An Origin-of-Life Reactor to Simulate Alkaline Hydrothermal Vents

Chemiosmotic coupling is universal: practically all cells harness electrochemical proton gradients across membranes to drive ATP synthesis, powering biochemistry. Autotrophic cells, including phototrophs and chemolithotrophs, also use proton gradients to power carbon fixation directly. The universality of chemiosmotic coupling suggests that it arose very early in evolution, but its origins are obscure. Alkaline hydrothermal systems sustain natural proton gradients across the thin inorganic barriers of interconnected micropores within deep-sea vents. In Hadean oceans, these inorganic barriers should have contained catalytic Fe(Ni)S minerals similar in structure to cofactors in modern metabolic enzymes, suggesting a possible abiotic origin of chemiosmotic coupling. The continuous supply of H2 and CO2 from vent fluids and early oceans, respectively, offers further parallels with the biochemistry of ancient autotrophic cells, notably the acetyl CoA pathway in archaea and bacteria. However, the precise mechanisms by which natural proton gradients, H2, CO2 and metal sulphides could have driven organic synthesis are uncertain, and theoretical ideas lack empirical support. We have built a simple electrochemical reactor to simulate conditions in alkaline hydrothermal vents, allowing investigation of the possibility that abiotic vent chemistry could prefigure the origins of biochemistry. We discuss the construction and testing of the reactor, describing the precipitation of thin-walled, inorganic structures containing nickel-doped mackinawite, a catalytic Fe(Ni)S mineral, under prebiotic ocean conditions. These simulated vent structures appear to generate low yields of simple organics. Synthetic microporous matrices can concentrate organics by thermophoresis over several orders of magnitude under continuous open-flow vent conditions.

[1]  W. Martin,et al.  How did LUCA make a living? Chemiosmosis in the origin of life. , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[2]  M. Russell,et al.  The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front , 1997, Journal of the Geological Society.

[3]  Nick Lane,et al.  Bioenergetic constraints on the evolution of complex life. , 2014, Cold Spring Harbor perspectives in biology.

[4]  W. Martin,et al.  Serpentinization as a source of energy at the origin of life , 2010, Geobiology.

[5]  D. Braun,et al.  Thermal trap for DNA replication. , 2010, Physical review letters.

[6]  D. Braun,et al.  Thermophoresis of single stranded DNA , 2010, Electrophoresis.

[7]  Allan Hall,et al.  In vitro growth of iron sulphide chimneys: possible culture chambers for origin‐of‐life experiments , 1989 .

[8]  G. Cody TRANSITION METAL SULFIDES AND THE ORIGINS OF METABOLISM , 2004 .

[9]  M. Lilley,et al.  An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30 degrees N. , 2001, Nature.

[10]  Jack W. Szostak,et al.  Formation of Protocell-like Vesicles in a Thermal Diffusion Column , 2009, Journal of the American Chemical Society.

[11]  P. Mitchell Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism , 1961, Nature.

[12]  P. Deymier,et al.  Where on Earth has our water come from? , 2010, Chemical communications.

[13]  H. Burd,et al.  Abundance of 4Fe-4S motifs in the genomes of methanogens and other prokaryotes. , 2004, FEMS microbiology letters.

[14]  H. Paulick,et al.  Unraveling the sequence of serpentinization reactions: petrography, mineral chemistry, and petrophysics of serpentinites from MAR 15°N (ODP Leg 209, Site 1274) , 2006 .

[15]  J. Kasting What caused the rise of atmospheric O2 , 2013 .

[16]  G. Fuchs Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? , 2011, Annual review of microbiology.

[17]  Charles S. Cockell,et al.  Emergence of a Habitable Planet , 2007 .

[18]  A. Yamaguchi,et al.  Electrochemical CO2 Reduction by Ni-containing Iron Sulfides: How Is CO2 Electrochemically Reduced at Bisulfide-Bearing Deep-sea Hydrothermal Precipitates? , 2014 .

[19]  M. O. Dayhoff,et al.  Evolution of the Structure of Ferredoxin Based on Living Relics of Primitive Amino Acid Sequences , 1966, Science.

[20]  W. Martin,et al.  The rocky roots of the acetyl-CoA pathway. , 2004, Trends in biochemical sciences.

[21]  B. Maden,et al.  No soup for starters? Autotrophy and the origins of metabolism. , 1995, Trends in biochemical sciences.

[22]  J. Szostak,et al.  Template-directed synthesis of a genetic polymer in a model protocell , 2008, Nature.

[23]  Christian de Duve,et al.  Vital Dust Life As A Cosmic Imperative , 1995, Nature Medicine.

[24]  P. Mitchell CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION , 1966, Biological reviews of the Cambridge Philosophical Society.

[25]  L. Orgel,et al.  The Implausibility of Metabolic Cycles on the Prebiotic Earth , 2008, PLoS biology.

[26]  Deborah S. Kelley,et al.  An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30° N , 2001, Nature.

