Rimicaris shrimp at NW Eifuku (Pacific Rim of Fire) Shrimp ( - - PowerPoint PPT Presentation

Rimicaris shrimp at NW Eifuku (Pacific Rim of Fire)

Shrimp (Cypridina hilgendorfii) uses bioluminescent vomit to avoid preda6on

41st Saas‐Fee course from Planets to Life 3‐9 April 2011 Lecture 5 ‐ Origin of Life and its Early Evolu6on on Earth

Abbreviated history of origin of life ideas: metabolism versus replica6on

• Darwin’s warm liKle pond (LeKer to Joseph Hooker, 1 Feb.

1871)

• Oparin‐Haldane ‐ Life started in a prebio6c soup
• RNA world (Gilbert, 1986)
• RNA catalysis preceded and led to metabolism (Eigen, Orgel

etc, 1980’s)

• Dyson (1985) ‐ ATP produced and consumed by protein‐based
• rganisms led to RNA from accumulated AMP; Kauffman, 1998

broadened Dyson’s idea so as to include other polymers and metabolites (autocataly6c sets)

• Metabolic reac6ons catalyzed by pyrites under hydrothermal

vent condi6ons (Wächtershäuser, 1988); Experimental evidence provided by Cody and others (2001‐2004); Eschemosser (2006), autocataly6c metabolic systems may be possible.

Outline

• BoKom‐up approach to the origin of life

– Sources of organic compounds – Chemical reac6ons to make biologically relevant

• rganic compounds
• Replicator first

– RNA as both the “Chicken and egg”

• Metabolism‐first

– “sparseness” of organic compounds favor metabolism – Metabolism needed to synthesize RNA

Bottom Up Approaches

Top Down Approaches

(Infer from extant life)

a) Settings for the origin of life b) Ancient physiologies (T°C, ±O2 etc) c) “Ancient” metabolisms (autotrophy vs heterotrophy) d) Ribozymes and the RNA world and models for the origin of the code e) Early replicators: ribozymes, ancient viruses, minerals, etc f) Origin of catalytic proteins

Organic precursors

(multiple sources) Metabolic circuits

RNA world

Genetic code and protein synthesis

Encapsulation?

DNA life

From Shen & Buick 2005

CO2, CO

The pathway leading to life (Earth)

• 1. Forma6on and concentra6on of organic precursor

compounds and organic catalysts

• 2. Condensa6on and polymeriza6on
• 3. ??? RNA, protein, protometabolism
• 4. ??? The gene6c code, ribosomes etc
• 5. “Unity of biochemistry”: selec6on of the fiKest genes,

biochemistry etc before the separa6on of the three domains of life

• 6. Transi6on from RNA to DNA
• 7. The three domains of life

– The origin of eukaryotes

A living en>ty?

Loca>on, loca>on, loca>on

Linked?

BoKom‐up approaches to origin of life studies: Five broad topics

1) Sources or organic precursors to life and chirality selection of d- and l-isomers 2) Synthesis of biopolymers 3) Metabolism versus “replicator” as the first step leading to cells 4) The origin of nucleic acids, the genetic code, and the evolution of the “central dogma” and the first evolving entity 5) Settings for the different steps (still unknown) in the origin of life and how settings can affect the

• utcomes in 1, 2 and 3

SPACE ATMOSPHERE

LIGHTNING IDP’S, COMETS, METEORITES, SHOCK SYNTHESIS UV CATALYSIS

OCEAN CRUST PHOTOREDUCTION OF CARBON

HYDROTHERMAL ORGANIC SYNTHESIS

REDUCED INORGANIC SPECIES

SOURCES OF ORGANIC CARBON ON THE PREBIOTIC EARTH ‐ Includes many of the organic building blocks of life

Peridotite-hosted hydrothermal vent

magma

From Schopf,2002

The Building Blocks – The first experiment

Urey, Miller 1953 – from Schopf, 2002 & Smith, Szathmary,1995

Organic Chemistry of Carbonaceous Meteorites

COMPOUNDS CM OCCURRENCE BIOLOGY

Biochemical Building Blocks

Amino acids

Fatty acids Glycerol Phosphate Purines Pyrimidines Ribose Phosphate + + + +

Others

Alcohols

Aldehydes Amides Amines Carboxylic acids Hydrocarbons Ketones Phosphonic acids Sulfonic acids Sulfides

