model of the structure of cell membranes. , 1972, Science.

[45]  D. Bartel,et al.  Synthesizing life : Paths to unforeseeable science & technology , 2001 .

[46]  N. Gershfeld Spontaneous assembly of a phospholipid bilayer as a critical phenomenon: influence of temperature, composition, and physical state , 1989 .

[47]  Ronald R. Breaker,et al.  Production of RNA by a polymerase protein encapsulated within phospholipid vesicles , 1994, Journal of Molecular Evolution.

[48]  N. Gershfeld,et al.  Thermal instability of red blood cell membrane bilayers: Temperature dependence of hemolysis , 2005, The Journal of Membrane Biology.

[49]  D. Deamer,et al.  Liposomes from ionic, single-chain amphiphiles. , 1978, Biochemistry.

[50]  D. Deamer,et al.  A novel method for encapsulation of macromolecules in liposomes. , 1985, Biochimica et biophysica acta.

[51]  D. Deamer,et al.  Polycyclic aromatic hydrocarbons: primitive pigment systems in the prebiotic environment. , 1992, Advances in space research : the official journal of the Committee on Space Research.

[52]  D. Lancet,et al.  Composing life , 2000, EMBO reports.

[53]  J. Oró,et al.  Cyanamide mediated syntheses under plausible primitive earth conditions , 1977, Journal of Molecular Evolution.

[54]  Harold J. Morowitz,et al.  The chemical logic of a minimum protocell , 2005, Origins of life and evolution of the biosphere.

[55]  D. Deamer,et al.  Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. , 2002, Biochimica et biophysica acta.

[56]  D. Deamer,et al.  Permeability of lipid bilayers to amino acids and phosphate. , 1992, Biochimica et biophysica acta.

[57]  D W Deamer,et al.  Light-dependent pH gradients are generated in liposomes containing ferrocyanide. , 1990, Bio Systems.

[58]  J. Oró,et al.  Studies on precellular evolution: the encapsulation of polyribonucleotides by liposomes. , 1986, Advances in space research : the official journal of the Committee on Space Research.

[59]  W. Martin,et al.  On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[60]  D. Deamer,et al.  Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. , 1996, Biophysical journal.

[61]  A. Keefe,et al.  Are polyphosphates or phosphate esters prebiotic reagents? , 2004, Journal of Molecular Evolution.

[62]  L E Orgel,et al.  RNA catalysis and the origins of life. , 1986, Journal of theoretical biology.

[63]  D. W. Deamer The Molecular Origins of Life: Membrane compartments in prebiotic evolution , 1998 .

[64]  A. Brack The origin of life on Earth , 1991 .

[65]  N. Gershfeld The critical unilamellar lipid state: a perspective for membrane bilayer assembly. , 1989, Biochimica et biophysica acta.

[66]  G. Ourisson,et al.  Membrane properties of sodium 2- and 6-(poly)prenyl-substituted polyprenyl phosphates , 2001 .

[67]  David W. Deamer,et al.  Boundary structures are formed by organic components of the Murchison carbonaceous chondrite , 1985, Nature.

[68]  P. Walde,et al.  Vesicles from docosahexaenoic acid. , 2007, Colloids and surfaces. B, Biointerfaces.

[69]  G Ourisson,et al.  The terpenoid theory of the origin of cellular life: the evolution of terpenoids to cholesterol. , 1994, Chemistry & biology.

[70]  J. Seddon,et al.  Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. , 1990, Biochimica et biophysica acta.

[71]  E. Anders,et al.  Meteorites and the Early Solar System , 1971 .

[72]  D. Deamer,et al.  Membrane self‐assembly processes: Steps toward the first cellular life , 2002, The Anatomical record.

[73]  D. Deamer,et al.  Synthesis of phospholipids and membranes in prebiotic conditions , 1977, Nature.

[74]  J. Trevors Possible origin of a membrane in the subsurface of the Earth , 2003, Cell biology international.

[75]  David W. Deamer,et al.  The Formation Of Glycerol Monodecanoate By A Dehydration Condensation Reaction: Increasing The Chemical Complexity Of Amphiphiles On The Early Earth , 2005, Origins of Life and Evolution of Biospheres.

[76]  P. Luisi,et al.  AUTOPOIETIC SELF-REPRODUCTION OF CHIRAL FATTY ACID VESICLES , 1997 .

[77]  John R. Cronin The Molecular Origins of Life: Clues from the origin of the Solar System: meteorites , 1998 .

[78]  Oparin Ai,et al.  Effect on coacervate systems of enzymatic synthesis of polyadenylic acid , 1976 .

[79]  S. Svetina,et al.  A relationship between membrane properties forms the basis of a selectivity mechanism for vesicle self-reproduction , 2004, European Biophysics Journal.

[80]  A. Oparin [The origin of life]. , 1938, Nordisk medicin.

[81]  J. Szostak,et al.  Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[82]  D. Deamer,et al.  The first cell membranes. , 2002, Astrobiology.

[83]  S. Rottem Transbilayer Distribution of Lipids in Microbial Membranes , 1982 .

[84]  D. Deamer,et al.  Hydrothermal Reactions of Pyruvic Acid: Synthesis, Selection, and Self-Assembly of Amphiphilic Molecules , 2007, Origins of Life and Evolution of Biospheres.

[85]  J. Szostak,et al.  Semipermeable lipid bilayers exhibit diastereoselectivity favoring ribose , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[86]  A. Weber The triose model: Glyceraldehyde as a source of energy and monomers for prebiotic condensation reactions , 2005, Origins of life and evolution of the biosphere.

[87]  Irene A Chen,et al.  A kinetic study of the growth of fatty acid vesicles. , 2004, Biophysical journal.

[88]  P. Walde Surfactant Assemblies and their Various Possible Roles for the Origin(S) of Life , 2006, Origins of Life and Evolution of Biospheres.

[89]  G. Lindblom,et al.  Lipid bilayer stability in membranes. Regulation of lipid composition in Acholeplasma laidlawii as governed by molecular shape. , 1980, Biochemistry.

[90]  A. Rushdi,et al.  Lipid Formation by Aqueous Fischer-Tropsch-Type Synthesis over a Temperature Range of 100 to 400 °C , 2001, Origins of life and evolution of the biosphere.

[91]  J. Gutknecht Proton conductance caused by long-chain fatty acids in phospholipid bilayer membranes , 1988, The Journal of Membrane Biology.

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

[93]  Pier Luigi Luisi,et al.  Self-replicating micelles: aqueous micelles and enzymatically driven reactions in reverse micelles , 1991 .

[94]  P. Lindahl Stepwise Evolution of Nonliving to Living Chemical Systems , 2004, Origins of life and evolution of the biosphere.

[95]  N. Gershfeld,et al.  Critical temperature for unilamellar vesicle formation in dimyristoylphosphatidylcholine dispersions from specific heat measurements. , 1993, Biophysical journal.

[96]  J. Oró,et al.  Synthesis of phosphatidylcholine under possible primitive Earth conditions , 1982, Journal of Molecular Evolution.

[97]  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.

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

[99]  S. Miller A production of amino acids under possible primitive earth conditions. , 1953, Science.

[100]  J. Oró,et al.  Synthesis of phosphatidylethanolamine under possible primitive earth conditions , 2005, Journal of Molecular Evolution.