This journal is c The Royal Society of Chemistry 2012 Chem. Soc. Rev.

Cite this: DOI: 10.1039/c2cs35112a

Mineral–organic interfacial processes: potential roles in the origins of

lifew

H. James Cleaves II,aAndrea Michalkova Scott,

bcFrances C. Hill,

bc

Jerzy Leszczynski,bc

Nita Sahaide

and Robert Hazenf

Received 2nd April 2012

DOI: 10.1039/c2cs35112a

Life is believed to have originated on Earth B4.4–3.5 Ga ago, via processes in which organic

compounds supplied by the environment self-organized, in some geochemical environmental

niches, into systems capable of replication with hereditary mutation. This process is generally

supposed to have occurred in an aqueous environment and, likely, in the presence of minerals.

Mineral surfaces present rich opportunities for heterogeneous catalysis and concentration which

may have significantly altered and directed the process of prebiotic organic complexification

leading to life. We review here general concepts in prebiotic mineral-organic interfacial processes,

as well as recent advances in the study of mineral surface-organic interactions of potential

relevance to understanding the origin of life.

1. Introduction

Mineral–organic interactions are important for a variety of

modern geochemical phenomena including petroleum forma-

tion and maturation1 and the global carbon cycle.2 These sorts

of interactions were potentially also important for the origin of

life on Earth,3–11 and on extra-terrestrial bodies.

It is notoriously difficult to define ‘‘life’’, which causes

significant problems for efforts to understand its origin (see,

for example, the special section in the journal Astrobiology

(2010) volume 10, pp. 1001–1042). One popular definition is

that life is a ‘‘self-sustained chemical reaction capable of

undergoing Darwinian evolution’’12 (i.e., one capable of

a Blue Marble Space Institute of Science, Washington,DC 20016, USA

bU.S. Army Engineer Research and Development Center (ERDC),Vicksburg, MS 39180, USA

c Interdisciplinary Nanotoxicity Center, Jackson State University,Jackson, MS 39217, USA

dDepartment of Polymer Science, University of Akron,Akron OH 44325, USA

eNASA Astrobiology Institute, University of Akron, Akron,OH 44325, USA

fCarnegie Institution of Washington, 5251 Broad Branch Rd. NW,Washington, DC 20015, USAw Part of the prebiotic chemistry themed issue.

H. James Cleaves II

Dr Cleaves received his PhDin chemistry in 2001 from theUniversity of California,San Diego, then conductedpost-doctoral research at theScripps Institution of Oceano-graphy and the CarnegieInstitution of Washington.His research concerns organicgeochemistry, abiotic organicsynthesis, the question of howlife arose on Earth, methodsfor detecting Life on otherplanets and the interactionsof organic compounds withmineral surfaces. Presently he

is exploring the application of chemoinformatics to prebioticchemistry and the analysis of extraterrestrial materials. He is aresearch scientist at the Blue Marble Space Institute of Science.

Andrea Michalkova Scott

Andrea Michalkova Scott wasborn in Slovak Republic. Shereceived MS in Mathematicsand Chemistry in 1997 andPhD in Inorganic Chemistryin 2002 (working with DanielTunega) from ComeniusUniversity in Bratislava,Slovakia. This was followedby nine years of post-doctoralwork in Jerzy Leszczynski’sgroup at Jackson StateUniversity, Jackson, MS. In2011 she joined the U.S.Army Engineer Researchand Development Center

(ERDC) in Vicksburg, MS where she works now as aResearch Chemist.

Chem Soc Rev Dynamic Article Links

www.rsc.org/csr CRITICAL REVIEW

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replication with mutations which are able to be culled by

natural selection). According to some definitions, this system

must also be membrane-bounded.

The origin of life is generally envisioned as having pro-

ceeded from the formation of organic compounds from

environmentally-supplied precursors, to their self-organization

under various environmental conditions into self-replicating

and energy-transducing systems, and their further evolution

into modern biochemical systems.13,14 These ideas are open to

experimental investigation, where the types of chemistry and

plausible geochemical environments must be given due con-

sideration. For example, models for the origin of life include

schemes for the origin of membranes,15 metabolic cycles10 and

nucleic acids (e.g., the RNA World16), many of which invoke

catalytic or functional roles for mineral surfaces.

Given the many likely available mineral types, and the hetero-

geneity of their surfaces in natural environments,17 mineral

surfaces could potentially have provided almost any type of

general catalysis,18 albeit with low specificity and efficiency. The

ubiquity of mineral–water interfaces at the surface of the Earth

renders it almost impossible to discount the role of interfacial

process with organic molecules relevant to the origin of life.

Modern biochemistry mainly uses protein enzymes, which

are genetically-encoded polymers of a-amino acids, as cata-

lysts. Many of these include a cofactor such as an organic

coenzyme, a metal sulfide cluster or a metal ion. Some

enzymes have evolved to be almost perfect catalysts, in that

they represent an exquisite balance between the affinity of the

catalyst for both substrate and transition state binding, and

product release.19–21 Such enzymes provide rate enhancements

of as much as 1020 fold for specific chemical reactions, though

more typical values are on the order of 106 to 1015-fold).22 The

reasons evolution selected a-amino acids to construct catalysts

remain speculative,23,24 but recent laboratory results suggest

that once formed, such enzymes were able to explore an almost

limitless catalytic space.25

Frances C. Hill

Frances C. Hill is a native ofCleveland Heights, OH. Shereceived a BA in Chemistryfrom Case Western ReserveUniversity,MS in Geochemistryfrom Purdue University,and PhD in Mineralogy/Geochemistry from VirginiaTech. She completed post-doctoral research at theUniversity of Notre Dame,and Rutgers University. Shespent eight years at the ArmyHigh Performance ComputingResearch Center inMinneapolis,MN, as the lead computational

chemist. Since 2007 she has worked as a Research Chemist/Team Leader for the computational chemistry team at the USArmy Engineer Research and Development Center (ERDC) inVicksburg, MS.

Jerzy Leszczynski

Jerzy Leszczynski is aProfessor of Chemistry andthe President’s DistinguishedFellow at Jackson StateUniversity (JSU). He joinedthe faculty of the JSU Depart-ment of Chemistry in 1990. Hedirects the InterdisciplinaryNanotoxicity CREST Centerat JSU. His broad researchinterests include variousapplications of computationalchemistry. Dr Leszczynskiobtained his MS and PhDdegrees at the TechnicalUniversity of Wroclaw in

Poland, where he was also a fculty member from 1976–1986.In 1986 he moved to the USA, initially working at the Universityof Florida, Quantum Theory Project (1986–88) and at theUniversity of Alabama at Birmingham (1988–1990).

Nita Sahai

Professor Nita Sahai has beenthe Ohio Research Scholar Chairin Biomaterials, Departmentof Polymer Science, Universityof Akron since August 2011.Prior to this, she was aProfessor in the Departmentof Geoscience, University ofWisconsin-Madison for 11 years.Prof. Sahai’s research focuseson the physical-chemicalaspects of cellular and bio-molecular interactions atmineral surfaces, of relevanceto prebiotic chemistry, bio-mineralization and bone tissue

engineering. Her research is supported by NSF, NASA andACS-PRF. Prof. Sahai has been interviewed on National PublicRadio’s, ‘‘To the Best of Our Knowledge,’’ for her research onthe origin of life.

Robert Hazen

Robert M. Hazen, SeniorResearch Scientist at theCarnegie Institution ofWashington’s GeophysicalLaboratory and the ClarenceRobinson Professor of EarthScience at George MasonUniversity, received the BSand SM in geology at theMassachusetts Institute ofTechnology (1971), and thePhD at Harvard Universityin earth science (1975).The Past President of theMineralogical Society ofAmerica, Hazen’s recent

research focuses on the possible roles of minerals in the originof life. He is also Principal Investigator of the Deep CarbonObservatory (http://dco.ciw.edu).

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Biological systems are required for the production of

protein enzymes, so what molecules or phases could have

catalyzed pre-biotic polymerization, ‘‘proto-metabolism’’ and

‘‘proto-self replication’’? Abiotic organic catalysis might have

been sufficient, but mineral surfaces could also have provided

an almost limitless array of catalytic sites which could have

contributed to prebiotic organic complexification. In contrast

to biological enzymes, however, mineral surfaces were likely

not genetic, in the sense that there were no feedback loops for

the regeneration of the catalyst and, thus, no Darwinian

evolution in the strict sense. On the other hand, there have

been suggestions that minerals might initially have been

genetic systems,26 and it has been suggested that metal-sulfide

co-factors may be relicts of primordial surface-promoted

chemistry.27 Thus, mineral surfaces may have served to

jump-start, if not sustain, the complexification of organic

matter.

Minerals lack the enormous combinatorial diversity of

organic compounds. There are B4500 known naturally occur-

ring minerals,28 with formula weights on the order of a few

hundred to a few thousand daltons. This same molecular

weight range includes a vastly larger number of organic

compounds. For example, a recently computed set of com-

pounds containing only up to 13 total C, N, O, Cl or S atoms

contained 9.77 � 108 compounds, and these were pre-filtered

for their drug-like properties, greatly reducing the size of the

final library.29 This relative paucity of combinations in terms

of structure and composition may be a benefit in making the

experimental exploration of mineral surface catalytic potential

considerably more tractable.

We review here the literature on the topic to date, and

attempt to highlight blind spots that could be addressed by

experimental and computational approaches in future studies.

We will set the stage by exploring which kinds of minerals and

organic compounds were likely on early Earth, and which

geochemical environments might plausibly have brought them

together. We then review studies in mineral-organic inter-

actions of possible relevance to the origin of life, and conclude

with a more detailed discussion of some recent computational

approaches.

We will not consider the potential role of water or other

volatile ices on prebiotic chemistry. While ice is a recognized

mineral species, and it is likely that ice interacted with

chemical species of relevance to the origin of life during the

early history of the solar system, chemistry occurring in ice

phases is complex, and may include ice surface promoted

effects as well as eutectic concentration effects. For further

description of ice chemistry of prebiotic relevance, the

interested reader is referred to ref. 30–34.

2. Plausible minerals, organic compounds and

environments on early Earth

2.1 Formation of the elements (nucleosynthesis), stars, the

solar system and minerals

Chemical compounds can be broadly classified as organic or

inorganic depending on the quantity and oxidation state of the

carbon they contain. Compounds of both types are widely

dispersed throughout the observable universe. We briefly

review the formation of both types of compounds.

Most of the chemical elements heavier than Li were pro-

duced in the interiors of large stars shortly after the Big Bang,

then dispersed later during supernova events.35 This process

resulted in a generally decreasing abundance with atomic

number, with exceptions that are attributable to fusion cycles

that occur in stellar interiors. 56Fe is especially abundant,

because it is the most stable element that can be synthesized

easily from a-particles. Silicon (Z = 14) and oxygen (Z = 8)

are also especially common as they are so-called ‘‘even-nuclei’’

elements and, thus, the silicates (containing SiO4 subunits) are

also cosmically abundant.

Much of the solar nebula was initially composed mainly of

H and He, the two most cosmically abundant elements, but

also included the entire periodic table of elements,36 resulting

in the elemental distribution known as the solar abundance.

