The Prebiotic Chemistry of Pyrite:The Prebiotic Chemistry of Pyrite:Molecular Scaffold & CatalystMolecular Scaffold & Catalyst

ABIOL 570ABIOL 570

November 21, 2004November 21, 2004

IntroductionIntroduction• Protocellular ScaffoldProtocellular Scaffold

– Framboidal PyriteFramboidal Pyrite A self-organizing systemA self-organizing system Synthesized with or without oxygenSynthesized with or without oxygen Physical properties of astrobiological significancePhysical properties of astrobiological significance

• CatalysisCatalysis– Adsorption of 5’-AMP onto FeSAdsorption of 5’-AMP onto FeS22

Modulation by acetateModulation by acetate– Readily synthesized under prebiotic conditionsReadily synthesized under prebiotic conditions– Common component of metabolic pathwaysCommon component of metabolic pathways

Simulated prebiotic environmentSimulated prebiotic environment– 5’-AMP inihibitor (DMF)5’-AMP inihibitor (DMF)– Interactions on mineral surfaceInteractions on mineral surface

Phase SeparationPhase Separation

• Adsorption on a Adsorption on a surfacesurface• Mineral-HMineral-H22O O • Air-HAir-H22OO• FeSFeS22-H-H22OO

• Trapping in a Trapping in a containercontainer• Oil dropletsOil droplets• ProteinoidsProteinoids• Amphiphile Amphiphile

vesiclesvesicleshttp://tycho.bgsu.edu/~laird/ast305/class/IVC-5.html

Framboidal PyriteFramboidal Pyrite Self-organization:Self-organization: “the autonomous “the autonomous

passage of a system from an unpatterned passage of a system from an unpatterned to a patterned state without the to a patterned state without the intervention of an external template”.intervention of an external template”.

Framboidal PyriteFramboidal Pyrite Closely-packed, spheroidal clusters of 100-Closely-packed, spheroidal clusters of 100-

100,000 pyrite microcrystals100,000 pyrite microcrystals

May be synthesized in 1 of 2 ways:May be synthesized in 1 of 2 ways:– FeSFeS(ppt)(ppt) + S + S(aq)(aq)FeFe33SS44FeSFeS22 (Low [O(Low [O22])])

• Greigite = magnetic thiospinel; formation determines Greigite = magnetic thiospinel; formation determines rxn rate in the presence of oxygenrxn rate in the presence of oxygen

– FeSFeS(mk)(mk) + H + H22SS(aq)(aq) FeS FeS2(py)2(py) + H+ H2(aq)2(aq) (no O (no O22))• Most rapid rxnMost rapid rxn

Framboidal PyriteFramboidal Pyrite Forms instantaneously in anoxic sedimentsForms instantaneously in anoxic sediments Texture is result of rapid nucleation where Texture is result of rapid nucleation where

pyrite is supersaturatedpyrite is supersaturated– Normal saturation: single crystals formNormal saturation: single crystals form

A porous, catalytic scaffold…A porous, catalytic scaffold…

• Fatty Acid vesicles Fatty Acid vesicles can be forced to can be forced to divide by extrusion divide by extrusion through porous through porous substances…substances…

• Liposomes range in Liposomes range in size from 50-60 nm size from 50-60 nm up to Giant Vesicles up to Giant Vesicles of 30-100 umof 30-100 um

• Framboidal or Framboidal or weathered FeSweathered FeS22 fits fits the bill!the bill!

The First “Membranes”The First “Membranes”

Spontaneously form proteinoid microspheres Spontaneously form proteinoid microspheres (electrostatic interactions)(electrostatic interactions)– Able to take up molecules & have electrical Able to take up molecules & have electrical

potentials across “membranes”potentials across “membranes”– Respond to changes in osmotic pressureRespond to changes in osmotic pressure

http://www.biologie.uni-hamburg.de/b-online/e41/3.htm

Fatty Acid VesiclesFatty Acid Vesicles

Phosphates + Glycerol Phosphates + Glycerol + Fatty Acids + Fatty Acids

PhospholipidsPhospholipids

Clumped together Clumped together

Phospholipid BilayersPhospholipid Bilayers

LiposomesLiposomes Acquire many different Acquire many different

solutes while dryingsolutes while drying Preferred size in range of Preferred size in range of

living cells!living cells!

www.bio.davidson.edu/Courses/Molbio/MolStudents/.../Favorite_Molecular_Tool.html

Creation of ProtocellsCreation of Protocells

Microsphere can pick up anMicrosphere can pick up anythingything… even … even liposomesliposomes

ATP + nucleotides ATP + nucleotides oligonucleotides oligonucleotides (inside ingested (inside ingested liposome)liposome)

– Began to base pair with itself?Began to base pair with itself? Liposomes + hollow proteins Liposomes + hollow proteins “membrane” pores “membrane” poreshttp://www.stc.uniroma2.it/cfmacro/cfmacroindex.htm

Primitive Protocell MetabolismPrimitive Protocell Metabolism Precursors needed to Precursors needed to

maintain “membranes”maintain “membranes”

– Proteins, lipids & Proteins, lipids & carbohydratescarbohydrates

– First chemoorganotroph First chemoorganotroph (popular; simple (popular; simple metabolism)metabolism)

– Protocells died when Protocells died when starved, became toxic, starved, became toxic, got too big or in wrong got too big or in wrong environmentenvironment

– Some grew faster than Some grew faster than others, made products others, made products that facilitated growth, that facilitated growth, etc.etc.

http://www.funhousefilms.com/sciencpg.htm

Origin of Heredity & MetabolismOrigin of Heredity & Metabolism

• RNA most likely not first RNA most likely not first genetic systemgenetic system