[27]  J. Amend,et al.  The energetics of organic synthesis inside and outside the cell , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  David Bryant,et al.  Genome Networks Root the Tree of Life between Prokaryotic Domains , 2010, Genome biology and evolution.

[29]  A. Bekker,et al.  Dating the rise of atmospheric oxygen , 2004, Nature.

[30]  M. Russell,et al.  Hydrothermal Focusing of Chemical and Chemiosmotic Energy, Supported by Delivery of Catalytic Fe, Ni, Mo/W, Co, S and Se, Forced Life to Emerge , 2009, Journal of Molecular Evolution.

[31]  D. Mills,et al.  An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Thauer,et al.  Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation. , 2013, Biochimica et biophysica acta.

[33]  Dieter Braun,et al.  Trapping of DNA by thermophoretic depletion and convection. , 2002, Physical review letters.

[34]  W. Martin,et al.  Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution , 2007, Proceedings of the National Academy of Sciences.

[35]  M. Hecker,et al.  An Ancient Pathway Combining Carbon Dioxide Fixation with the Generation and Utilization of a Sodium Ion Gradient for ATP Synthesis , 2012, PloS one.

[36]  D. Moreira,et al.  The early evolution of lipid membranes and the three domains of life , 2012, Nature Reviews Microbiology.

[37]  William F. Martin,et al.  Energy at life's origin , 2014, Science.

[38]  W. Martin,et al.  On the origin of biochemistry at an alkaline hydrothermal vent , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[39]  W. Doolittle,et al.  Archaea and the Origin(s) of DNA Replication Proteins , 1997, Cell.

[40]  Manoj Kumar,et al.  Nickel-Containing Carbon Monoxide Dehydrogenase/Acetyl-CoA Synthase(,). , 1996, Chemical reviews.

[41]  D. Pinti The Origin and Evolution of the Oceans , 2005 .

[42]  J. Ferry,et al.  The stepwise evolution of early life driven by energy conservation. , 2006, Molecular biology and evolution.

[43]  W. Fyfe The water inventory of the Earth: fluids and tectonics , 1994, Geological Society, London, Special Publications.

[44]  P. Falkowski,et al.  Discovering the electronic circuit diagram of life: structural relationships among transition metal binding sites in oxidoreductases , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  Anne-Kristin Kaster,et al.  Methanogenic archaea: ecologically relevant differences in energy conservation , 2008, Nature Reviews Microbiology.

[46]  A. Ducluzeau,et al.  Free energy conversion in the LUCA: Quo vadis? , 2014, Biochimica et biophysica acta.

[47]  H. Janka,et al.  Neutrino signal of electron-capture supernovae from core collapse to cooling , 2010 .

[48]  Eric Bapteste,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Pattern pluralism and the Tree of Life hypothesis , 2007 .

[49]  Anne-Kristin Kaster,et al.  Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea , 2011, Proceedings of the National Academy of Sciences.

[50]  T. McCollom,et al.  Thermodynamic constraints on hydrogen generation during serpentinization of ultramafic rocks , 2009 .

[51]  G. Wächtershäuser,et al.  Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions. , 1997, Science.

[52]  R. Daniel,et al.  A hydrothermally precipitated catalytic iron sulphide membrane as a first step toward life , 1994, Journal of Molecular Evolution.

[53]  Graham A. Shields,et al.  Palaeoclimatology: Evidence for hot early oceans? , 2007, Nature.

[54]  N. Arndt,et al.  Geodynamic and metabolic cycles in the Hadean , 2004 .

[55]  J. Amend,et al.  Energetics of Biomolecule Synthesis on Early Earth , 2009 .

[56]  G. Fuchs,et al.  Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme , 2010, Nature.

[57]  Jasmine B. D. Jaffrés,et al.  The oxygen isotope evolution of seawater: A critical review of a long-standing controversy and an improved geological water cycle model for the past 3.4 billion years , 2007 .

[58]  Dana R. Yoerger,et al.  A Serpentinite-Hosted Ecosystem: The Lost City Hydrothermal Field , 2005, Science.

[59]  P. Mitchell The Origin of Life and the Formation and Organizing Functions of Natural Membranes , 1959 .

[60]  B. Maden Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism. , 2000, The Biochemical journal.

[61]  A. Pomiankowski,et al.  A Bioenergetic Basis for Membrane Divergence in Archaea and Bacteria , 2014, PLoS biology.

[62]  S. Harris,et al.  The archaebacterial origin of eukaryotes , 2008, Proceedings of the National Academy of Sciences.

[63]  Filipa L. Sousa,et al.  Origins of major archaeal clades correspond to gene acquisitions from bacteria , 2014, Nature.

[64]  N. Arndt,et al.  Processes on the Young Earth and the Habitats of Early Life , 2012 .

[65]  M. Schulte,et al.  The Emergence of Metabolism from Within Hydrothermal Systems , 1998 .