During the formation of the solar system, molecular com-

pounds were sorted in terms of distance from the sun approxi-

mately according to their boiling points. Radial mixing,

however, scattered these compounds in smaller amounts

throughout the early solar system. Lighter, more volatile

compounds generally froze in the outer regions of the solar

system, giving rise to the cometary bodies of the Oort cloud

and Kuiper belt as well as the gas and ice giant planets and

their moons, whereas the heavier, more refractory elements

were concentrated in the inner solar system giving rise to the

terrestrial planets, Mercury, Venus, Earth and Mars, and the

asteroid belt. Asteroids are rocky bodies that did not accrete to

the terrestrial planets, thus, being the ‘‘leftovers’’ of planet

formation.36

The terrestrial planets are ‘‘rocky’’. Rocks are aggregates of

minerals. A mineral is a naturally-occurring inorganic com-

pound that has a fixed chemical composition or range of

compositions and a specific crystal structure. On Earth and

other rocky planets, primary minerals are formed from cooling

and crystallization of magma (a mixture of molten or semi

molten rocks, volatiles and solids). Transformation of primary

minerals by weathering and alteration at planetary surfaces

produces secondary minerals.

Rocky planets are thought to be especially suited as abodes

for life because they provide a solid surface that can support

the presence of liquid water and temperatures that allow for

the existence of liquid water. These conditions may require a

planet to be relatively near to its parent star, which would

require the planet to be largely composed of refractory

(or high-boiling point) inorganic components such as metal

oxides and silicates.

Liquid water on rocky planets. It is generally presumed that

liquid water is a pre-requisite for life.37 The stability of liquid

water requires a planet to be close enough to its star that the

surface temperature is above freezing but distant enough to

prevent boiling.38 Some of Earth’s water inventory is believed

to have been delivered by bolides, including meteorites and

comets.39 Bolide impact rates would have been much greater

early in Earth’s history when the planet was accreting from

rocky planetesimals similar to the asteroids.40 The Earth

is B4.54 Ga old, and the period up to B3.8 Ga is called

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the Hadean (derived from hades, the name of the Greek

underworld) eon, because Earth’s surface temperatures were

believed to have been much higher than the boiling point of

water. Oxygen isotopes in the oldest known terrestrial zircons

discovered recently, suggest liquid water may have been pre-

sent on Earth’s surface as early as 4.3 Ga41 to 4.4 Ga.42 These

results push back to the earliest stages of Earth’s history and

provide a considerably longer time-span for surface temperatures

compatible with liquid surface water (‘‘cool early Earth’’) and,

consequently, the self-assembly of organic molecules into

replicating systems.

The bolide impact assumed to have been responsible for

formation of the Moon would have re-melted the entire Earth

B4.5 Ga, and there may have been a period called the ‘‘Late

Heavy Bombardment’’ (LHB) B3.8 Ga when meteoritic

impact rates increased briefly and surface temperatures may

have been frequently elevated above the boiling point of

water.43 While some have seen the LHB as a restriction for

when the origin of life could have occurred, others suggest life

could have survived the LHB,44 and others have questioned

whether the LHB occurred as interpreted.45

The oldest known accepted microfossils date from B3.5 Ga

and are associated with shallow marine evaporitic environments.46

Thus while early cells may have survived in sub-surface

environments, which seems plausible given that modern

bacteria have been found as deep as 2.8 km in mines,47 early

life either rapidly colonized or re-colonized surface environ-

ments. Alternatively, early life may not have survived the LHB

and may have evolved a second time on Earth. In any event,

the presence of lower surface temperatures and liquid water on

Earth’s surface would have resulted in rapid weathering of

Earth’s primary surface minerals, increasing the mineral types

available for interaction with prebiotic organics.

There is considerable evidence that Earth’s mantle and core

differentiated rapidly, and that the oxidation state of Earth’s

mantle has been at its current state since B4.35 Ga.48 The

oxidation state of the mantle would have governed the oxida-

tion state of the gases emitted by volcanism. It is, therefore,

often presumed that the amount of CO2, SO2 and NO2 in the

atmosphere would have been much higher than in the modern

atmosphere, and would likely have resulted in acidic oceans.49

Alternative scenarios envision alkaline early oceans.50,51

It remains possible that on the early Earth, as today, there

were a variety of local and microenvironments in which a wide

range of conditions, such as pressure, temperature, pH, exposure

to light and oxidation state of volcanic out-gassing.

The prebiotic distribution of mineral species. The possible

roles of mineral surfaces in protecting, selecting, concen-

trating, templating, and catalyzing reactions of prebiotic

organic molecules are recurrent themes in discussions of

life’s origins. Since the pioneering suggestions of Bernal5 and

Goldschmidt,3 who independently speculated on the possible

influences of various minerals in the origins of life, many

authors have proposed general principles and detailed scenarios

for mineral-assisted biogenesis.52–56

Among the specific mineral groups that have been invoked,

clay minerals are the most frequently cited.57–69 Various

transition metal (e.g., Fe, Ni, Co and Cu) sulfide minerals

have also been proposed to have played key catalytic roles in

prebiotic organic synthesis.10,27,70–86 Many other minerals

have also been proposed, including quartz,87–89 feldspar,90,91

zeolites,90,91 olivine,92,93 rutile,94,95 ferrous metal alloys,96

transition metal phosphides,97 transition metal hydroxides,8,98,99

micas,100 hydroxylapatite,101–103 alkaline earth metal carbonates104

and borates.105,106

In spite of these numerous proposals, few authors have

addressed the question of which minerals might actually have

been present on the prebiotic Earth (Tables 1 and 2) (see,

however, ref. 107 and 108). If a particular mineral phase was

rare or absent, then it is unlikely to have been a significant

contributor to the origins of life.

The hypothesis of ‘‘mineral evolution’’, which outlines

10 stages of near-surface mineral diversification since the

beginning of the Earth, offers some insight to this question.28,109

The starting point of mineral evolution is a group of a dozen

‘‘ur-minerals’’ that condensed during the cooling and expan-

sion of the gaseous envelopes of supernovas and red giant

stars—those that are enriched in ‘‘heavy’’ element (i.e., Z Z 6).

Diamond was probably the first mineral in the cosmos, owing to

its high temperature of crystallization (B4400 1C) and the

significant concentration of carbon in the atmospheres of large

active stars. The graphite polymorph of carbon; moissanite (SiC);

the nitrides, osbornite (TiN) and nierite (Si3N4); the oxides,

Table 1 Minerals identified in Eoarchaen (B4.0–3.6 Ga) mineral deposits (adapted from ref. 108). *Protolith ambiguous

Rock Type Possible Protoliths Major Minerals Minor Minerals

Metavolcanicrocks

komatiite, amphibolite,ultramafic rock

olivine, clinopyroxene, garnet,orthopyroxene, biotite, chlorite,amphibole (hornblende)

serpentine, antigorite, magnetite, talc, magnesite, epidote,phlogopite, kyanite, chromite, rutile, ilmenite, sulfides,dolomite, calcite, K-feldspar, plagioclase, cordierite, apatite

Banded ironformation

BIF, ferruginouschert

quartz, magnetite, amphibole clinopyroxene, orthopyroxene, olivine, garnet, chlorite,tremolite, calcite, magnesite, hematite, goethite, apatite,sulfi des, zircon, graphite

Schist(metapelite)

ferruginous shale,mudstone, siltstone,argillite

quartz, biotite, amphibole,garnet, chlorite

muscovite, sillimanite, kyanite, staurolite, andalusite,cordierite, plagioclase, epidote, microcline, clinozoisite,tourmaline, magnetite, ilmenite, rutile, graphite, sulfides, zircon

Quartzite chert, sandstone* quartz, amphibole magnetite, clinopyroxene, orthopyroxene, biotite, chlorite,epidote, plagioclase, zircon, fuchsite, hematite, sulfides,carbonate

Calc-silicate andmetacarbonaterocks

Metasomatic contact*hydrothermal edifice*

quartz, siderite, dolomite, calcite,ankerite, magnesite, magnetite

clinopyroxene, orthopyroxene, olivine, amphibole, garnet,phlogopite, biotite, feldspar, muscovite, chlorite, epidote,fuchsite, apatite, hematite, sulfides, graphite

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rutile (TiO2), corundum (Al2O3), spinel (MgAl2O4), hibonite

(CaAl12O19); and the silicates, forsterite (Mg2SiO4) and

enstatite (MgSiO3), have also been discovered as micro- or

nano-particles in pre-solar dust grains (inter-planetary dust

particles).110–113 All of these refractory minerals condensed at

temperatures above B1900 1C and likely formed within the

first hundred million years following the Big Bang. The

refractory minerals have been present continuously on Earth

since its formation.114

A principal objective of ‘‘mineral evolution’’ research is to

document the mechanisms and timing by which these dozen

minerals were processed in the solar nebula, planetesimals and

on Earth to generate the more than 4500 mineral species

known today. One significant result of this research is the

proposal that the great majority of minerals—perhaps

3000 species of the B4500 currently known—arose after the

Great Oxidation Event at B2.2 Ga and, thus, are a con-

sequence of life’s influence on the chemical state of the oceans

and atmosphere.28,115 Furthermore, many rare elements,

including Li, B, Be, Hg, Se, As, Bi, Sb, U, and Th and many

others, required at least a billion years of fluid-rock inter-

actions to achieve sufficient concentration to form new

minerals.106,114,116–119 Thus as many as 1000 additional minerals

formed abiotically must postdate the time of life’s origins. We

conclude, therefore, that the great majority of minerals—

perhaps as many as 4000 of the 4500 known species—could

not have contributed to life’s origins. In that context, which

mineral phases were present 4 billion years ago?

Stage 1 of mineral evolution, which occurred during the first

few million years following the Sun’s earliest radiative phase

(beginningB4.567 Ga),120 incorporates approximately 60 minerals

that condensed in the early solar nebula to form the primitive

chondritic meteorites.28,121 This includes all of the dozen

ur-minerals, plus a variety of Mg–Al–Ca–Fe silicates and

oxides, Ni–Fe–Mg–Mn–Ca sulfides, Fe–Ni phosphides, and

Fe–Ni metal alloys.

Stage 2, which encompasses mineralogical consequences of

the accretion of chondrites, the differentiation of planetesimals,

and the subsequent processing in those planetesimals by

thermal metamorphism, aqueous alteration, and impact

shocks, saw a cumulative total of approximately 250 different

minerals.121,122 Among the key new minerals formed in stage 2

are the first significant accumulations of feldspars, phosphates,

and clay minerals. All of these phases are found in meteorites,

and all have thus been present continuously at or near Earth’s

surface for more than 4.5 billion years.

Subsequent mineral evolution on the young Earth resulted

from the sequential evolution of igneous rocks, including the

stage 3 generation of basaltic magmas from partially molten

peridotite, and the subsequent stage 4 generation of granitic

melts by partial melting of basalt (e.g. ref. 123 and 124).

Terrestrial mineralogical diversity also increased by the forma-

tion of hydrous minerals, notably hydroxides, clays and zeolite

minerals, as well as localized deposits of evaporate minerals.