Membranes Nucleic acids

+ + ‐ +

Proteins

+ + + + + + + + + +

Synthe6c organic reac6ons poten6ally occurring

• n the early Earth
• Gas phase reac6ons

– Reduced gases (H2, CH4, NH3, H2) + energy (heat, electric discharge, UV etc) → Cyanide (HCN) and formaldehyde

• Reac6ons producing water‐soluble products

– HCN → purines (e.g. adenine) – HCHO → simple sugars (glyceraldehyde, glucose) – HCN + HCHO → amino acids (Strecker synthesis)

• Reac6ons producing water insoluble products (hydrocarbon

deriva6ves)

– CO, H2 + heat, iron catalyst → hydrocarbons and amphiphiles (long‐chain faKy acids, alcohols) (Fisher‐Tropsch reac6ons)

• Polymeriza6on reac6ons (least undestood)

– Amino acids + dry heat → pep6de bonds (protein‐like polymers) – Glyceraldehyde → polyglyceric acid – Purines, pyrimidines, sugar, phosphate → nucleic acids

The BIG gap

• We know how to synthesize many of the
• rganic compounds required by life but we

know liKle about how to incorporate these compounds into “useful” macromolecules

• While it is generally believed that RNA

preceded DNA, we don’t know if it can be synthesized under “environmental condi6ons” in contrast to how we synthesize in a laboratory

The two compe6ng models for the

• rigin of life: “Replicator first”,

“Metabolism first”

Both models involve encapsula6on into small cell like structures usually formed by lipids

(From Shapiro, 2007)

Shapiro favors a “metabolism first” model; his model also starts in an organic soup except that organic compounds are incorporated into compartments that have a beKer chance of developing into a network of autocataly6c cycles and eventually into an informa6on macromolecule.

The Shapiro builds on an idea first discussed by Freeman Dyson (1999) and summarized in one of his famous quotes: “Life began with liKle bags, the precursors of the cell, enclosing small volumes of dirty water containing miscellaneous garbage.”

The “Central Dogma” (left) and the RNA world (right). The transition from the RNA world to the DNA world is thought to have required “reverse transcription”. There are reverse transcriptase enzymes in some RNA viruses including the AID’s virus (Figure from De Duve, 1995)

The “Replicator first” model predicts that RNA preceded DNA, protein and metabolism

The RNA world – a compelling model

• RNA ‐ The all purpose molecule

– Templates in chemical systems – Informa6on storage and retrieval – Catalysis

• Self‐splicing
• Self‐reproducing (self‐cleaving)
• Pep6de forma6on
• RNA combines genotype and phenotype: self‐

replica>on permits Darwinian evolu>on

• The goal is to understand how a protein‐free RNA

world became established on the primi6ve Earth ‐ led to the “Molecular Biologists Dream”

RNA and DNA

RNA with its nitrogenase bases to the llen and DNA with its nitrogenase bases to the right

The Ribosome: brown is RNA and blue is proteins. The ribosome contains 4 RNA molecules >50

• proteins. The ribosome

is the site where mRNA’s code is translated so as to form specific proteins

A ribozyme that func6ons as an RNA‐dependent RNA polymerase

RNA molecule that can make copies of RNA from an RNA template Requires an RNA template and RNA primer (like in the PCR reac>on) and a mixture

• f the 4 nucleo>des.

It can make an RNA molecule that is only 14 bases long ‐ more work on this is needed

Some progress on the RNA world

Recent research results on the RNA world

• Ribose and nucleo>des have been synthesized

abio>cally (in some cases under unrealis>c early earth condi>ons)

• Polymeriza>on of nucleo>des (oligonucleo>des

20‐50 mers)

– Clays (Huang and Ferris 2006) – Eutec6c phase of water‐ice (Monnard et al., 2003) – Lipid‐bilayer lapces (Rajamani et al., 2007)

• S>ll needed:

– RNA polymerase ribozyme capable of self replica6on – Insight on the emergence of the RNA code (not dependent on the RNA polymerase ribozyme) – The origin and evolu6on of the ribosome – Linking metabolism and replica6on in a “compartment” (the emergence of a “cell”)

The “Molecular Biologists Dream” ‐ a scenario for the origin of the RNA world (from Orgel, no date)

The Scenario:

First, forma>on of precursors to nucleic acids on Earth or elsewhere and accumula>on on Earth Next, nucleo6des were formed from prebio6c bases, sugars and phosphates and accumulated in some “special” environment. Next, a mineral catalyst such as a mineral like clays then catalyzed the forma>on of long single‐stranded polynucleo>des some of which were converted to complementary double strands by template‐directed synthesis ‐ this resulted in a “library” of double‐stranded RNA on the primi>ve Earth Next, among the double‐stranded RNAs there is at least one that on mel6ng yields a single‐stranded ribozyme capable of copying itself and its complementary RNA ‐ this would eventually lead to an exponen6ally growing popula6on subjected to Darwinian evolu6on

Summary of outstanding problems with the RNA world

• Sources (source reac6ons) of the precursors to

RNA (nucleo6des, ribose* and phosphate)

• Abio6c synthesis of RNA from precursors
• The transi6on RNA to self‐replica6ng RNA (RNA

catalysis)

• The transi6on from a self‐replica6ng RNA to the

“gene6c code”, transla6on and transcrip6on

• The origin of the ribosome
• The transi6on from RNA to DNA

*Ribose demonstrated to be synthesized in the presence of boron

minerals (Ricardo et al., Science 2004)

Encapsula6on and the emergence of “cell‐ like” structures

(From Deamer 2007)

Encapsula6on of macromolecules during a drying‐wepng cycle. (A) If liposomes are mixed with soluble proteins or nucleic acids and dried, the liposomes produce a mul6lamellar structure in which the macromolecules are “sandwiched” between lipid layers. Upon rehydra6on, vesicles form that encapsulate up to half of the soluble macromolecules. (B) Electron micrograph of a 2:1 (wt/wt) mixture of mixture of dioleoytlphospha6dylcholine‐salmon tes6s DNA aner drying, showing the fused mul6lamellar structure. (C) Fluorescence micrograph of the lipid‐DNA mixture following rehydra6on. Acridine orange was used to stain the DNA captured in large vesicles (From Deamer, 1998, 2004)

Encapsula6on of RNA and protein by lipid membranes

Lipid bilayer showing the hydrophilic polar head (a`ract H2O) on the outside and the hydrophilic tails inside. These lipid compounds (amphiphiles) self‐ assemble into biolayer structures

(From Deamer 2007)

Forma6on of membrane vescles from mixtures of meteoric amphiphilic compounds (lipid vesicles, monolayers etc) Transmission electron micrograph showing that almost all of the vescles have a membrane surrounding an internal mass of non‐membraneous material. At higher magnifica6on (insert) the membrane shows the trilaminar structure typical of bilayer membranes

From Deamer, 1998

The protocell model from Mansy and Szostak,

PNAS 2008; Cold Spring Harbor Press 2009

Schema6c model of a protocell. A replica6ng vesicle enables spa6al localiza6on, and a replica6ng genome encodes heritable informa6on. A complex environment provides nucleo6des, lipids, and various sources of energy, including mechanical energy for division, chemical energy for nucleo6de ac6va6on, and phase transfer and osmo6c gradient energy for growth.

Cold Spring Harbor Press 2009

Cycles of vesicle growth and division. A spherical mul6cellular vesicle grows aner the addi6on of faKy acid micelles by the forma6on of a thin

• protuberance. This grows over 6me un6l the ini6ally spherical vesicle

transforms into a filamentous vesicle. Gentle agita6on leads to division into daughter vesicles, which in turn can grow and repeat the cycle.

DNA strand separa6on and reanealing in vesicles (Mansy and Szostak, PNAS 2008)

Strand separa6on inside vesicles (Black lines) DNA strands labeled with donor and quencher dyes. When annealed to each other, fluorescence is low. (Open lines) Unlabeled DNA strands. Following strand separa6on and reannealing, the donor and quencher oligonucleo6des are separated, resul6ng in a high fluorescence signal.

Conclusion from Mansy and Szostak

The requirement for cycling between low and high temperature for nucleic acid copying and strand separa6on strongly suggests that freshwater ponds or springs in a generally cold environment, locally heated by geothermal ac6vity as a volcanic region, would be an ideal incuba6on of life.

What did Earth look like at the 6me life

• riginated?