[66]  P. Falkowski,et al.  Evolutionary history of redox metal-binding domains across the tree of life , 2014, Proceedings of the National Academy of Sciences.

[67]  R. Coleman,et al.  H2-rich fluids from serpentinization: geochemical and biotic implications. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  J. Bada,et al.  Submarine hot springs and the origin of life , 1988, Nature.

[69]  A. Anbar,et al.  The photochemistry of manganese and the origin of Banded Iron Formations. , 1992, Geochimica et cosmochimica acta.

[70]  Y. Koga,et al.  Did Archaeal and Bacterial Cells Arise Independently from Noncellular Precursors? A Hypothesis Stating That the Advent of Membrane Phospholipid with Enantiomeric Glycerophosphate Backbones Caused the Separation of the Two Lines of Descent , 1998, Journal of Molecular Evolution.

[71]  K. Stetter,et al.  Hyperthermophiles in the history of life , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[72]  E. Shock,et al.  The Potential for Abiotic Organic Synthesis and Biosynthesis at Seafloor Hydrothermal Systems , 2010 .

[73]  Eugene V Koonin,et al.  On the origin of genomes and cells within inorganic compartments , 2005, Trends in Genetics.

[74]  T. Williams,et al.  An archaeal origin of eukaryotes supports only two primary domains of life , 2013, Nature.

[75]  Filipa L. Sousa,et al.  Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism. , 2014, Biochimica et biophysica acta.

[76]  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.

[77]  W. Martin,et al.  Hydrothermal vents and the origin of life , 2008, Nature Reviews Microbiology.

[78]  Detlef D. Leipe,et al.  Did DNA replication evolve twice independently? , 1999, Nucleic acids research.

[79]  E. Szathmáry,et al.  The Origin of Life: Chemical Evolution of a Metabolic System in a Mineral Honeycomb? , 2009, Journal of Molecular Evolution.

[80]  J. Hayes,et al.  Extraordinary 13C enrichment of diether lipids at the Lost City Hydrothermal Field indicates a carbon-limited ecosystem , 2009 .

[81]  Filipa L. Sousa,et al.  Early bioenergetic evolution , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[82]  K. Ludwig,et al.  U/Th Geochronology of Carbonate Chimneys at the Lost City Hydrothermal Field , 2005 .

[83]  W. Martin Hydrogen, metals, bifurcating electrons, and proton gradients: The early evolution of biological energy conservation , 2012, FEBS letters.

[84]  M. Antonietti,et al.  Hydrothermal formose reaction , 2011 .

[85]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[86]  L. Ljungdahl A life with acetogens, thermophiles, and cellulolytic anaerobes. , 2009, Annual review of microbiology.

[87]  W. Brazelton,et al.  Serpentinization, Carbon, and Deep Life , 2013 .

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

[89]  R. Daniel,et al.  On the emergence of life via catalytic iron‐sulphide membranes , 1993 .

[90]  Doolittle Wf Phylogenetic Classification and the Universal Tree , 1999 .

[91]  Did God make RNA? , 1988, Nature.

[92]  W. Martin,et al.  The Origin of Membrane Bioenergetics , 2012, Cell.

[93]  S. Ragsdale,et al.  Acetogenesis and the Wood-Ljungdahl pathway of CO(2) fixation. , 2008, Biochimica et biophysica acta.

[94]  Pierre-Alain Monnard,et al.  Primitive Membrane Formation, Characteristics and Roles in the Emergent Properties of a Protocell , 2011, Entropy.

[95]  Purificación López-García,et al.  Ancestral lipid biosynthesis and early membrane evolution. , 2004, Trends in biochemical sciences.

[96]  N. Sleep The Hadean-Archaean environment. , 2010, Cold Spring Harbor perspectives in biology.

[97]  Dieter Braun,et al.  Extreme accumulation of nucleotides in simulated hydrothermal pore systems , 2007, Proceedings of the National Academy of Sciences.

[98]  B. Schoepp‐Cothenet,et al.  The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[99]  J. H. Lee,et al.  Characterization of synthetic nanocrystalline mackinawite: crystal structure, particle size, and specific surface area. , 2008, Geochimica et cosmochimica acta.

[100]  M. J. Russell,et al.  Formation of fossil hydrothermal chimneys and mounds from Silvermines, Ireland , 1983, Nature.

[101]  Jeremy J. Yang,et al.  The origin of intermediary metabolism. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[102]  J. Wiegel,et al.  Thermophiles : The Keys to the Molecular Evolution and the Origin of Life? , 1998 .

[103]  D. Braun,et al.  Escalation of polymerization in a thermal gradient , 2013, Proceedings of the National Academy of Sciences.

[104]  Christian de Duve,et al.  Singularities: Landmarks on the Pathways of Life , 2005 .

[105]  Deborah S. Kelley,et al.  Abiogenic Hydrocarbon Production at Lost City Hydrothermal Field , 2008, Science.

[106]  S. R. Seidel,et al.  Chemical evolution II : from the origins of life to modern society , 2010 .