Hazen et al.28 estimated that igneous magmatic differentiation

and near-surface processes resulted in B500 different mineral

species. However, subsequent mineralogical diversification

required significant time. For example, London125 estimated

that a billion years was required for the generation of complex

pegmatites that represent eutectic fluids enriched in rare

elements. Approximately 500 minerals, including a variety of

Li, Be, Cs, Nb, Ta, U, Th and other species, are unique to

these deposits. Subduction and associated abiotic mineraliza-

tion associated with arc volcanism also generates hundreds of

new mineral species, for example massive sulfide deposits that

contain more than 100 exotic sulfosalts (metal sulfide minerals

with one or more other chalcogenide elements, for example,

Se, As, Sb, or Bi). However, recent studies suggest that

subduction-driven plate tectonics, and associated continent

formation and arc volcanism, did not become a significant

process on Earth until approximately 3 billion years ago.126

In summary, many of the minerals mentioned above which

are commonly-invoked for the origin of life were almost

certainly present on the surface of the early Earth. Various

sulfides, most notably those of Fe and Ni, were ubiquitous if not

plentiful, along with meteoritic Fe–Ni alloys and phosphides,

Table 2 Minerals modeled to be likely products of primordial basalt weathering under 5 atm CO2. Adapted from ref. 107

Mineral Class Formula

Amesite Silicate, Serpentine group (Mg2Al)(SiAl)O5(OH)4Brucite Hydroxide Mg(OH)2Calcite Carbonate CaCO3

Celadonite Silicate, Illite group KMg0.8Fe2+

0.2Fe3+

0.9Al0.1Si4O10(OH)2Chalcedony Oxide SiO2

Clinoptilolite Silicate, Zeolite group (Na,K,Ca)2-3Al3(Al,Si)2Si13O36�12(H2O)Daphnite Silicate, Chlorite group (Fe,Mg)5Al(Si,Al)4O10(OH)8Dawsonite Carbonate NaAl(CO3)(OH)2Diaspore Hydroxide a-AlO(OH)Dolomite Carbonate (CaMg)CO3

Greenalite Silicate, Serpentine group (Fe2+, Fe3+)2-3Si2O5(OH)4Gyrolite Silicate, Mica group Ca4(Si6O15)(OH)2�3H2OMagnesite Carbonate MgCO3

Mesolite Silicate, Zeolite group Na16Ca16(Al48Si72O240)�6H2OMontmorillonite Silicate, Smectite group (Na,Ca)0.33(Al,Mg)2(Si4O10)(OH)2�nH2ONontronite Silicate, Smectite group Ca0.5(Si7Al0.8Fe.2)(Fe3.5Al0.4Mg.1)O20(OH)4Portlandite Hydroxide Ca(OH)2Prehnite Silicate, Sheet silicate Ca2(Al, Fe3+)(AlSi3O10)(OH)2Saponite Silicate, Smectite group Ca0.25(Mg,Fe)3((Si,Al)4O10)(OH)2�n(H2O)Siderite Carbonate FeCO3

Stilbite Silicate, Zeolite group NaCa4[Al9Si27O72]�30H2O

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although the abundance of these latter categories may have

been limited to a lower steady-state concentration due to

their lability. Feldspar, olivine, rutile, hydroxides and zeolite

minerals would also have been readily available, and are thus

reasonably invoked in origin of life scenarios. In contrast,

neither quartz nor phosphates were volumetrically significant

prior to 4.0 Ga, but increased rates of granitization would

have produced more quartz, alkali feldspar, and hydroxy-

lapatite from 4.0 to 3.5 Ga. The presence of Hadean and

Paleoarchean (B3. 6–3.2 Ga) carbonates is as yet unconfirmed

(e.g. ref. 108), and there is no evidence for any borate minerals

prior to 3.5 Ga.106 This may be due to the relatively greater

solubility of these minerals compared to the others discussed

above.

The diverse group of fine-grained layer silicates, collectively

called clay minerals, deserve special mention. Clay minerals,

especially from the montmorillonite group, are often

employed in origins of life experiments, because of their high

specific surface area and the ability of certain clay minerals to

absorb organic molecules. Confusion arises, however, because

there are more than 50 distinct approved phases, as well as

many mixed phases, such as bauxite, bentonite, phengite and

steatite that are sometimes characterized as clay minerals.

These diverse phases can be grouped into seven major clay

mineral groups, each of which is distinguished by its layered

atomic structure, its interlayer constituents and its relative

ability to expand in water.127,128

Elmore128 noted five principal mechanisms of clay mineral

formation: (1) subsurface aqueous/hydrothermal alteration;

(2) authigenesis, described as in situ formation from a parent

mineral, especially from pore-solution in marine sediments;

(3) low-grade metamorphism to greenschist facies, representa-

tive of temperatures of B400 to 500 1C and depths of about

8 to 50 km, with subsequent exposure through orogenesis

(mountain-building) related to plate tectonics; (4) near-surface

weathering reactions, especially under oxic and/or acidic

conditions; and (5) the rise of the biosphere, most notably

the advent of soil-forming microbes, fungi and plants, and

associated biological weathering. Of these five mechanisms,

only the first (via serpentinization) and anoxic near-surface

weathering would have been significant prior to 3.5 Ga. Earlier

authigenesis (mechanism 2) was limited by the dearth of

Hadean and Paleoarchean marine sediments; greenschist

facies rocks (mechanism 3) were rarely exposed at the surface

prior to the onset of plate tectonics which is estimated by some

to have begun by at leastB2.5 Ga; the atmosphere was devoid

of O2, so oxic weathering (mechanism 4) could not have

occurred; and there was no biologically-mediated weathering

(mechanism 5). We conclude that most clay minerals observed

in modern sediments would not have occurred in any signifi-

cant volume prior to 3.5 Ga. Indeed, the only major clay

mineral species prior to life’s origins was probably serpentine,

the product of aqueous alteration of olivine and other ferro-

magnesian silicates in the ubiquitous mafic and ultramafic

rocks of the early crust.129 Alteration of Ca–Al silicates,

including the plagioclase feldspar anorthite, must have

resulted in some production of montmorillonite, kaolinite as

well as halloysite, and mixed clay assemblages would also be

expected in such alteration zones. The only other significant

mechanism of clay mineral production may have been the

weathering of volcanic rocks in acidic surface environments,

resulting in montmorillonite. In summary, serpentine and

montmorillonite would have been the dominant clay minerals

before 3.5 Ga.

The above discussion suggests that most of the minerals

invoked for origins of life research would have been present on

Earth prior to 3.5 Ga. In the following pages we consider

recent approaches to understanding the nature of those

interactions.

Available early environments. The vast majority of Earth’s

mass is contained in its core and mantle, yet the most

important minerals with respect to the origin of life were those

present at the surface from volcanism and extraterrestrial

delivery, and the corresponding secondary minerals produced

from weathering at Earth’s surface.28 Most organic com-

pounds of modern biochemical relevance are composed of

simpler moieties, and include heteroatoms such as nitrogen,

sulfur and oxygen, as for example in amino acids, sugars and

nucleobases (NBs). It is widely believed that life formed from

these simpler organic compounds (see, for example, ref. 130).

Such molecules are, however, not particularly stable at high

temperatures for extended periods of time.131–133 Thus, it is the

minerals that come into contact with Earth’s hydrosphere at

moderate temperatures, which were likely of greatest relevance

to origin of life. This assumption still leaves an enormous

inventory of minerals of potential relevance, and numerous

plausible environments, with the two types most discussed in

the literature being shallow evaporative environments and

submarine hydrothermal fields.

Modeling studies of basalt weathering under putative early

atmospheric conditions suggest a complex suite of secondary

minerals107 (Table 1). Petrographic evidence suggests that the

minerals shown in Table 2 were already present on the surface

of the primitive Earth by 4.0–3.6 Ga, and perhaps somewhat

earlier,108 confirming and extending the conclusions of

Schoonen et al.107 and Hazen et al.28

A variety of possible environments could plausibly satisfy

the criterion of being in contact with the primitive hydrosphere

at reasonably low temperatures. These include sub-aerial

environments on nascent continents or island arcs including

beaches and inland hydrothermal springs,134 as well as sea-

floor environments including sediments and environments

associated with rising mantle plumes or sea-floor spreading

centers.135–137 Recently, the remarkable properties of pumice,

perhaps occurring in floating pumice rafts, as a possible site

for the origin of life has been suggested.138 During eruption

pumice develops the highest surface-area-to-volume ratio

known for any rock type and is the only known rock type

that floats at the air–water interface. Pumice can be exposed to

an unusually wide variety of conditions, including dehydration

under atmospheric interfaces. As will be discussed, for many

biochemically relevant condensation reactions, the elimination

of water is particularly important. These porous rocks can

adsorb metals, organics, and phosphates and host inorganic

catalysts such as zeolites and titanium oxides. A caveat to

the idea of pumice serving as an environment for the origin

of life, however, is that most pumices are acidic (felsic) to

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intermediate in composition, and basaltic compositions are

rarer. The abundance of typical acidic – intermediate compo-

sition pumices on early Earth before widespread formation of

continents is open to further investigation.

Evaporitic environments. Shallow surface environments,

such as intertidal zones and inland lakes (e.g., the Great Salt

Lake), offer the obvious advantages of being in direct contact

with atmospheric and extraterrestrial sources of prebiotic

organics, and providing locations for concentration of molecules

and ions by evaporation.139 These environments, however,

would also have been subject to higher ultraviolet radiation

(UV) fluxes, as it is generally believed that as the primitive

atmosphere contained little free O2, and consequently little

ozone (O3), thus providing little shielding from the higher UV

output of the early Sun.140 On the other hand, other atmospheric

and oceanic mechanisms may have offered UV-shielding.141,142

For example, even thin sediment layers in shallow or subaerial

environments could have completely shielded organic com-

pounds form UV radiation.141,143 Seafloor environments would,

likewise, have shielded organics from UV exposure.

Mineral surface – catalyzed photolysis may have been a

significant source of organics and reduced nitrogen species,144–146

and may also have been a significant mechanism for organic

destruction. Indeed, minerals have been implicated via UV

induced photodegradation in explaining the absence of organic

compounds on Mars.147

Typical sedimentary minerals include clay minerals, zeolites,

oxyhydroxides of iron, aluminum and manganese, calcite,

diatomaceous silica, pyrite and various evaporitic minerals

such as calcite, gypsum, epsomite, and halite (see Tables 1

and 2). Clay minerals are especially significant as they have

high specific surface areas and are often the final weathering

products of basaltic minerals, so adsorption of organic com-

pounds on clay minerals has been studied extensively. Clay

minerals appear to be common on the surface of Mars,148 as

do evaporitic minerals such as hydrated sulfates.149 Many

other minerals also have high specific surface areas such as

zeolites, oxyhydroxides of iron, aluminum and manganese,

calcite, amorphous silica and pyrite, but these have not been

studied as extensively in the origin of life literature.

Submarine environments. Marine hydrothermal vents, both

high – temperature sulfide – dominated ‘‘black smokers’’ and

lower – temperature carbonate – dominated ‘‘white smokers’’,

associated with submarine, ocean ridge spreading centers have

attracted a good deal of attention as possible sites for the

origin of life.10,150,151 Such environments may provide a

variety of advantages over subaerial locations, including the

UV shielding problem. Hydrothermal vents also offer sites

with continuous thermal and concentration gradients of

molecules. It has, therefore, been proposed that the vents

may be good sites for abiotic organic synthesis, especially

if the atmosphere was not particularly reducing. Mineral

surface – catalysis provided by hydrothermal minerals such

as sulfides has been suggested as an important aspect of the

potential for organic synthesis in these environments.82,84

While submarine environments may offer an alternate loca-

tion for prebiotic organic synthesis, means of concentrating

what must have been rather dilute organics are not as obvious

as in evaporitic environments. Mineral surface adsorption

offers one possibility. Recently, thermophoresis, in which

organics are concentrated in mineral pores subject to thermal

gradients, has been suggested as another possible mechanism,152

and some experiments support this idea.153

Models for the origin of life. As mentioned above there is

presently only a broad idea of how life originated on Earth.

