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Darwin, Chemistry and the Origin of Life

Darwin, Chemistry and the Origin of Life. Andy Pratt Department of Chemistry. OVERVIEW. Darwinian natural selection and the generation of complexity Cells as historical artifacts Molecular fossils A model for the origin of life based on molecular selection

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Darwin, Chemistry and the Origin of Life

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  1. Darwin, Chemistry and the Origin of Life Andy Pratt Department of Chemistry

  2. OVERVIEW • Darwinian natural selection and the generation of complexity • Cells as historical artifacts • Molecular fossils • A model for the origin of life based on molecular selection • Some simple experiments involving biomimetic phosphate chemistry

  3. The complex products of natural selection http://itech.dickinson.edu/chemistry

  4. TAKING DARWIN SERIOUSLY Cells are archaeological sites The fossils are chemical: metabolites and metabolic processes Darwin, Chemistry and the Origin of Life

  5. The complex products of natural selection http://itech.dickinson.edu/chemistry

  6. The complex products of natural selection http://itech.dickinson.edu/chemistry

  7. Darwin, Chemistry and the Origin of Life

  8. “Jack, the next Darwin?” “Jack, the neck scar twin” “Jack, the next car wins” Genomes & Chinese whispers: The insights of Pauling and Zuckerkandl “Jack, the next card wins” Darwin, Chemistry and the Origin of Life

  9. TAKING DARWIN SERIOUSLY • Darwinian natural selection provides a mechanism for generating complexity • Inspiration to chemical creativity • But how did something as complex as a cell arise? • When did chemistry become biology? • The role of the selection of chemical process in the origin of life, two examples: • Catalysis and Solubility

  10. Time (Mya) 4000 3000 2000 1000 0 ORIGINS OF METABOLISM • Features • Anaerobic environment • Rich in Iron and Sulfur • Constant input of redox energy • Carbon fixed into organic molecules • Compartments for evolution • A contemporary fit • Hydrothermal vent systems • Mike Russell and others

  11. HYDROTHERMAL VENT SYSTEMS http://uwnews.washington.edu/

  12. Anaerobic carbon fixation Wood-Ljungdahl pathway - ACS / CODH Likely original anaerobic carbon fixation

  13. Biogeochemistry and element fixation Hegg, Acc. Chem. Res. 2004, 37, 775 CODH ACS Wood-Ljungdahl pathway - ACS / CODH Likely original anaerobic carbon fixation

  14. CH3SH + CO CH3COSCH3 + CH3COOH NiS, FeS, H2O,100oC Huber & Wächtershäuser, Science, 1997,276, 245 BIOMIMETIC CARBON FIXATION Carbon fixation: the reductive acetyl CoA pathway Seravalli, Kumar, & Ragsdale Biochemistry, 2002, 41, 1807 CH3-B12 + CO + HSCoA CH3COSCoA CO dehydrogenase Acetyl CoA synthase

  15. HYDROTHERMAL VENT BIOGEOCHEMISTRY? Russell & Martin, TiBS, 2004, 29, 358

  16. BIOGEOCHEMISTRY EMERGES? Minerals to Enzymes • BIOMIMETIC Fe(Ni)S CATALYSIS: • Huber & Wächtershäuser, Science, 1997,276, 245 • Cody et al., Science, 2000, 289, 1337 • Dörr et al, Ang. Chem. Int. Edn. Engl. 2003, 42, 1540 • Wächtershäuser etc Tet Lett., 2003,44, 1695

  17. IN PRINCIPLE, MIKE RUSSELL’S MOUND PROVIDES: • On going chemical input and redox gradient for energy and metabolite flux • Catalytic surfaces to mediate electron-transfer and other protobiochemical processes • Compartmentalisation in microporous material • Concentration of proto-metabolites via surface adsorption Surfaces and solutions? Evolution of chemistry of metabolism?

  18. IRON SULFIDE MICROCOMPARTMENTS Russell & Martin, Phil Trans RS (B), 2003, 358, 59

  19. PROTEINS + WATER DNA/RNA + WATER POLYSACCHARIDES + WATER AMINO ACIDS NUCLEOTIDES SUGARS • “The most important thing in life is death”- Monod • FEATURES OF LIFE • Ongoing redox energy input • Occurs in discrete aqueous environments (cells) • Darwinian selection • KEY EARLY DISCOVERIES OF METABOLISM • Reductive fixation of carbon generates BOTH organic molecules AND dehydrating power in water • Selective production of condensation polymers which are kinetically stable, but thermodynamically unstable

  20. “The most important thing in life is death”- Monod FEATURES OF LIFE PROTEINS + WATER DNA/RNA + WATER POLYSACCHARIDES + WATER AMINO ACIDS NUCLEOTIDES SUGARS ATP PROTEINS + WATER DNA/RNA + WATER POLYSACCHARIDES + WATER AMINO ACIDS NUCLEOTIDES SUGARS KINETIC vs THERMODYNAMIC STABILITY Molecular evolution: Molecules survive if formed faster than they degrade Kinetic stability + catalysis ATP as the harnessing of dehydrating power

  21. SURFACES: CONCENTRATION & CATALYSIS POLYPHOSPHATE ACCUMULATION Susie Meade & Ico de Zwart • Phosphate species concentrate via precipitation • Mineral catalysis of biomimetic phosphoryl transfer • Surface accumulation of polyphosphates