Summary of encapsula6on models

• Small lipid‐membrane structures were an early

stage in the origin of life

– These structures some6mes call “micells” form spontaneously when the lipids are accumulate

• The lipid‐membrane structures can self‐replicate
• The lipid‐membrane structures, when exposed to

wet‐and‐dry cycles can entrap macromolecules (nucleic acids and proteins)

• The nucleic acids entrapped in lipid‐membranes

can divide if exposed to a high‐ and low‐ temperature cycle (like the Polymerase Chain Reac6on)

“Protometabolism”

• The need for high concentra6ons of organic

compounds that are the core of macromolecules (purines, pyrimidines, amino acids, faKy acids etc)

• Generate cataly6c organic compounds (CN,

CO, formate, formaldehyde, etc)

• Chemical energy (thioesters?) to drive more

complex organic reac6ons Can you get “protometabolism” from a soup?

“Sparseness” is a hallmark characteris6c of metabolism (from Shelly Copley)

Aquifex aeolicus Metabolism uses a very limited (sparse) set of

• rganic molecules. Aquifex aeolicus grows on CO2,

H2, O2 and NH3 and at 95°C The total organic compounds in the metabolome is 162 small organic compounds (<160 daltons)

Photo: SteKer and Rachel

All possible small organic molecules (C, N, H, O) with a MW of <160 daltons = >14

million (does not include

many aroma6c and heterocyclic compounds) (Fink et al., 2005)

Metabolism versus Replica6on, cont.

A “Protometabolic” network is necessary for the con6nuous

synthesis of organic precursor compounds to proteins and nucleic acids; The “thioester world” (De Duve, 1991).

The key to protometabolism is the thioester bond, a high energy bond that supports energy‐requiring reacNons (DeDuve, 1995)

“The requirements for both life and protometabolism are essen6ally the same: (1) a sustained source of energy driven by chemical disequilibrium origina6ng from either geological processes or sunlight, and (2) the presence of certain elements, in par>cular transi>on metals, to provide cataly>c poten>al for synthesis of

• rganics” Cody and ScoS, 2007

Ini6al stages of the acety‐CoA pathway, highligh6ng the extensive use of transi6on metals and sulfur. Migra6on and inser6on of the CO between the methyl group and the Ni atom yields the acetyl group. The acetyl group is transferred to a biochemical co‐factor yielding acetyl‐CoA providing the ini6a6on point to the acetyl‐CoA metabolic pathway. (Cody and ScoK, 2007)

CH3 transferred to a cobalt atom than to nickel atom (Ni‐X‐Fe4S4) “A” CO2 reduced to CO and transferred to an iron atom in the Fe4S4 cluster

Environmental sources of CO2, H2 and metals.

The acetyl‐CoA pathway

“New findings from the enzymes at the heart of the acetyl‐CoA pathway, carbon monoxide dehydrogenase and acetyl‐CoA synthase, indicate that metals and metal sulfides do the biochemical work of CO2 fixaNon” (Russell and Mar6n, 2004)

Acetyl‐CoA is a thioester

The acetyl‐CoA pathway showing the posi6on of metals at various steps (This is a hydrogen dependent pathway)

The presence of a sustaining chemistry‐ genera6ng‐system preceded RNA instruc6on

• New evidence suppor6ng some kind of proto‐

metabolic system producing the precursors to RNA synthesis

PNAS 104:9358‐9363, 2007 along with other modeling papers 2010, 2011

The authors suggest that modern metabolism involving proteins originated in nucleo6de metabolism. “The first enzyma6c takeover of an ancient biochemistry or prebio6c chemistry involved processes related to the synthesis of nucleo6des for a world in which RNA was the only gene6cally encoded catalyst.” The authors also point

• ut how liKle we know about how the RNA

world transi6oned into modern biochemistry.

“Our findings suggest that modern metabolism developed early at the

• nset of protein discovery and had
• rigins that benefited the forma6on of

building blocks for the RNA world”.

Synthesis of nucleodides bases and ribose, and polymerase into RNA

A popular model for the development of the gene6c system (Goldman et al., 2010)

Goldman et al., 2010

Conclusion from Goldman et al., 2010

• A func6onal ribosome existed during the RNA

world

• All of the ribosome proteins tested had only

the ancient 9 protein folds

• Most of the proteins used by extant life

evolved during and aner the separa6on of the three domains of life

What is the origin of these metal dependent metabolic pathways?

