The Prebiotic Chemistry of Pyrite: Molecular Scaffold & Catalyst ABIOL 570 November 21, 2004

Introduction Protocellular Scaffold Framboidal Pyrite A self-organizing system Synthesized with or without oxygen Physical properties of astrobiological significance Catalysis Adsorption of 5’-AMP onto FeS 2 Modulation by acetate Readily synthesized under prebiotic conditions Common component of metabolic pathways Simulated prebiotic environment 5’-AMP inihibitor (DMF) Interactions on mineral surface

Protocellular Scaffold

Framboidal Pyrite

A self-organizing system

Synthesized with or without oxygen

Physical properties of astrobiological significance

Catalysis

Adsorption of 5’-AMP onto FeS 2

Modulation by acetate

Readily synthesized under prebiotic conditions

Common component of metabolic pathways

Simulated prebiotic environment

5’-AMP inihibitor (DMF)

Interactions on mineral surface

Phase Separation Adsorption on a surface Mineral-H 2 O Air-H 2 O FeS 2 -H 2 O Trapping in a container Oil droplets Proteinoids Amphiphile vesicles http://tycho.bgsu.edu/~laird/ast305/class/IVC-5.html

Adsorption on a surface

Mineral-H 2 O

Air-H 2 O

FeS 2 -H 2 O

Trapping in a container

Oil droplets

Proteinoids

Amphiphile vesicles

Framboidal Pyrite Self-organization: “the autonomous passage of a system from an unpatterned to a patterned state without the intervention of an external template”.

Self-organization: “the autonomous passage of a system from an unpatterned to a patterned state without the intervention of an external template”.

Framboidal Pyrite Closely-packed, spheroidal clusters of 100-100,000 pyrite microcrystals May be synthesized in 1 of 2 ways: FeS (ppt) + S (aq)  Fe 3 S 4  FeS 2 (Low [O 2 ]) Greigite = magnetic thiospinel; formation determines rxn rate in the presence of oxygen FeS (mk) + H 2 S (aq)  FeS 2(py) + H 2(aq) (no O 2 ) Most rapid rxn

Closely-packed, spheroidal clusters of 100-100,000 pyrite microcrystals

May be synthesized in 1 of 2 ways:

FeS (ppt) + S (aq)  Fe 3 S 4  FeS 2 (Low [O 2 ])

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

FeS (mk) + H 2 S (aq)  FeS 2(py) + H 2(aq) (no O 2 )

Most rapid rxn

Framboidal Pyrite Forms instantaneously in anoxic sediments Texture is result of rapid nucleation where pyrite is supersaturated Normal saturation: single crystals form

Forms instantaneously in anoxic sediments

Texture is result of rapid nucleation where pyrite is supersaturated

Normal saturation: single crystals form

A porous, catalytic scaffold… Fatty Acid vesicles can be forced to divide by extrusion through porous substances… Liposomes range in size from 50-60 nm up to Giant Vesicles of 30-100 um Framboidal or weathered FeS 2 fits the bill!

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

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

Framboidal or weathered FeS 2 fits the bill!

The First “Membranes” Spontaneously form proteinoid microspheres (electrostatic interactions) Able to take up molecules & have electrical potentials across “membranes” Respond to changes in osmotic pressure http://www.biologie.uni-hamburg.de/b-online/e41/3.htm

Spontaneously form proteinoid microspheres (electrostatic interactions)

Able to take up molecules & have electrical potentials across “membranes”

Respond to changes in osmotic pressure

Fatty Acid Vesicles Phosphates + Glycerol + Fatty Acids  Phospholipids Clumped together Phospholipid Bilayers  Liposomes Acquire many different solutes while drying Preferred size in range of living cells! www.bio.davidson.edu/Courses/Molbio/MolStudents/.../Favorite_Molecular_Tool.html

Phosphates + Glycerol + Fatty Acids

 Phospholipids

Clumped together

Phospholipid Bilayers

 Liposomes

Acquire many different solutes while drying

Preferred size in range of living cells!

Creation of Protocells Microsphere can pick up an ything … even liposomes ATP + nucleotides  oligonucleotides (inside ingested liposome) Began to base pair with itself? Liposomes + hollow proteins  “membrane” pores http://www.stc.uniroma2.it/cfmacro/cfmacroindex.htm

Microsphere can pick up an ything … even liposomes

ATP + nucleotides  oligonucleotides (inside ingested liposome)

Began to base pair with itself?

Liposomes + hollow proteins  “membrane” pores

Primitive Protocell Metabolism Precursors needed to maintain “membranes” Proteins, lipids & carbohydrates First chemoorganotroph (popular; simple metabolism) Protocells died when starved, became toxic, got too big or in wrong environment Some grew faster than others, made products that facilitated growth, etc. http://www.funhousefilms.com/sciencpg.htm

Precursors needed to maintain “membranes”

Proteins, lipids & carbohydrates

First chemoorganotroph (popular; simple metabolism)

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

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

Origin of Heredity & Metabolism RNA most likely not first genetic system TNA suggested but linking bases, sugars & PO 4 ’s has not been demonstrated Mineral catalysis? http://nai.arc.nasa.gov/news_stories/news_detail.cfm?ID=189

RNA most likely not first genetic system

TNA suggested but linking bases, sugars & PO 4 ’s has not been demonstrated

Mineral catalysis?