Most modern models for this process assume the presence

of one or more types of molecules found in present-day

biochemistry, for example lipids, nucleic acids, amino acids

or small metabolites such as Krebs cycle intermediates (for

general reviews see ref. 154–156).

One major schism in modern hypotheses is that between

replicator-first and metabolism-first models. Replicator – first

models (‘‘RNA world’’) generally assume that a primordial

genetic molecule initiated Darwinian evolution, and thus consider

the prebiotic synthesis of RNA or someRNA-like molecule as the

central problem in the origin of life.154,155,157,158 Metabolism-first

models generally focus on the prebiotic synthesis of metabolic

intermediates and their cyclic interconversion,10,159 or on the

synthesis of small catalysts such as peptides.63,160 The two models

need not be mutually exclusive,161 and mineral surface adsorption

phenomena may have assisted both.162

Likely available organics. A variety of processes likely

contributed to early Earth’s (and possibly early Mars’) organic

inventory, including processes such as atmospheric synthesis,

extra-terrestrial input, from bolide impact and geothermal and

planetary surface syntheses.163

The organic products of the action of ultraviolet light, high

energy radiation and electric discharges acting on various

types of gas mixtures have been the subject of extensive

investigation since Miller’s pioneering 1953 experiment.164

Extraterrestrial sources, such as meteorites, micrometeorites

and comets could also have been important sources of pre-

biotic organic compounds.40 Submarine hydrothermal systems

have been offered as additional sites of organic synthesis.151

Surface-water photochemistry may also have been an impor-

tant source of reduced organics, as it has been suggested that

great quantities of ferrous iron (Fe2+) were present in the

early oceans because of early Earth’s low atmospheric

pO2. This Fe2+ could have served as a reductant for

bicarbonate, yielding appreciable amounts of reduced one-

carbon species.165

Rather than describe all of the nuances and variations in

prebiotic synthesis that have been investigated over the years

(for reviews of this topic see ref. 154, 156 and 166) we stress

that some, but by no means all, biochemicals have robustly

demonstrated-prebiotic syntheses and could have been plau-

sibly present in certain terrestrial environments prior to the

origin of life. As an important cautionary note regarding the

potential organic complexity in the primitive environment, a

recent investigation of the Murchison meteorite has shown

that there remain perhaps millions of as-yet-unidentified

organic compounds which could also have been present.167

For the purposes of this review, neither the specific model

for the origin of life nor the specific type of organic compounds

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necessary for its occurrence will be considered of paramount

importance, as too little is known to make strong statements

about these questions, and the interactions between mineral

surfaces and organic compounds are generalizable based on

other considerations. We will focus instead on ways in which

mineral–surface interactions could have contributed to the

complexification of organic compounds via concentration

and catalysis.

3. Mineral–organic interactions of potential

relevance to the origin of life

Mineral surfaces as adsorbants

Perhaps the simplest and most important role that mineral

surfaces could have played in prebiotic evolution is as sites for

concentrating organic compounds, as suggested early in the

modern history of thought on the origin of life.5,168 The

assumed mechanism for this is adsorption, which simply

implies that dissolved species are concentrated at mineral

surfaces due to kinetic or thermodynamic factors, mediated

by various forms of interaction including solvophobic effects,

and covalent, ionic and weak electrostatic and van der Waals

interactions.

Surface adsorption of organic compounds could be a parti-

cularly efficient means of sorting molecules from complex

mixtures, either by removing molecules which interfere in a

given solution-phase reaction, or by leaving undesirable

molecules in solution, and concentrating desired ones in the

adsorbed state.

Equilibrium adsorption is usually described using iso-

therms, or plots of the quantity of a given species per unit of

solid adsorbant at various solution compositions and at a fixed

temperature. Various units for the adsorbed species may be

reported, including molecules, moles or mass. The choice of

units for the adsorbing solid phase is, typically, given in units

of mass or specific surface area (area per unit mass of solid).

It is important to recognize that the same mineral phase may

have a widely varying specific surface area depending on its

source or means of synthesis.

Generally speaking, adsorption can be considered as an

equilibrium between dissolved and adsorbed phases of the

same species. The affinity of organic molecules for surfaces can

vary widely depending on their size, available functional

groups, solubility, and charge, as well as the properties of

the mineral surface, such as surface charge, dielectric constant,

and crystal structure,169 under the conditions of the measure-

ment. The experimental variables include, for example, pH,

temperature, ionic strength, presence of inorganic ions which

may facilitate adsorption by forming salt bridges and/or by

modulating solvophobic effects, and all these factors may

affect the speciation of mineral surface sites. It is typically

found, however, that the greater the solution concentration

of a species, the greater the number of surface adsorbed

molecules (Fig. 1).

The simplest method for studying mineral–organic inter-

actions is the batch isotherm method. In this type of study,

an aliquot of mineral powder is added to a solution containing

an organic compound of interest, at a fixed solution pH

and ionic strength. The amount adsorbed is assumed to be

the amount of solute lost from solution after interaction with

the solid particle suspension. In many studies the results are

reported in terms of mass or moles of compound adsorbed per

unit weight of mineral. This is unfortunate because the surface

area of the mineral is of primary importance and determines

the ratio of surface area to solution volume and concentration.

For example, a given surface area of mineral will not adsorb

the same amount of solute from 1 ml of solution of a given

concentration as from 100 ml of a solution containing the

same concentration of solute.

Adsorption can be often be described by a Langmuir type

isotherm, which displays a steady rise in adsorption with

increasing concentration of solute until reaching an asymptotic

maximum representing a complete monolayer of adsorbed

species. In some cases, however, this is a gross over-simplification

and Langmuir-type adsorption behavior is commonly not

observed, as species may adsorb in multilayers or adsorb

cooperatively either with other molecules of the same type or

with some other dissolved species, for example a dissolved

inorganic ion. Also, if the data follow a Langmuir-type

isotherm, it does not confirm the single-site, monolayer

adsorption mechanism. Adsorption mechanisms must be

determined by spectroscopic analyses in situ.

Importantly for discussions of adsorption behavior in

natural environments, the higher the ratio of solvent-accessible

solid surface area to solvent volume, the closer the adsorbed

molecules will be to one another. The closer the adsorbed

molecules are to one another, the greater the likelihood that

Fig. 1 Schematic showing the general tendency for adsorption of

molecules (spheres) to increase with increasing (a. - c.) solute

concentration at a fixed volume to mineral surface (plane) area ratio.

The arrows in the figure represent the direction of motion of solute or

solvent molecules.

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they will interact with one another, underscoring the need

for some sort of initial concentration mechanism such as

evaporation or thermophoresis for pre-biotic synthesis. For

homogeneous intra-molecular catalysis in solution, however,

concentration need not be an important factor.

Based on modern Earth’s radius, the Earth’s surface area is

B5.1 � 1013 m2, with B71% or 3.6 � 1013 m2, covered by

water. The modern ocean volume is B1.3 � 1021 L, giving a

volume to surface area ratio of B3.6 � 106 L m�2. This ratio

could scale � several tens of percent given that there was likely

less continental surface area early in Earth’s history, and that

the ocean volume may have changed somewhat over time.

However, it is critical to recognize that Earth’s surface area is

highly fractal, with the ocean floor often being covered with

many meters of sediment, mud or ooze, giving a solvent-

accessible surface area thousands to millions of times greater,

and a consequently greater ratio of solid surface area to water

volume, presenting considerably more sites for adsorption.

Lahav and Chang conducted an important early survey of

adsorption literature of possible relevance to the origin of

life,162 and examined the interplay between solute concen-

tration, solute type and mineral surface area. An especially

illustrative figure from their publication is reproduced in

Fig. 2.

It has been estimated that the total concentration of amino

acids in the prebiotic oceans was on the order of 10�3 M under

very favorable synthesis or bolide delivery conditions, while

those of the nucleobases may have been several orders of

magnitude lower.166,171 At such low bulk oceanic concentra-

tions, it is unlikely that organic compounds would have been

significantly concentrated on mid-ocean sediments or minerals.162

Simple concentration mechanisms such as evaporation,

provided subaerial land masses existed at that time, could

easily have circumvented this problem. The ease with which we

can envision such mechanisms given modern surficial pro-

cesses does not guarantee that these types of environments

existed on the primitive Earth.

Adsorbed organics would likely modify surfaces presenting

entirely new adsorption phenomena, in some sense organic

coated surfaces are yet another type of mineral. It has been

suggested that vast amounts of complex high-molecular

weight organic polymers similar to melanoidans could have

been deposited in marine sediments during the prebiotic

era.172,173

Temperature likely has an important effect on surface

adsorption, with some species being more strongly adsorbed

at higher temperatures and others more weakly adsorbed.

Most studies are conducted at room temperature for practical

reasons, but adsorption could be drastically different at other

temperatures. Temperature affects surface acidity, isoelectric

points of surfaces and ionic solutes, adsorption isotherms of

minerals, lipid bilayer fluidity, etc. The effect of temperature

on adsorption, with its obvious implications for various

postulated early environments, remains a significant lacuna

in our understanding of the potential for concentration of

organic species by mineral surface adsorption. This behavior

can be complex, and there are few controlled studies in the

literature of prebiotic relevance (i.e., using plausible minerals,

relevant solution parameters, or studying organic compounds

of possible interest). In one exceptional study, it was found

that adenine adsorbs less strongly on graphite as a function of

temperature.174 Poly-(n-butylmethacrylate) in organic solvents

has been shown to adsorb less on alumina surfaces as

temperature decreases.175 It has also been found that Cd2+

adsorption is greatly lowered on activated charcoal as a

function of increasing temperature.176 The degree to which

this phenomenon is generalizable remains to be demonstrated.

One problem with conducting temperature-adsorption studies,

and indeed aqueous mineral–surface adsorption studies in

general, is that mineral surfaces can be dynamic interfaces

with respect to dissolution and redeposition which is in fact the

basis of aqueous weathering.177 For some minerals (especially

evaporitic minerals) the rate of dissolution may be significant

over the time-scales on which laboratory experiments are

conducted.178,179 Dissolution and reprecipitation could have

numerous effects on adsorption, including alteration of

specific surface area and giving rise to new mineral veneers,

with different adsorption properties than the mineral initially

being studied, for example via the oxidation of surface iron

species. Careful characterization of surfaces before and after

adsorption is seldom conducted, but may at times be necessary.

The complicated nature of mineral surface transformation in

more complex geomimetic environments was demonstrated180

using a hydrothermal vent reactor designed to test the models of

Russell and colleagues.77

Adsorption studies tend to focus on the solution conditions

that yield measurable changes over the time-scale of the experiment.

Fig. 2 Relationship between mean intermolecular distance (reciprocal

density, or surface area occupied per adsorbed molecule) between

adsorbed molecules, equilibrium solute concentration, surface adsorp-

tion equilibrium constant (K) and mineral surface area (A). Brackets

represent typical adsorption equilibria K values for A: several amino

acids such as alanine, glycine, leucine and serine, and glucose; B: most

of the purine and pyrimidine bases and nucleosides; and C: the

aminoalkylated nucleotides studied by Burton et al.170 For example,

at 10�3 M equilibrium solute concentration, an amino acid adsorbed

on clay (a high specific surface area mineral, right-hand y-axis) would

have its nearest neighbor between 100 and 1000 A, or approximately

10–100 molecular diameters distant. Adapted from ref. 162

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The ratios of solution to surface area, and solution concen-

tration to surface area must be appropriately balanced in

order to observe adsorption. Clay minerals have been favorite

topics of study because they are significant components of soils

(and thus are of interest for various agricultural funding

sources); because they have extremely high specific surface

areas (a gram of clay may have a surface area roughly

equivalent to a tennis court, whereas a gram of coarse sand

may have a surface area of a few cm2); and clay minerals have

ionic exchange sites, and are thus reminiscent of ion exchange

resins.57,181–183

Organic adsorption to mineral surfaces may approximately

be generalized based on functional group chemistry. Because

ionic bonds are relatively strong, and many biochemicals

contain ionizable functional groups, interactions between

amines, phosphates or carboxylic acids are often the focus of

adsorption studies.