1) Minerals, minerals, minerals 2) Some early ideas about minerals and the

• rigin of life

Cairns‐Smith Clay Model for the origin of life Clay crystals

Crystal growth and “muta6on”

Condense organic compounds (clays as templates and reac6ve surfaces)“organic takeover”

Macromolecules Cells Crystal growth occurs by addi6on of units

• f the kink edge of a con6nuous ramp

spiraling around the central core Informa6on stored in crystals as a group of crystal “defects” that can be replicated through cleavage and crystal growth

Examples of possible reac>ons involving pyrite based on pyrite having a ca>onic surface in which a variety of anionic reac>ons are possible. The example in (A) is the adsorp>on of glyceraldehyde‐3‐phoshate to the surface followed by polymeriza>on. (B) Par>cipa>on of pyrite in a reac>on that can drive and otherwise energe>cally unfavorable reac>on. For example, the reduc>on of CO2 by H2 has a posi>ve Gibbs free energy reac>on. However, if CO2 reduc>on is linked to the pyrite reac>on the synthesis of formic acid is energe>cally favorable

Organic reac>on on pyrite surfaces under hydrothermal condi>ons (Wächterhäuser, 1988, 1998)

Pyrite

Wächterhäuser Model 1980’s Pyrite Organic synthesis and condensa6on “surface metabolites” Informa6on Macromolecules CELLS Russell Model 1990’s FeS membranes (bubbles formed from a mix of acidic seawater and alkaline hydrothermal fluid) Organic synthesis (ΔEh across membrane) Metabolic pathway Condensa6on reac6ons Informa6on macromolecules CELLS

Models for the origin of life in vent environments

How to get high concentra6ons of useful organic compounds?

• Specific synthesis – requires catalysts

(minerals)

• Very limited data at the present 6me, but

preliminary data looks very promising

Keep in mind that the cataly6c reac6ons carried out by proteins in present‐day organisms was very likely carried out by minerals before the gene6c code and ribosomes were fully developed

Mineral surfaces that may be involved in the origin of life (Modified from Deamer, 2007)

Mineral Surface Properties Lava minerals Si, O, Fe Major mineral surface on early Earth Apatite Ca, PO4

2-

Primary phosphate mineral Clays Si, Al, O Can organize organics into films and catalyze polymerization reactions Pyrite FeS2 Source of reducing power Calcite CaCO3 Chiral surfaces; concentrate

• rganics such nucleotides from

models Quartz SiO2 Chiral surfaces Ultramafic minerals Fe, Mg Generate hydrogen and organic compounds from CO2 Borate minerals B Catalyze the synthesis of ribose Elemental composi6on

Mineral Needs

• Catalyze metabolic networks that involve

the reduc6on of CO2 to organic compounds.

• There is a need to iden6fy the cataly6c

ability of other minerals under different T/ pH condi6ons (minerals that mimic known enzyme groups: oxidoreductases, transferases, hydrolases, lyases, isomerases and ligases)

We can accomplish this by looking at minerals that contain the metals that are present in different minerals and examine their cataly>c ac>vity under the environmental condi>ons that they can form and remain stable

Are there realis6c early‐Earth sepngs that support the “metabolism first”, or the “replicator first” and the encapsula6on models? What about the source sites of cataly6c minerals?

• The answer is there is much we

don’t know

Billion years from human

Origin of Earth (4.5 Gya) Cyanobacteria (the rise of O2) Origin of life?

Thermophilic methanogens, S reducers (thermophilic N‐fixa6on) 4 3 2 1 Anoxygenic photosynthe>c bacteria?(anaerobic)

Accumula6on of O2 Single celled eukaryotes

(beginning of prey/predator associa6ons?)

Algal kingdoms Shelly invertebrates Vascular plants Mammals Humans Time of transi6on from anaerobic microbial ecosystems to aerobic microbial/eukaryo6c ecosystems

Early Earth temperature and O2 produc6on and accumula6on are controversial issues

4 3 2 1 0 1033 1031 1029 1027 1025 1023 1021

K/T Ty

3000 30 0.3 0.003

Time (Ga) Water evaporated (m) Impact energy (J)

• rigin of life

The largest bolide impacts on the Earth and the Moon. Light gray filled boxes are lunar, black filled boxes terrestrial. Red line is inferred earth impact history. Dashed blue line is depth of ocean vaporized by impact. K/T refers to the Cretaceous/Tertiary impact and Ty refers to the lunar crater Tycho (From Sleep et al., 1989)

Life may have started during the heavy bombardment period

• heavy bombardment, while rendering the
• cean water column and any landmass that

may have existed uninhabitable, would not have removed all water from the subsurface and thus would not have sterilized the Earth, but would have resulted in widespread impact‐volcanism (Abramov and Mojzsis, 2009). Did life originate in the subsurface and did volcanism play a role?