  22. COMPETITIVE PHOSPHATE SURFACE BINDING Glycerol-2-phosphate vs Pyrophosphate

  23. COMPETITIVE PHOSPHATE SURFACE BINDING Glycerol-2-phosphate vs Pyrophosphate

  24. COMPETITIVE PHOSPHATE SURFACE BINDING Glycerol-2-phosphate vs Pyrophosphate Experiments repeated with other phosphate species e.g. Glycerol-2-phosphate vs Phosphate Adenosine-5’-monophosphate (AMP) vs Pyrophosphate

  25. COMPETITIVE PHOSPHATE SURFACE BINDING SELECTIVE “METABOLITE” RELEASE • Selection for organic phosphates in solution • Homeostatic backdrop of sparingly soluble phosphates

  26. EVOLVING SOLUTION METABOLISM • Mineral surface chemistry can proliferate until the local redox gradient is dissipated • Protometabolism will ‘die’ unless it becomes mobile • Selection of solubilized autocatalytic networks which colonize new compartments • ORIGIN OF MOLECULAR EVOLUTION AND METABOLISM

  27. EVOLVING SELECTION • Selection processes: • Molecules made faster than they are lost, e.g. by decomposition or dilution • Catalytic chemistry is reproduced in a new compartment before redox gradient exhausted • Selection favours: • Increased autocatalytic efficiency • Manipulation of solubility equilibria • Dynamic solubility equilibria allows reproduction and homeostasis • Encapsulation of cohorts of catalytic centres

  28. Pi Fe2+ Pi S2- S2- Pi Fe2+ Fe2+ Fe2+ Fe2+ S2- S2- S2- S2- EVOLVING TO AN INTEGRATED SOLUTION METABOLISM • Sparingly soluble salts • Dynamic ion exchange  Homeostasis • Control of solubility via: • Redox • Organic ligands for phosphate (e.g. organic derivatives) and Fe2+ (peptides) • Competitive equilibria (e.g. S2-) • Feedback loops • Micellar encapsulation Pi Pi Pi Pi Fe2+ Fe3+ Fe2+ Fe2+ Fe3+ S2- S2- S2- S2-

  29. Many thanks to Ico de Zwart Susie Meade Marie Squire Ward Robinson Mike Russell (NASA) and

  30. Evolving catalysis by the mineral surface FeS is deposited as Mackinawite Figure: Russell & Hall, GSA Memoir198 (2006), 1

  31. Mackinawite, Greigite and the Origin of Molecular evolution? Electron-transfer co-factor Fig: Rickard & Luther, Chemical Reviews, 2007, 107, 514-62

  32. Mackinawite & Greigite Fig: Rickard & Luther, Chemical Reviews, 2007, 107, 514-62

  33. Greigite FeII/III FeII Fig: Rickard & Luther, Chemical Reviews, 2007, 107, 514-62

  34. CO2 CH3COSR AcPi Pi Greigite (Fe3S4) Pi PPi Pyruvate Organic ligands Amino acids Peptides Mackinawite, Greigite and the Origin of Molecular evolution? Fe2+(aq) S2-(aq) Mackinawite (FeS)

  35. Organics + Fe3+ THE INVENTION OF METABOLISM CO2 • CO2: weak electron acceptor • FeS: electron donor Fe2+ S2- • Electron transfer slow without catalysis • Iron sulfides provide generic catalysis • Ligands & Fe3+ provide feedback loop • Reproduction with variation and selection

  36. Protein FeS Clusters Rao & Holm Chem. Rev. 2004, 104, 527

  37. “Nothing in Biology Makes Sense Except in the Light of Evolution” Theodore Dobhzhansky • Complexity of Life: a product of • Reproduction • Variation • Selection • Life is a process not an entity • Cells are historical documents

  38. CHEMICAL FUNDAMENTALS OF LIFE • Thermochemical gradient • Kinetic barrier to dissipation • CATALYSIS • Feedback loops  AUTOCATALYSIS • SELECTION for enhanced catalysis • EVOLUTION of autocatalytic loops Energy • REPLICATION of autocatalysis with VARIATION and SELECTION LIFE is a PROCESS, not an ENTITY Based on REPLICATION of METABOLICINFORMATION with VARIATION & SELECTION

  39. CHEMICAL FUNDAMENTALS OF LIFE • METABOLIC EVOLUTION The greatest improvement in the productive powers of labour, and the greater part of the skill, dexterity, and judgment with which it is any where directed, or applied, seem to have been the effects of the division of labour. An Inquiry into the Nature and Causes of the Wealth of Nations, Adam Smith Energy

  40. CHEMICAL FUNDAMENTALS OF LIFE • METABOLIC EVOLUTION • At start: inefficient GENERIC catalysts • REPLICATION with VARIATION and SELECTION  diversified, more effective catalysts • Need LOCALIZATION (compartments) • Ongoing & later issues: • Evolving COMPLEXITY of interlocked autocatalytic cycles • Benefit of REPLICATION FIDELITY • HOMEOSTASIS Energy

  41. Greigite mimics diverse Fe4S4 clusters Feedback loop: C-fixation induces mineral change; creates better catalyst; increases C-fixation rate

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