Mineral surfaces can be characterized by their points of zero

charge (PZC), similar in concept to an isoelectric point. The

PZC is the pH at which the net surface charge averaged over

all sites is zero, but may possess balanced positive and negative

charges. As the net positive or negative charge on a mineral

surface changes as a function of pH, the surface becomes a

better or worse adsorbant for species of the opposite charge,

and the net charges on adsorbing organic compounds may

also change as a function of pH.184 Solution pH is thus a

fundamentally important parameter in adsorption studies.

Distinct from the classical batch adsorption studies, adsorp-

tion affinity has also been studied in flow-through conditions

using high-pressure liquid chromatographic techniques.174,185,186

Chromatography essentially depends on the interactions of

solutes, solvents and the stationary phase. Rather than the loss

of the solute to adsorption, the retention of the solute by the

stationary phase is measured, in terms of the lag time for the

solute to emerge in the solvent front. Adsorption of molecules

as solvents flow past stationary mineral phases could also

result in the phenomenon of geochromatography, which has

been suggested to be a potential mechanism for sorting

complex prebiotic mixtures.187

Adsorption is not always a mechanism for preserving

organic molecules. Instead, adsorption may also result in

degradation of the organics. Radioactive elements such as40K+ (b-decay half-life = 1.25 � 109 years) were likely much

more abundant on the primitive Earth. The K+ ion is highly

water-soluble and adsorbs well to clay surfaces. Thus, organics

concentrated on clay minerals by adsorption would have been

co-localized with a potent b-emitter, which may have made

clay surfaces especially destructive environments for organics.188

Very low recovery of amino acids was obtained after adsorp-

tion to clay minerals and irradiation with a 60Co gamma ray

source.189

Transition metal-containing mineral surfaces may also be

capable of photocatalytic degradation of organics, because of

the presence of reactive oxygen species generated on the

mineral surfaces by Fenton-like reactions. For example,

adenine is readily oxidized on pyrite surfaces by peroxides

generated from reaction of surface ferrous iron with water,190

and copper-containing clay minerals increase the degradation

rates of adenine and adenosine.191

The protective effects of organic adsorption on mineral

surfaces may be important for preserving biomolecules as

biosignatures, or for preserving organics for their concen-

tration on early Earth. These effects may be associated with

the exclusion of water from the reaction milieu. The racemiza-

tion of amino acids in carbonate mineral matrices was found

to be roughly as fast as that occurring in solution.192 To this

end the types of evaporitic minerals found on the surface of

Mars have attracted great interest, as they may dictate

the types of mineralogies that might preserve early martian

biosignatures.193 The observed association of early bio-

signatures on Earth with evaporitic environments46 may also

hold true on Mars, assuming that the Earth’s biosphere and a

potential Martian biosphere followed similar evolutionary

trajectories. Aubrey et al.194 found some evidence for the

preferential preservation of amino acids in ancient (B25 Ma)

sulfate minerals which was later corroborated by Kotler et al.195

Amino acids. Considerable effort has been focused on the

interactions of amino acids with mineral surfaces.Modern protein

enzymes contain 20 canonical a-amino acids, approximately

half of which are considered not to have been primordial.24,196,197

The primordial amino acids are generally assumed to be the

structurally simplest (thus excluding the aromatics), so that

their interactions would have been governed primarily by

electrostatic interactions. All amino acids exist as zwitterions

over a broad pH range, because they contain at least two

ionizable groups, with pKa values ranging from 2–3 (for the

carboxylic acid group) and 8–9.5 (for the amine group).

Most studies have focused on investigating the adsorption

of negatively-charged amino acids on positively-charged

mineral surfaces or vice versa. This choice has been driven

mainly by the practical issue of being able to detect measur-

able amounts of adsorption. Since amino acids are typically

zwitterions in solution, adsorption could result in the forma-

tion of a surface coated with solvent-exposed charges of the

same polarity as the original surface and, in the case of amino

acids such as glutamic acid, high surface coating could result

in the presentation of a surface coated in charges opposite to

the original surface’s. Thus a positively-charged mineral sur-

face could become a good adsorbant for positively-charged

species if coated with zwitterionic organic species. This

cooperative phenomenon could lead to co-adsorption effects,

as has been noted by Lambert and coworkers.198

Mineral surfaces as catalysts

Minerals could be catalysts for a variety of potentially

important prebiotic reactions. However, it is important to

bear in mind that true catalysts promote reactions that are

thermodynamically favorable, but kinetically inhibited, but

lowering the energy barrier. Catalysts thus speed the approach

to thermodynamic equilibrium, but do not alter that final

equilibrium. However, minerals certainly alter the kinetic

landscape of organic transformations over geological timescales.

Peptide formation catalyzed by mineral surfaces. A number

of studies have been conducted exploring the potential for

mineral surfaces to catalyze peptide bond formation. Lahav

and coworkers have shown that clay minerals including

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kaolinite and bentonite speed the rate of formation of oligo-

glycine when these were cyclically dried together and heated.63

The final species distribution was compatible with the attain-

ment of thermodynamic equilibrium, suggesting that the clay

surface is indeed acting as a true catalsyst. Marshall-Bowman

et al.199 showed that several likely common prebiotic mineral

surfaces, such as hematite, pyrite, rutile and amorphous silica,

promote the hydrolysis of peptides over the background

solution rate.

Using a combination of experimental and computational

techniques, Lambert et al. investigated the mode of amino acid

covalent adsorption in the dry state on minerals, and how

these amino acids might form polypeptides when heated.200

Schreiner et al.201 examined the ability of amino acids to be

oigomerized by carbonyl sulfide (COS) on pyrite surfaces

using computational methods. COS has been demonstrated

to assist short peptide formation in fairly concentrated

solution.202 Schreiner et al. found that the pyrite surface was

able to change the free energy landscape of the elementary

reaction steps, and that the mineral could directly participate

in some of the reaction steps, changing the reaction mecha-

nism compared to the situation in bulk water. These computa-

tional results have not been tested experimentally.

Kawamura et al.203 examined peptide formation in a hydro-

thermal flow reactor at 275 1C and near neutral pH at contact

times limited to a few seconds. It was found that a preformed

alanine tetramer (Ala4) could cross-react to form higher pep-

tides to a greater extent in the presence of some minerals, in

particular, the carbonates calcite and dolomite. Tourmaline,

galena, apatite, mica, sphalerite, quartz, chalcopyrite, and

pyrite did not enhance longer peptide yields. However, the

total available surface area of the minerals was not strictly

controlled, thus hampering comparison across these minerals.

All of the minerals also significantly catalyzed the degradation

of the starting Ala4, in agreement with the results of Marshall-

Bowman et al.199

Clay mineral suspensions in alternating drying-heating

(to 85 1C)-wetting cycles were also found to promote the

oligomerization of glycine up to the pentamer, and shorter

mixed oligomers of Asp-Gly and Val-Gly.204 A similar cata-

lytic effect was observed for aluminum oxides with GlyGlu

peptides.205 Rimola et al. conducted calculations suggesting

that feldspar surfaces might also enhance peptide elongation

rates.206

The coupling of mineral hydration to organic oligomeriza-

tion has been investigated inspired by the observation that

many biological polymerization reactions are dehydration

condensations.207 To test this hypothesis, glycine was mixed

with simple anhydrous salts (MgSO4, SrCl2, BaCl2 and

Li2SO4) at 140 1C for up to 20 days, which promoted Gly

polymerization. Oligomers up to Gly6 were synthesized from

Gly–MgSO4, with concomitant hydration of the mineral. The

total yield was about 200 times larger than that from heating

Gly alone.

Salt induced peptide formation coupled with peptide chain

elongation on clay minerals starting from dipeptides and

dipeptide/amino acid mixtures was investigated by Rode and

coworkers.208 It was shown that both reactions can take place

simultaneously and that the presence of mineral catalysts

favors formation of higher oligomers. The effects of the

specific clay mineral were found to depend both on the nature

of the mineral and the solution phase reactants.

Lipid and membrane formation catalyzed by mineral surfaces.

Fatty acids and polyprenol phosphates spontaneously form

micelles and vesicles in aqueous solution when placed at the

appropriate pH, lipid concentration and salt concentrations.

This phenomenon has been used to argue that lipid-like

materials may have been involved in the formation of the

earliest cells.33

Ourisson and coworkers have shown several addition reac-

tions catalyzed by minerals which lead to higher isoprenoids

lipid compounds, for example the conversion of farnesol to

squalene over iron(III) sulfide,209 and the synthesis of geraniol

and its isomers from the condensation of C5 monoprenols in

the presence of montmorillonite.210

Hanzyc et al.65 offered compelling micrographic evidence

that clay mineral surfaces can speed up the formation of

vesicles over very short (minutes to hours) timescales. The

minerals apparently provide nucleation sites for vesicle for-

mation after adsorption of the fatty acids. It is not clear that

such systems would overcome the limitations to vesicle for-

mation imposed by the critical vesicle concentration (CVC),

which is the concentration at which vesicles become the more

stable form of dissolved fatty acids compared to the mono-

meric dissolved state. In fact, as a new phase (the mineral

surface) is added to the system, which may remove fatty acids

from solution, the presence of minerals may make the CVC

higher. In evaporative environments, this effect is likely of

marginal importance, as the concentration of fatty acids could

range from extremely dilute to solid.

The integrity or rupture of phospholipid vesicles and the

affinity of bilayers in contact with oxide mineral surfaces has

been examined by bulk adsorption isotherms, atomic force

microscopy, neutron reflectivity, and classical DLVO theory

modeling.211–215 The head-group charge of the lipids as well as

oxide surface charge, solution ionic strength and effect of

divalent Ca2+ ions was examined. It was found that phospho-

lipid vesicles are more stable in contact with positively-charged

mineral surfaces such as corundum rather than negatively-

charged minerals surface such as quartz. The results of Sahai

and co-workers are consistent with the work of Hancyzc et al.

(2003) in showing that mineral surface chemistry can affect

protocell stability. It is recognized that phospholipids are

biologically-produced molecules but these are routinely used

in protocell studies, as alternatives to fatty acids or oil

droplets.

The formation of C–O–P ether bonds in phospholipids is a

high energy reaction and is catalyzed in biology by enzymes.

The formation of phospholipids is, therefore, considered to be

one of the major knowledge gaps in the origins of life.

Extending the work of Oro on the dehydrative synthesis of

more complex membrane lipids such as acylglycerols,216

Maheen et al. were able to show the synthesis of glycerol

phosphates under hydrothermal conditions.217

Chirality. Biochemistry is remarkable in its preference

for using only one of a given pair of enantiomeric monomers

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(for example, L-amino acids and D-nucleotides). The origin of

this chiral preference has received a great deal of attention in

the field. Since the pioneering work of Louis Pasteur, it has

been known that mineral crystals can occur in different chiral

forms, and the various surfaces of a mineral may be asym-

metric. Globally, the various mirror-image surfaces of a given

mineral are likely to be balanced but, locally, mineral surfaces

may present interesting environments for chiral selection.