Geological sites relevant to the origin of life (Modified from Deamer, 2007)

(modified from Deamer 2007)(

SITE PROPERTIES

Inter-tidal zones, tide-pools, sand Fluctuating environment can concentrate organic solutes Fresh water ponds, lakes Moderate T°C ranges. Low mineral content can be conducive to self-assembly processes. Impacted by lightning, bolides etc. Ice fields Organics can be concentrated in eutectics within ice. Low T°C preserves organic compounds Subterranean geothermal regions T°C range from moderate (40-60°C) to boiling. Reducing power available Magma-hosted Hydrothermal vents T°C range from 2°C (present day) to >400°C with everything in between . Multiple gradients in physical and chemical

• conditions. Reducing power and catalytic minerals available

Peridotite-hosted Hydrothemal vents T°C to >90°C, pH up to 11; high concentrations of CH4, formate, acetate and low MW hydrocarbons; porous calcite for concentration of organic compounds Atmosphere, clouds Water droplets as “cell-like” enclosures for synthesis of complex

• rganic compounds using UV light

Radioactive Beaches (Adam, Astrobiology 2007) The possible role of Actinides (elements with atomic numbers between 89-103) in the abiotic synthesis of organic compounds, polmerization reactions; P release from minerals

The sepngs and metabolism of the earliest microbial communi6es

• All evidence points to hydrogen as the earliest

source of chemical energy (both non‐ photosynthe6c and photosynthe6c organisms)

• Hydrothermal vent environments would have

provided the hydrogen, other vola6les (CO2, sulfur compounds, nitrogen, etc) and key elements to support life

• Evolu6onary phylogeny of extant organisms

support the hypothesis of hydrogen u6lizing, high temperature microbes as ancient groups

Nisbet & Sleep, 2001

The earliest microbial ecosystems might have been biofilms that u>lized H2 as the primary energy source

The earliest evidence for life is found in 3.8 billion year old rocks from hydrothermal sepngs – the chemical and isotopic signatures point to microbial communi6es that used H2 as their energy source and formed “biofilms”

Electron donors, metabolism and vola>le metabolites on an anoxic Earth

(modified from Canfield et al 2006)

Electron donors Environmental settings Metabolism Metabolites in the atmosphere

H2 Submarine hydrothermal vents; subaerial volcanoes Methanogenesis, anoxygenic photosynthesis, SO4

2-, S°, FeIII

reduction, acetogenesis, denitrification CH4, H2S, N2O, N2, CO2 depletion? H2S Submarine hydrothermal vents; subaerial volcanoes anoxygenic photosynthesis NO3

• reduction

N2, decreasing H2S and H2, CO2 depletion? S° Submarine hydrothermal vents; subaerial volcanoes anoxygenic photosynthesis, NO3

• reduction, S disproportionation

N2, CO2 depletion? Fe(II) Submarine hydrothermal vents; subaerial volcanoes anoxygenic photosynthesis, NO3

• reduction

CO2 depletion? N2 CH4 Hydrothermal vents Anaerobic CH4 oxidation CO2 NH4

+

Hydrothermal vents Anammox N2, CO2 depletion? CH2O Hydrothermal vents heterotrophy CO2, H2

Timeline for Archean photosynthesis with proposed reductants (from Olson 2006)

Reductant Ga Marker

H2O 2.3 2.4 O2 level begins to rise H2O 2.5 Hamersley BIF H2O 2.6 Nauga cyanobacteria H2O 2.7 2.8; 2.9 Pilbara methylhopanes Tumbiana stromatolites Fe(OH)+ 3.0 3.1 Protocyanobacteria and Proteobacteria emerge? H2S 3.2 3.3 Swaziland barites H2 3.4 Buck Reef microbial mats (Tice and Lowe, 2006; Sleep 2010) H2S 3.5 3.6; 3.7 Warrawoona evaporites H2 3.8 Isua carbon isotope fractionation