• TNA suggested but linking TNA suggested but linking bases, sugars & PObases, sugars & PO44’s has ’s has

not been demonstratednot been demonstrated

• Mineral catalysis?Mineral catalysis?

http://nai.arc.nasa.gov/news_stories/news_detail.cfm?ID=189

A A TTNA World?NA World? (L)-(L)-αα–threofuranosyl-(3–threofuranosyl-(3112211) )

oligonucleotideoligonucleotide– Threose is the sugarThreose is the sugar

Simplest nucleic acid Simplest nucleic acid alternativealternative– Possible ancestor of RNAPossible ancestor of RNA– Possible protector/regulator Possible protector/regulator

of RNA (binds to it)of RNA (binds to it)

Forms base pairsForms base pairs– GG==C & T/U=A C & T/U=A – Informational in anti-parallelInformational in anti-parallel– Cross-pairs with RNA & DNACross-pairs with RNA & DNA

A & T nucleobase analogs:A & T nucleobase analogs:– 2’-amino-(2’-NH2 TNA)2’-amino-(2’-NH2 TNA)– 3’-amino-(3’-NH2 TNA)3’-amino-(3’-NH2 TNA)

Bst PolI, bacteriophage T7 Bst PolI, bacteriophage T7 DNA Pol (exo-) & MMLV-RTDNA Pol (exo-) & MMLV-RT

Chaput, J.C., Ichida, J.K & Szostak, J.W. (2002) DNA Polymerase-Mediated DNA Synthesis on a TNA Template. J. AM. CHEM. SOC. 125, 856-857.

A A TTNA World?NA World? Easily forms hairpinsEasily forms hairpins

much more stable to much more stable to hydrolytic cleavage than hydrolytic cleavage than are RNAs and may be as are RNAs and may be as stable as DNAs stable as DNAs

TNA strands can be TNA strands can be synthesized by template-synthesized by template-controlled ligation with controlled ligation with either complementary TNA either complementary TNA or RNA strands as or RNA strands as templates templates

corresponding formation of corresponding formation of RNA sequences by ligation RNA sequences by ligation on a TNA template does on a TNA template does also occur, although with also occur, although with less efficiency less efficiency

http://www.scripps.edu/research/sr2001/chm03.html

Mineral Catalysis… Mineral Catalysis… remember remember the the framboidal pyriteframboidal pyrite??

A multifunctional A multifunctional surface!surface!

• Implicated in:Implicated in: Reverse Citric Acid Reverse Citric Acid

CycleCycle LPS of bacteria in LPS of bacteria in

bioleachingbioleaching COCO22 fixation (+ H fixation (+ H22S)S)

• Purine can adsorb to Purine can adsorb to uncharged sites on uncharged sites on FeSFeS22 surface! surface!

Pyrite CatalysisPyrite Catalysis• Bases arranged in Bases arranged in

planar arrangementplanar arrangement• Adsorbed purines Adsorbed purines

(attached by van der (attached by van der Waals interactions) Waals interactions) may have paired with may have paired with pyrimidines (H-pyrimidines (H-bonding)bonding)

• Enclosure by vesicles Enclosure by vesicles act as reaction vesselsact as reaction vessels

• Wachtershauser:Wachtershauser: 2-D 2-D surface surface ↑↑ organizationorganization

Pyrite CatalysisPyrite Catalysis

• FeS+ HFeS+ H22SSFeSFeS22

• Reducing power that Reducing power that could convert COcould convert CO22 C- C-containing metabolitescontaining metabolites

• Directly to CODirectly to CO22 failed but failed but successful from CO successful from CO (Stetter et al.)(Stetter et al.)

• COCO22 + FeS + 2 H + FeS + 2 H22S S FeSFeS22 + 2 H + 2 H22O + CO + C

• FeS needs higher FeS needs higher reductive power to fix COreductive power to fix CO22

• Possible with additional Possible with additional energy inputenergy input

Pyrite CatalysisPyrite Catalysis

Fe implicated in e- transferFe implicated in e- transfer– Light-driven generation of HLight-driven generation of H22 gas gas– Oxidative/Reductive rxns catalyzed by Fe-S minerals (FeSOxidative/Reductive rxns catalyzed by Fe-S minerals (FeS22))

Adoption of Fe-S clusters in:Adoption of Fe-S clusters in:– FerredoxinesFerredoxines– N-fixing enzymesN-fixing enzymes– Many other cofactorsMany other cofactors

– Solubilization of FeSSolubilization of FeS22 by Cys by Cys dissolved chemical energy dissolved chemical energy– Semiconducting PropertiesSemiconducting Properties

Adsorption Constant of α = 6E5 cmAdsorption Constant of α = 6E5 cm-1-1 for h for hvv>1.8 eV)>1.8 eV) High quantum efficiencies (up to 90% of adsorpbed photons High quantum efficiencies (up to 90% of adsorpbed photons

generate e- hole pairs in the sulfide)generate e- hole pairs in the sulfide)

A tantalizing possibility!A tantalizing possibility!

The first life form may have been The first life form may have been photosynthetic! photosynthetic! You’re kidding, right?You’re kidding, right?

http://www.bact.wisc.edu/bact330/lecturestaph

Earliest PhotosynthesizersEarliest Photosynthesizers Anaerobic Anaerobic

environmentenvironment

11stst photosynthesizers photosynthesizers used Hused H22 or H or H22S as S as substratessubstrates

Microbes still do Microbes still do this (Hthis (H22SSHH22 + S) + S)

– Purple & green Purple & green sulfur bacteriasulfur bacteria

http://bio.winona.msus.edu/bates/Bio241/images/figure-08-12-2.jpg

Questions?Questions?