Enantiomeric excesses have been observed for some amino

and hydroxy acids in carbonaceous chondrites, including non-

biological amino-acids such as isovaline, some of which could

be due to mineral effects.218 Hazen et al. were able to demon-

strate a preference for the adsorption of aspartate enantiomers

on chiral calcite surfaces.104 Activated nucleotide monomers

may preferentially form homochiral oligomers when elongated

over homoionic montmorillonite.219

On the other hand, zirconium dioxide surfaces have been

shown to catalyze the racemization of secondary alcohols,220

and montmorillonite has been shown to catalyze the racemiza-

tion of amino acids.221

Nucleic acids and their components. Saladino and coworkers

have conducted a number of studies examining the effects of

various mineral phases on the reactions of neat formamide

(FA), and shown that many minerals, including iron sulfides,

montmorillonite, and rutile are catalysts for the formation of

nitrogen heterocycles, including some of those found in nucleic

acids.222–227

The so-called formose or Butlerov reaction,228 involving the

alkaline oligomerization of formaldehyde,229 has long been

held to be the most important prebiotic source of sugars,

especially of ribose, for the development of a primordial

RNA World. A wide variety of minerals including clay

minerals and calcite have been shown to catalyze the formose

reaction.230,231

Early studies of mineral-catalyzed formose reactions were

somewhat disappointing with respect to the origin of an RNA

World because, despite catalytic effects, ribose was always

found to be a minor component of a complex product

mixture.232 More recently, however, Prieur233 and Ricardo

et al.105 have shown that conducting the formose reaction over

borate mineral surfaces results in enhanced synthesis of ribose-

borate adducts. Although there has been debate over the

abundance (hence, relevance) of borates in prebiotic contexts,106

silicates have also been found to have a stabilizing effect on

ribose at high pH.234 The question of how borate- or silicate-

ribose adducts were selectively stripped of borate or silicate,

nucleosidated and phosphorylated merits further study. The

further influence of molybdate and carbonate on these reac-

tions was also reported.235 Clay minerals such as perlite were

shown to catalyze the formation of sugar phosphates by

Maheen et al.,236 however Baldwin et al. showed conversely

that minerals including several metal oxides and hydroxides

can be catalysts for the hydrolysis of phosphate ether C–O–P

bonds.237

Borate minerals have been shown to stabilize ribose.105 The

ability of borate minerals to stabilize RNA in water or

formamide has also been studied.238 Most borate minerals

were found to either have no effect or to catalyze degradation

of RNA, although again no effort was made to normalize for

surface area in this study.

The adsorption of NBs to graphite, likely a minor mineral

phase but perhaps a general model for a non-ionic surface,

showed the general trend that purines are adsorbed more

strongly than pyrimidines,239 consistent with other studies

for adsorption on clay minerals (bentonite, kaolinite, and

montmorillonite)240 and rutile.241

Theng and coworkers242 conducted a study on the adsorp-

tion of NBs, ribose and phosphate (Adenine (A), Cystosine

(C) and Uracil (U, hereafter referring to uracil, rather than the

element uranium)) to Mg2+-exchanged montmorillonite and

found that the isotherms were typically of the C-(constant

partitioning) type, where the amount adsorbed increased

linearly with the equilibrium solute concentration. The bases

were proposed to adsorb by coordination to Mg2+ ions through

water bridges. Little ribose was adsorbed, again indicating the

importance of ionic interactions. Phosphate adsorption showed

an L- (Langmuir) type isotherm, indicating strong chemi-

adsorption and a saturation phenomenon. The plateau value

of adsorption for phosphate (B0.012 mmol g�1) showed that

phosphate adsorbed on the edge surfaces of montmorillonite.

The differences in adsorption behavior of ribose and phosphate

were interpreted to reflect differences in ionizibility, size and

solubility, underscoring the importance of strong ionic inter-

actions, which have been suggested to have been a selective

pressure for biology’s choice of the coded amino acids.243

Kamaluddin and co-workers have conducted a number of

studies on the adsorption of mononucleotides and found

similar adsorption isotherms for several metal oxides.244,245

The phosphate moiety was found to be especially important

for adsorption, in agreement with other studies. There is,

however, some discrepancy as to the role of other functional

groups in adsorption as compared with the conclusions of

other authors.241 These nuances in adsorption modes are

important in determining the ability of the mineral surface

to serve as a scaffold for higher-order oligomerization and

templating reactions.246

The adsorption of ssDNA on olivine, pyrite, calcite, hematite,

and rutile was examined at pH 8.1 and room temperature.

Results showed that when normalized for surface area, there

was little difference in the adsorption of short (B30 nucleotide)

oligonucleotides on surfaces, suggesting that most minerals

become equivalent for nucleic acid adsorption at a relatively

short oligonucleotide length.247

An enormous amount of research has been conducted over

the years demonstrating the catalysis of oligonucleotide for-

mation from activated RNA monomers by mineral surfaces,

most notably by Ferris and coworkers, frequently using

montmorillonite.219,248–251 Using activated phosphoimidazolides,

montmorillonite has been shown to speed oligomerization

reactions, and in some cases to be able to do so in a manner

that enriches homochirality. An important gap in the field is to

address how the RNA monomers or phosphoimidazoles

would have been activated in the prebiotic environment.

Swadling and coworkers252 examined the adsorption of nucleic

acid oligomers on layered double hydroxide minerals compu-

tationally and concluded that DNA has some significant

advantages over RNA or PNA (peptide nucleic acid).

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Mineral surfaces as reactants

Several proposals have been put forward in which mineral

surfaces undergo irreversible stoichiometric reactions that

could have contributed to prebiotic chemistry. As mentioned

above, Fe2+ in solution or at mineral surfaces may have been

an important photo-reactant for organic synthesis, resulting in

oxidized Fe3+ iron and reduced carbon in a stoichiometric

manner. Hydrothermal redox reactions of reduced iron species

with dissolved nitrogen species has also been shown to be a

potential source of reduced nitrogen in the primitive

seas.80,94,253 More recently, sphalerite-assisted photochemistry

(ZnS) has been proposed as an important prebiotic synthetic

process.146 Many of the carbon fixation reactions central

to Wachtershauser’s surface metabolism model are also

stoichiometric,74 with carbon reduction being coupled to iron

or sulfur oxidation.

Schreibersite ((Fe,Ni)3P, has been proposed as a stoichio-

metric source of phosphorylated and phosphonylated organic

compounds on the primitive Earth.254 This synthesis over-

comes some of the previous objections to phosphate minerals

such as apatite serving as prebiotic phosphorylating reagents,

such as their insolubility and non-reactivity.255 It is important

to note, however, that schreibersite is a rare mineral on Earth,

though common in iron–nickel meteorites.

Computational studies of experimental results and theoretical

models

Common nickel and iron sulfide (Ni–Fe–S) minerals of hydro-

thermal origin, such as greigite (Fe3S4) and violarite (Fe2+-

Ni23+S4) have been proposed as catalysts in metabolism-first

models for the origin of life256 (see also ref. 257 and 258 for

reviews). Wachtershauser’s ‘‘metabolism first’’ theory for the

origin of life proposes surface adsorbed primordial metabolic

cycles driven by oxidative formation of pyrite (FeS2) from

ferrous sulfide (FeS) and confined to the Ni–Fe–S and Fe–S

mineral surfaces.10 Based on Raman spectroscopic studies,

violarite nanocrystals were suggested to act as a carbon

monoxide dehydrogenase (in place of pentlandite, (Fe,Ni)9S8),

because in violarite the sulfur atoms on the surface are likely to

be hydrogenated, leaving the nickel and iron sites available for

reaction.259

A few studies have investigated the mechanism of the

FeS/H2S redox system and its properties.260 Kalapos criticized

the notion of surface-adsorbed metabolic cycles261 based on

energetic considerations (an aspect not addressed in recent

reviews by Anet262 or Cody84). Interestingly, a new stoichio-

metry was proposed, and the energetics of this novel reductive

citric acid cycle were compared with those in the original

version.72 Thermodynamic analysis of this putative archaic

chemoautotrophic CO2 fixation cycle and its self-organization

in hydrothermal systems was conducted.263

One problem with this model is that the synthesis of citric

acid from CO2 on FeS catalysts has thus far proven elusive

(see ref. 264 and references therein). One of the reasons for the

failure is that for redox reactions, favorable thermodynamics

alone are not sufficient to ensure the formation of significant

amounts of products; kinetics must also be considered.264 The

lack of thermodynamic calculations for the individual reactions,

and complications surrounding anaplerotic reactions (those in

which the intermediates must be cyclically regenerated) have

attracted appreciable skepticism.261,265–267 Ross’ thermo-

dynamic calculations268 suggest that the presence of FeS is

not enough to drive CO2 reduction.

Clay mineral adsorption modeling

Clay minerals may have characteristics conducive to the

concentration of precursor organic molecules for the synthesis

of biomolecules on early Earth. Kaolinite and dickite are clay

minerals with a 1 : 1 dioctahedral layered structure.269,270 The

layers consist of a tetrahedral sheet formed from SiO4 tetra-

hedra and an octahedral sheet consisting of AlO6 octahedra.

Dickite differs from kaolinite in layer stacking. The unit cell of

dickite consists of two kaolinite layers and is twice as large as

the unit cell of kaolinite. Layers are held together by hydrogen

bonds between surface hydroxyl groups on the octahedral

side and the basal oxygen atoms on the tetrahedral side.

Montmorillonite is a 2 : 1 clay mineral belonging to the

smectite group.269,270 Each layer is composed of two tetra-

hedral silica sheets sandwiching an octahedral alumina sheet.

In all of these minerals, isomorphic substitution can occur in

the octahedral sheet (the most common being replacement of

Mg2+ by Al3+) and/or in the tetrahedral sheet (with Al3+

substituted for Si4+).271 These substitutions can lead to the

presence of permanent negative charges or local charge

defects,272 which are compensated by cations such as Na+273

present between adjacent tetrahedral–octahedral–tetrahedral

sandwich layers. The broken edges of the clay platelet-like

particles expose silicate and aluminate sites, called edge sites.

Protons can adsorb at edge sites, resulting in pH-dependent

surface charge.