Phototrophic Fe(II)‐oxidizing bacteria (Thodobacter ferrooxidans, Chrorobium ferrooxidans and Thiodictyon sp.) 4Fe2

+ + CO2 + 11H2O + hv → [CH2O] +

4Fe(OH)3 + 8H+ Purple sulfur bacteria (Chlorobiaceae, ChromaNaceae) 2HCO3

‐ + H2S → 2CH2O

+ SO4

2‐

Mul6ple groups of Bacteria and Archaea use H2 as energy source: methanogenesis, Phototrophic Bacteria; S reducers

Anoxygenic photosynthe6c bacteria

PNAS 102:9306‐9310, 2005 Morphology and ultrastructure

• f GSB1 cells. Bar, 300 nm

Chlorosomes

A Green‐sulfur photosynthe6c bacteria was isolated from a submarine hydrothermal vent smoker where the only source of light is geothermal radia6on that includes wavelengths absorbed by photosynthe6c pigments. This organisms is an

• bligate anaerobe and reduces CO2 coupled with oxida6on of

sulfur compounds

Photosynthe6c bacteria 2HCO3

‐ + H2S → 2CH2O + SO4 2‐

Summarizing the case for a subseafloor seong for the origin of life and early microbial ecosystems

• Extensive bolide impacts before 3.8 Ga including ocean

evapora6ng impacts (Maher & Stevenson, 1988; Sleep et al., 1989)

• LiKle con6nental mass before 3.8 GA (Lowe, 1994)
• Extensive hydrothermal ac6vity in the early Archaean

with ridge lengths >5X present (Bickle, 1978; Nisbet and Sleep, 2001)

• Abundant and diverse cataly6c minerals from geophysical

processes

• Extensive temperature, pH and chemical gradients
• Source of Fe/S, C compounds, C‐S compounds, P with

serpen6ne (alkaline hydrothermal systems) thio‐esters

• Sources of thio‐esters, ammonia and phosphate not well

understood

Extreme physical and chemical condi6ons at different vent systems

Magma hosted hydrothermal systems ‐ Most elements required for life

‐ Carbon sources, cataly6c minerals ‐ Temp to >400°C ‐ pH <3; sulfide chimneys

PeridoNte hosted hydrothermal systems ‐ High concentra6ons of H2, CH4 and

• ther hydrocarbons and organic acids

‐ Temp to >90°C ‐ pH to ~11 ‐ Carbonate chimneys

Kelley 2001

Hypotheses

– “Sparseness” , from soup to a few nuts (Morowitz, Smith and Copley) – “protometabolic networks” that produce high concentrations of “key” organic compounds and not an “organic soup”, is a necessary “first step” leading to life – The origin of the “RNA world” required a “protometabolic network” – The genetic code and protein synthesis evolved in the “RNA world” – DNA world: large genomes and free-living cells

The “Molecular Biologists Dream” ‐ a scenario for the origin of the RNA world

The Scenario:

First, forma>on of precursors to nucleic acids on Earth or elsewhere and accumula>on on Earth Next, nucleo6des were formed from prebio6c bases, sugars and phosphates and accumulated in some “special” environment. Next, a mineral catalyst such as a mineral like clays then catalyzed the forma>on of long single‐stranded polynucleo>des some of which were converted to complementary double strands by template‐directed synthesis ‐ this resulted in a “library” of double‐stranded RNA on the primi>ve Earth Next, among the double‐stranded RNAs there is at least one that on mel6ng yields a single‐stranded ribozyme capable of copying itself and its complementary RNA ‐ this would eventually lead to an exponen6ally growing popula6on subjected to Darwinian evolu6on

Condensa6on reac6ons and the forma6on of macromolecules

• Polymeriza6on on clays – proteins and nucleic acids
• Not known how to make a self‐replica6ng RNA

molecule or cataly6c proteins

• Lipids can self assemble into membrane‐like structures

– Very interes6ng studies

The big ques>on is how to get high concentra>ons

• f the precursor compounds (either formed in

situ or concentrated from dilute solu>ons)? This ques>on is crucial in the arguments for and against the “metabolism first” vs the “replicator first” ideas.