A T NA World? (L)- α –threofuranosyl-(3 1  2 1 ) oligonucleotide Threose is the sugar Simplest nucleic acid alternative Possible ancestor of RNA Possible protector/regulator of RNA (binds to it) Forms base pairs G = C & T/U=A Informational in anti-parallel Cross-pairs with RNA & DNA A & T nucleobase analogs: 2’-amino-(2’-NH2 TNA) 3’-amino-(3’-NH2 TNA) Bst PolI, bacteriophage T7 DNA 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.

(L)- α –threofuranosyl-(3 1  2 1 ) oligonucleotide

Threose is the sugar

Simplest nucleic acid alternative

Possible ancestor of RNA

Possible protector/regulator of RNA (binds to it)

Forms base pairs

G = C & T/U=A

Informational in anti-parallel

Cross-pairs with RNA & DNA

A & T nucleobase analogs:

2’-amino-(2’-NH2 TNA)

3’-amino-(3’-NH2 TNA)

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

A T NA World? Easily forms hairpins much more stable to hydrolytic cleavage than are RNAs and may be as stable as DNAs TNA strands can be synthesized by template-controlled ligation with either complementary TNA or RNA strands as templates corresponding formation of RNA sequences by ligation on a TNA template does also occur, although with less efficiency http://www.scripps.edu/research/sr2001/chm03.html

Easily forms hairpins

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

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

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

Mineral Catalysis… remember the framboidal pyrite ? A multifunctional surface! Implicated in: Reverse Citric Acid Cycle LPS of bacteria in bioleaching CO 2 fixation (+ H 2 S) Purine can adsorb to uncharged sites on FeS 2 surface!

A multifunctional surface!

Implicated in:

Reverse Citric Acid Cycle

LPS of bacteria in bioleaching

CO 2 fixation (+ H 2 S)

Purine can adsorb to uncharged sites on FeS 2 surface!

Pyrite Catalysis Bases arranged in planar arrangement Adsorbed purines (attached by van der Waals interactions) may have paired with pyrimidines (H-bonding) Enclosure by vesicles act as reaction vessels Wachtershauser: 2-D surface ↑ organization

Bases arranged in planar arrangement

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

Enclosure by vesicles act as reaction vessels

Wachtershauser: 2-D surface ↑ organization

Pyrite Catalysis FeS+ H 2 S  FeS 2 Reducing power that could convert CO 2  C-containing metabolites Directly to CO 2 failed but successful from CO (Stetter et al.) CO 2 + FeS + 2 H 2 S  FeS 2 + 2 H 2 O + C FeS needs higher reductive power to fix CO 2 Possible with additional energy input

FeS+ H 2 S  FeS 2

Reducing power that could convert CO 2  C-containing metabolites

Directly to CO 2 failed but successful from CO (Stetter et al.)

CO 2 + FeS + 2 H 2 S  FeS 2 + 2 H 2 O + C

FeS needs higher reductive power to fix CO 2

Possible with additional energy input

Pyrite Catalysis Fe implicated in e- transfer Light-driven generation of H 2 gas Oxidative/Reductive rxns catalyzed by Fe-S minerals (FeS 2 ) Adoption of Fe-S clusters in: Ferredoxines N-fixing enzymes Many other cofactors Solubilization of FeS 2 by Cys  dissolved chemical energy Semiconducting Properties Adsorption Constant of α = 6E5 cm -1 for h v >1.8 eV) High quantum efficiencies (up to 90% of adsorpbed photons generate e- hole pairs in the sulfide)

Fe implicated in e- transfer

Light-driven generation of H 2 gas

Oxidative/Reductive rxns catalyzed by Fe-S minerals (FeS 2 )

Adoption of Fe-S clusters in:

Ferredoxines

N-fixing enzymes

Many other cofactors

Solubilization of FeS 2 by Cys  dissolved chemical energy

Semiconducting Properties

Adsorption Constant of α = 6E5 cm -1 for h v >1.8 eV)

High quantum efficiencies (up to 90% of adsorpbed photons generate e- hole pairs in the sulfide)

A tantalizing possibility! The first life form may have been photosynthetic! You’re kidding, right? http://www.bact.wisc.edu/bact330/lecturestaph

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

Earliest Photosynthesizers Anaerobic environment 1 st photosynthesizers used H 2 or H 2 S as substrates Microbes still do this (H 2 S  H 2 + S) Purple & green sulfur bacteria http://bio.winona.msus.edu/bates/Bio241/images/figure-08-12-2.jpg

Anaerobic environment

1 st photosynthesizers used H 2 or H 2 S as substrates

Microbes still do this (H 2 S  H 2 + S)

Purple & green sulfur bacteria

Questions?