Reactions of formamide (FA), a simple polar prebiotic

molecule, have been studied with a wide array of mineral

surfaces.222–225,274–277 FA can serve as a building block for

several compounds of biological interest, possibly by dehydration

to form cyanide as an intermediate.278,279 When heated in the

presence of a variety of mineral catalysts, including kaolinite,

zeolites, olivines, phosphate minerals, TiO2 and cosmic dust

analogues,224 FA condenses into a variety of nitrogen hetero-

cycles, including many of the canonical NBs.222–225,280,281

Horvath et al. recently summarized results from vibrational

spectroscopy and X-ray powder diffraction studies of kaolinite

organo-complexes, including kaolinite-FA.282 The kaolinite

surface may be altered through chemical reactions by insertion

of FA.283 The degree of intercalation of FA depends on

whether kaolinite is ordered (low defect) or disordered (high

defect).284 FA is also known to adsorb on minerals of the

kaolinite group by hydrogen bonds between the CQO group

of FA and mineral surface inner sphere (covalent) hydroxyl

group complexes.285–289 Edge sites are mainly involved in these

adsorption interactions, while basal surfaces remain essentially

unoccupied.290 IR spectroscopy studies indicate that inner-

sphere bonding between the hydroxyl groups and organic

molecules is weaker for FA than for N-methylformamide.291

The prebiotic availability of purine and pyrimidine base deriva-

tives from hydrogen cyanide-based chemistries seems likely,292–295

with synthesis perhaps mediated by eutectic concentration.296–298

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Both organic and inorganic soil components may be impor-

tant for the surface adsorption of NBs.299 Depending on their

composition, NBs can have markedly different affinities for

mineral surfaces.300 Polyvalent cations, especially alkaline

earth cations,301,302 can also promote NB adsorption.303 At

higher concentrations these cations can interact with NBs, so

as to disrupt inter-NB hydrogen bonding and compromise the

structural integrity of nucleic acid polymers.304–306 In the

presence of cations, purines adsorb more readily to some clay

surfaces than pyrimidines do.162 For most studied minerals at

neutral pH, nucleotides were adsorbed most strongly, followed

by nucleosides and free NBs. This sequence depends on

mineral type and solvent conditions, such as pH, temperature

and ionic strength, which can alter the mineral surface proper-

ties, such as net charge and charge density.307

Clay mineral surfaces efficiently adsorb amino acids308 and

NBs. Some pyrimidines, which are not normally adsorbed

onto clay minerals, may interact with purines and co-adsorb

on clay surfaces. NBs interact with the interlayer cations of

clay minerals by various exocyclic functional groups and ring

nitrogen atoms,309 where adsorption is partially governed by

van der Waals interactions and H-bonds.310 U adsorption on

rutile (TiO2) was significantly weaker than that of A or C,241

possibly due to the involvement of electrostatic interactions.

U was suggested to adsorb cooperatively, edge-on, rather than

parallel, to the surface.241 The surface site density for different

minerals can vary significantly allowing possible adsorption of

a complete monolayer of U.311 The adsorption of NBs and

their derivatives can vary in the entire range from 0–100%

depending on experimental conditions.188

4. Computational models and methods

Computational approximations involving model clusters or

periodic systems can be used to predict interactions of model

prebiotic molecules with mineral surfaces. A cluster model of a

single kaolinite layer was prepared using experimental crystal

structure data in order to study the adsorption of FA and NBs

on kaolinite group minerals.312 Each cluster was constructed

as a cut-off from the periodic structure of the mineral. Both

tetrahedral and octahedral clay surfaces were mimicked in

order to investigate which surfaces preferentially interact with

the studied molecules. These models consist of one ring of the

tetrahedral sheet formed from six SiO4 tetrahedra, and/or one

ring of the octahedral sheet containing six AlO6 octahedra.

Dangling bonds at the edges of the clusters were saturated

with protons. Several initial positions of the adsorbate were

tested to investigate which orientation toward the mineral

surface, such as parallel or perpendicular orientations,

mediated by cation–p or cation–heteroatom interactions, is

preferred. Substitution of Al3+ by Mg2+ in the octahedral

fragment and Si4+ by Al3+ in the tetrahedral sheet was also

modeled. Following substitution, the model was made electro-

neutral by addition of Na+.

Models of Ni–Fe sulfide were constructed as truncations of

the crystal structure of violarite.313 Due to changes caused by

optimization, the original model was modified. The new model

consisted of one Fe atom, one Ni atom, and six sulfur atoms.

Dangling bonds on four of the sulfur atoms were saturated

with protons to ensure electroneutrality of the entire system.

Solvating water molecules were initially placed close to the

Na+ ions as this position was shown to be the most favorable

on the mineral surfaces.314

Calculations of systems involving NBs with water, cations

and clay minerals were performed using density functional

theory (DFT).315 Several DFT functionals (B3LYP (Becke,

three-parameter, Lee–Yang–Parr), BLYP316,317 and M05-2X318)

were used. Application of the B3LYP functional in studies of

large systems has become popular in the area of adsorption

on clay minerals; however, this functional has some unsatis-

factory performance issues such as underestimation of the

energies for weak non-covalent interactions.319 Binding

energies were therefore also calculated using the M05-2X

functional. M05-2X is a hybrid meta-exchange–correlation

functional319 derived from the M05 functional,320 which

adds a kinetic energy component to the exchange–correlation

functional.

Several basis sets, including two Ahlrichs valence split basis

sets321 and pseudopotential LANL2DZ322–324 were used to

calculate the modeled reactions involving small Fe–S clusters.

Employing an electron core potential (ECP) basis set such as

LANL2DZ (Los Alamos National Laboratory 2 double zfor transition metals) has become popular in computations

of transition metal-containing systems. The medium size

6-31G(d) basis set325 was employed due to the large size of

calculated models in the case of adsorption of NBs on clay

mineral surfaces.

Topological characteristics of electron density distribu-

tion were obtained using Bader’s ‘‘Atoms in Molecules’’

approach,326 which gives insight into the nature of bonds.

An occurrence of the (3,�1) critical point of the electron

density between two atomic centers indicates the presence of

a stabilizing interaction, generally interpreted as the existence

of a chemical bond.327,328 The charge density (r(r)) and the

Laplacian of the electron density (r2r(r)) at such points were

also calculated. In the case of closed-shell electron interactions

(ionic bonds, van der Waals interactions or hydrogen bonds) a

small r(r) and a large and positive r2r(r) are typically

observed. The maps of electrostatic potential of the NBs

adsorbed on clay minerals were calculated using the Molekel

program package.329 The values of the interaction energy

(Eint) of the systems studied were obtained as differences

between the energy of the complex and the sum of the energy

values of the adsorbate and adsorbent subsystems. The Eint

value was corrected (Ecorr) for basis set superposition errors

using the counterpoise method.330

Solvation of the system was modeled in two different ways.

First, the supermolecular approximation was applied, which

involves the explicit consideration of microsolvation by water

molecules. Second, solvent molecules were replaced by a

dielectric continuum with a permittivity, e, surrounding the

solute molecules outside of a molecular cavity (Conductor-like

Screening Model).271 Water with a relative dielectric constant

of er = 78.39 was used as a solvent. The values of interaction

enthalpy (DH), Gibbs free energy (DG) and entropy (SDT)were calculated using the rigid rotor-harmonic oscillator-ideal

gas approximation based on the vibrational frequencies of the

optimized structures of the studied systems.

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Periodic DFT calculations were carried out to compute

equilibrium structures and energies of the NBs adsorbed on

montmorillonite. Calculations were performed using the pro-

jected augmented wave method331,332 to describe the ionic

cores and a plane-wave basis set for the valence electrons.

Full geometry optimizations were performed using a conjugate-

gradient algorithm. A unit cell of montmorillonite was

modeled using the unit cell of pyrophyllite, which has identical

aluminosilicate layers as montmorillonite but exhibits no

substitution. Subsequently, an Al3+ ion was substituted by a

Mg2+ ion, with the induced negative charge being compen-

sated by a Na+ cation placed in the center of the six-

membered silicate ring above the Mg2+.

Violarite as a catalyst in Wachterhauser’s surface metabolism

model

Despite the impact of Wachterhauser’s model,74 only one

paper has been published studying the thermodynamic and

kinetic aspects of the putative carbon fixation cycle using

ab initio techniques,333 in which the DFT approach was applied

to simple models of Ni–Fe sulfide catalysts to evaluate possible

reactions at 373 K. Such temperatures are perhaps on the low

end of what might be expected in black smoker type on-axis

vent systems, but are commensurate with those commonly

encountered in off-axis vent systems.

The formation of acetic acid from CO and CH3SH, sum-

marized in eqn (3.1), was modeled:

CH3SH + CO + H2O - CH3COOH + H2S (3.1)

This reaction can be divided into two separate sub-reactions as

shown below:

CH3SH + CO - CH3COSH (3.2)

CH3COSH + H2O - CH3COOH + H2S (3.3)

The sequence of transformations of adsorbed reactants on

the NiS–FeS surface and the thermodynamics of each step of

this mechanism were calculated.333 Fig. 3 shows the Gibbs free

energy of reaction (DGr) for each step of the proposed

mechanism of the carbon fixation pathway.

The addition of carbon monoxide into the Fe–Ni–S model

by binding with the iron center (forming an Fe–CO center)

and addition of the CH3SH molecule are characterized by

positive DGr values. The most endergonic step is migration of

the CH3 group to a surface Fe site. The total DGr value of all

reactions (expressed by eqn (3.2)) is positive by 37.7 kcal mol�1,

which means the reaction is not feasible as modeled, at least in

the gas phase, at 373 K.

Most of the remaining steps of the putative cycle are

characterized by negative DGr values (binding of the CH3

group to the carbonyl group anchored to the Fe center,

dissociation of a water molecule and formation of acetic acid).

If one considers only the reaction described by eqn (3.3)

(formation of acetic acid and H2S from CH3COS acid and

water), this process is exergonic by �21.0 kcal mol�1. How-

ever, the DGr value of the overall reaction summarized by

eqn (3.1) is positive by 16.7 kcal mol�1 (see Fig. 3 for details).

This result suggests that the proposed cycle will not proceed

spontaneously under the modeled conditions.

In contrast, several studies calculated the Gibbs free energy of

the formation of pyrite (FeS2) from H2S and iron monosulfide

(FeS) to be exergonic at standard state (–10.0 kcal mol�1,334

�9.2 kcal mol�1,72 and �7.5 kcal mol�1264). Physico-chemical

analysis based on thermodynamic potentials predicts this

value to be �3.3 kcal mol�1 at room temperature.263 Ross,268

however, calculated that the conversion of FeS does not

provide enough energy to drive CO2 reduction.

These results do not allow a conclusive discussion of

possible reaction pathways. Laboratory kinetic studies need

to be performed under conditions mimicking those in hydro-

thermal settings to confirm the feasibility of these reactions.

Interactions of FA with minerals of the kaolinite group

Intercalation and adsorption of FA on two clay minerals,

dickite and kaolinite were investigated using both cluster

(intercalation and adsorption) and periodic (intercalation)

approaches.335–337 The intercalation of FA in dickite was

found to be strongly specific. The structure having two FA

molecules in the same orientation is more stable than the

structure with different orientation of a pair of FA molecules

within the same interlayer space.336 Formations and orienta-

tions of hydrogen bonds between intercalated or adsorbed FA

and mineral layers were found to be similar in all of the

studies. Moreover, the orientation and interactions of the

adsorbed FA molecule with the octahedral surface are similar

Fig. 3 Modeling of the carbon fixation pathway catalyzed by the

Fe–Ni–S model. The DGr values (kcal mol�1) are calculated at the

B3LYP/TZVP level of theory. Reprinted from ref. 333 with permission

from Elsevier.

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as found for the intercalated model.335 The FA oxygen atom

was shown to play the main role in the formation of contacts

with atoms of the aluminosilicate layer and in the energetic

stabilization of all intercalated/adsorbed systems.

Fig. 4 illustrates the optimized structure of the FA-dickite

adsorbed (A – D-FA(ads)) and intercalated systems

(B – D-FA(int)). FA is placed close to the center of the

tetrahedral (and octahedral) ring in both intercalated

FA-dickite and FA-kaolinite systems. FA forms four hydrogen

bonds with both surfaces.335,338 Two of these H-bond contacts

are formed between surface hydrogen atom and FA carbonyl

oxygen atom, in which the FA oxygen atom behaves as a

proton-acceptor. In both intercalated and adsorbed systems,

FA forms additional H-bonds with the octahedral surface

between the FA carbonyl oxygen atom, the –NH2 group335–337

and/or nitrogen atom336,338 and the surface hydroxyl groups.