The two compe6ng models for the

• rigin of life: “Replicator first”,

“Metabolism first”

Both models involve encapsula6on into small cell like structures usually formed by lipids

(From Shapiro, 2007)

Shapiro favors a “metabolism first” model; his model also starts in an organic soup except that organic compounds are incorporated into compartments that have a beKer chance of developing into a network of autocataly6c cycles and eventually into an informa6on macromolecule.

The Shapiro builds on an idea first discussed by Freeman Dyson (1999) and summarized in one of his famous quotes: “Life began with liKle bags, the precursors of the cell, enclosing small volumes of dirty water containing miscellaneous garbage.”

The “Central Dogma” (left) and the RNA world (right). The transition from the RNA world to the DNA world is thought to have required “reverse transcription”. There are reverse transcriptase enzymes in some RNA viruses including the AID’s virus (Figure from De Duve, 1995)

The “Replicator first” model predicts that RNA preceded DNA, protein and metabolism

The “Molecular Biologists Dream” ‐ a scenario for the origin of the RNA world (from Orgel, no date)

The Scenario:

First, forma>on of precursors to nucleic acids on Earth or elsewhere and accumula>on on Earth Next, nucleo6des were formed from prebio6c bases, sugars and phosphates and accumulated in some “special” environment. Next, a mineral catalyst such as a mineral like clays then catalyzed the forma>on of long single‐stranded polynucleo>des some of which were converted to complementary double strands by template‐directed synthesis ‐ this resulted in a “library” of double‐stranded RNA on the primi>ve Earth Next, among the double‐stranded RNAs there is at least one that on mel6ng yields a single‐stranded ribozyme capable of copying itself and its complementary RNA ‐ this would eventually lead to an exponen6ally growing popula6on subjected to Darwinian evolu6on

A ribozyme that func6ons as an RNA‐dependent RNA polymerase

RNA molecule that can make copies of RNA from an RNA template Requires an RNA template and RNA primer (like in the PCR reac>on) and a mixture

• f the 4 nucleo>des.

It can make an RNA molecule that is only 14 bases long ‐ more work on this is needed

Some progress on the RNA world

Recent research results on the RNA world

• Ribose and nucleo>des have been synthesized

abio>cally (in some cases under unrealis>c early earth condi>ons)

• Polymeriza>on of nucleo>des (oligonucleo>des

20‐50 mers)

– Clays (Huang and Ferris 2006) – Eutec6c phase of water‐ice (Monnard et al., 2003) – Lipid‐bilayer lapces (Rajamani et al., 2007)

• S>ll needed:

– RNA polymerase ribozyme capable of self replica6on – Insight on the emergence of the RNA code (not dependent on the RNA polymerase ribozyme) – The origin and evolu6on of the ribosome – Linking metabolism and replica6on in a “compartment” (the emergence of a “cell”)

Summary of outstanding problems with the RNA world

• Sources (source reac6ons) of the precursors to

RNA (nucleo6des, ribose* and phosphate)

• Abio6c synthesis of RNA from precursors
• The transi6on RNA to self‐replica6ng RNA (RNA

catalysis)

• The transi6on from a self‐replica6ng RNA to the

“gene6c code”, transla6on and transcrip6on

• The origin of the ribosome
• The transi6on from RNA to DNA and the

synthesis of deoxyribose

*Ribose demonstrated to be synthesized in the presence of boron

minerals (Ricardo et al., Science 2004)

Condensa6on reac6ons and the forma6on of macromolecules

• Polymeriza6on on clays – proteins and nucleic

acids

• Not known how to make a self‐replica6ng RNA

molecule or cataly6c proteins

• Lipids can self assemble into membrane‐like

structures

– Very interes6ng studies

Some Hypotheses on the Origin of Life: Sepngs Implica6ons

Primordial soup ‐ heterotrophic origin (Oparin, 1936) Dissipated Structures “Order Out of Chaos” (Prigogine 1980) Submarine Hydrothermal Vents (Corliss et al., 1981) Mineral World (Cairns‐Smith, 1982) RNA World (Gilbert, 1986) Thioester World (De Duve, 1981) Pyrite World ‐ Metabolism first (Wächterhäuser, 1988) Self‐organiza6on and complexity theory (Kauffman, 1993) Fe/S membrane, redox/pH front at vents (Russell, 1994; 1997) Panspermia (Arrhenius, 1908)