The NH2 group of FA acts as a proton-donor and the surface

oxygen atom behaves as a proton-acceptor. In intercalated

complex H-bonds are also formed between the NH2 group of

FA and the siloxane surface (see Fig. 4 in ref. 335). The bond

lengths of groups of adsorbed and intercalated FA, which

participate in the formation of H-bridges with the surface

(CQO, N–H1 and N–H2), are enlarged compared to those in

isolated FA. Generally, it can be concluded that both inter-

calation and adsorption lead to structural changes in FA, which

correspond to an effort to form the maximum number of

attractive interactions with both mineral surfaces.

The interaction energy for adsorbed FA on dickite is

–14.6 kcal mol�1.335 This value is larger than the binding energy

for the water molecule adsorbed on the aluminum-oxygen site of

kaolinite (value of –10.4 kcal mol)�1.339 Thus the FA molecule

forms very strong interactions with this type of surface. The

calculated intercalation energy of FA-dickite335 is higher than

the adsorption energy for the water-kaolinite system.339 The

difference between the adsorption and intercalation energy of

the FA-dickite system was found to be B5–6 kcal mol�1. This

difference represents an additional stabilization of the FA

molecule in the interlayer space of dickite. The interaction

energies predicted using both approaches (periodic and cluster)

differ by only 0.3 kcal mol�1, indicating that the cluster model of

dickite used to study the FA-dickite systems is likely a good

approximation.335 On the other hand, the intercalation energy

of FA-kaolinite obtained at the PM3/6-31G(d) level is less

than �12 kcal mol�1 for five different configurations.338 The

difference in the binding energies for different geometries

amount to 5.6 and 2.9 kcal mol�1, respectively.

Interactions of NBs whith clay minerals

Only a few theoretical papers have been published on the inte-

ractions of the NBs with clay minerals. These include periodic

plane-wave calculations (based on the PBE functional) of

adsorption of RNA/DNA NBs on the external surfaces of

Na+-montmorillonite340 and with acidic montmorillonite at the

PBE-D level of theory.341 Adsorption of NBs onto Na+-containing

surfaces can be mediated by several interactions, e.g., cation–p/displaced, and cation/heteroatom interactions. Dispersive forces

between the NBs and the surface were shown to be essential for

stabilizing the adsorbed complexes in the face-to-face and cation/

p-displaced configurations. The preferred mode of adsorption for

guanine (G) and C with bidendate coordination is the cation/

heteroatom configuration due to electrostatic interactions, which

corresponds to larger adsorption energies than those found for

A, U and T. T and U display a preference for the cation–p/displaced configuration. The gas phase interaction energies,

computed at the B3LYP/6-311+G(2df, 2p) level for the alkali

metal cation interacting with isolated C or G, and for O4

coordination of T and U were calculated to be nearly twice as

large.342 Adsorption of NBs on surfaces without Na+, either in

face-to-face or orthogonal orientations, is sizable for all of the

NBs studied, with adsorption energies ranging from �3.7 to

�11.3 kcal mol�1, due to the stabilizing effect of dispersion

interactions. All bases except G show a preference for the face-to-

face configuration. The orthogonal orientation was found to be

more favorable for G due to its large dipole moment and the

formation of weak hydrogen bonds with the surface.

In the case of alkali metal cation-NB binding in the gas

phase,343–348 the rotation of the exocyclic amino groups of A

and C is revealed, which rehybridize from sp2 to sp3 to

coordinate the metal cation. This sp3 rehybridization is not

observed in solution349 nor in the above discussed study.340

The most favorable coordination environments for other NBs

interacting with alkali metal cations in the gas phase corre-

spond to the most stable orientations found in ref. 340.

Mignon and Sodupe studied the adsorption of A, G and C

on octahedral (Osub) and tetrahedral (Tsub) substituted forms

of montmorillonite.341 Adsorption was shown to involve

spontaneous proton transfer to the NB. The results related

to the binding energy are consistent with other published

studies on the adsorption of NBs on mineral surfaces since the

NBs were shown to interact more strongly by B10 kcal mol�1

with Osub than with Tsub complexes. This is likely due to the

greater acidity of Osub surfaces and the stronger stabilization

provided by hydrogen bonding. Binding of NBs in co-planar

orientation was found to be as strong as in orthogonal ones.

G and A were adsorbed more strongly by B6 kcal mol�1 on

the acidic surface than C (�50 vs. �44 kcal mol�1).

Interactions of T and U with dickite

Robinson et al. studied interactions between T and U and

dickite using the ab initio cluster approach (DFT method).350

Both molecules adsorb in a similar manner, which implies that

Fig. 4 The optimized structure of formamide adsorbed (A–D-FA

(ads)) (A) and intercalated (B–D-FA(int)) (B) on dickite. Reproduced

from ref. 335 with permission from Elsevier.

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the methyl group of T does not influence binding between the

NB and the mineral surface. NBs are less stably adsorbed on

the tetrahedral surface (denoted as D(t)) than on the octahedral

surface (denoted as D(o)) as was found for the adsorption

of FA335,336,351 and other small molecules352 on minerals of

the kaolinite group. Another similarity found in these

studies335–338,350–353 is that the most important components

of the intermolecular interactions are hydrogen bonds of

the O–H� � �O, N–H� � �O and C–H� � �O type. The octahedral

system with T forms a larger number of hydrogen-bonds than

the octahedral systems do with U.350

T and U adsorb to the octahedral mineral fragments and

hydrated tetrahedral mineral fragments by their N3–H groups

and O2 and O4 atoms similar to the way in which they interact in

A:T and A:U base pairs.354 The presence of proton donors (the

hydrogen atoms of the OH groups of the octahedral surface or

water) and proton-acceptors (the oxygen atoms of the octahedral

surface or water) governs adsorption. For tetrahedral systems the

presence of only proton-acceptors causes the pyrimidine N1–H

proton-donor surrounded by other proton-donors (the C–H

groups) to play the main role in intermolecular binding.

The presence of water has a large effect on the adsorption of

NBs on the cation-free dickite surface. T and U are most

strongly adsorbed on the hydrated octahedral surface. The

adsorption changes the geometrical parameters and atomic

charges of the adsorbates. This influence is largest for adsorp-

tion on the hydrated octahedral surface. The molecular geo-

metry of the studied complexes is modified more significantly

for the systems with U while the atomic charges change more

for the systems containing T.

Interactions of T and U with kaolinite

The optimized structure of T adsorbed on the non-hydrated

and hydrated (W) tetrahedral (K(3t)) and octahedral (K(3o))

kaolinite surfaces with Na+ is shown in Fig. 5.353 These

systems are denoted K(3t)Na-T, K(3o)Na-T, K(3t)NaW-T

and K(3o)NaW-T, respectively.

T and U were physisorbed on both hydrated and non-

hydrated kaolinite surfaces interacting with the Na+ through

the O2 atom (Fig. 5). Such binding was also found for NBs

interacting with bare alkali metal cations343,344 but the Na� � �Odistance was shorter by about 0.1–0.2 A.343,344,355 This attrac-

tive interaction contributes the most to the NB adsorption

strength, depending on several other factors such as the sur-

face type and orientation of the target molecule on the surface.

Hydrogen bonds between the target molecule and the surface

hydroxyl groups or the basal oxygen atoms additionally

stabilize the studied complexes. Two hydrogen bonds are

formed between the adsorbate N1–H1 and C6–H6 groups

and two different oxygen atoms of the octahedral site (Os)

or of the tetrahedral site (Ob). In all K(3o)Na-T, K(3o)Na-U,

K(3t)Na-T and K(3t)Na-U complexes the N1–H1� � �O bond

(denoted as HB1 in Fig. 5) is calculated to be stronger than the

C6–H6� � �O bond (denoted as HB2 in Fig. 5).

Addition of Na+ leads to significant stabilization of the

tetrahedral systems, which can be seen from comparison of

the interaction energy values for T and U adsorbed on

different mineral surfaces (Na+ free montmorillonite (�6 to

�11 kcal mol�1),340 including Na+-non-hydrated and hydrated

tetrahedral surface of kaolinite (�24 to�28 kcal mol�1),353 and

Na+ free non-hydrated and hydrated surface of dickite (�1 to

�9 kcal mol�1)350). The same is true for adsorption on the

octahedral surface of kaolinite. The adsorption energies for

K(3t)Na-T and K(3t)Na-U are larger than those for T and U

binding with Na-montmorillonite.340 They are also larger than

those for pyridine adsorbed on dry surfaces of Na-smectite

(�17.2 kcal mol)�1314 and for pyridine on a clay cluster

substituted with Mg2+.356

The explicit inclusion of water as solvent in the calculations

has only a small influence on the adsorption of the NBs in the

presence of Na+ (the oxygen and hydrogen atoms of water

will be denoted hereafter as Ow and Hw). Orientation of the

NBs by O2 toward Na+ remains the most favorable in all

KNaW systems (see Fig. 5c and d). A water molecule on both

tetrahedral and octahedral kaolinite surfaces is strongly

attracted to a Na+ ion in two different positions. In the first

position (the most stable on the octahedral fragment) the

water monomer interacts with the surface mainly by the

formation of two Ow� � �H–Os H-bridges and one

Ow–Hw� � �Os H-bond (HB3 in Fig. 5d). In a second configu-

ration (dominant on tetrahedral fragments) water remains

oriented by both H atoms toward the surface. In a theoretical

study of hydration of Na+ in a montmorillonite model,357 the

cation also coordinates to water molecules as well as to the

surface oxygen atoms. On the Na-smectite surface, water is

adsorbed through one hydrogen-bond with the surface oxygen

atom next to the substitution site.314,358

The NBs interact directly with water in the K(3o)NaW

systems through H-bonds, as is observed in systems of isolated

water and T or U.359,360 T and U form two hydrogen bonds

(Ow–Hw� � �O and N–H� � �Ow) with isolated water359,360 having

the Ow and Hw atoms in a co-planar position with the

T molecule. If a cation is added to a system with an isolated

base and water, then one ionic bond with a bond length 2.1 A

is formed between U and the cation.355 It can be concluded

that along with the substitution, the surface oxygen atoms also

Fig. 5 The optimized structures of T adsorbed on the non-hydrated

(a – K(3t)Na-T, b – K(3o)Na-T) and hydrated (c – K(3t)NaW-T,

d – K(3o)NaW-T) tetrahedral and octahedral surfaces of kaolinite

obtained at the B3LYP/6-31G(d) level of theory. Reproduced from

ref. 353 by permission of the PCCP Owner Societies.

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govern binding with the adsorbent, cation and water. This

influence is also seen for the basal oxygen atoms, which help to

stabilize the water molecule by the formation of hydrogen

bonds.314 Addition of water leads to a decrease of the inter-

action energy of T and U adsorbed on the tetrahedral kaolinite

surface,353 but increases the Ecorr value for K(3o)NaW-T.

Therefore, T and U are most stable on the hydrated octahedral

surface of kaolinite with an interaction energy of about

�36 kcal mol�1.

The NBs interact more strongly with the octahedral than

with the tetrahedral surface of kaolinite. The energy difference

is 6 to 7 kcal mol�1 for the non-hydrated fragments and 9 to

12 kcal mol�1 for the hydrated systems.353 This result agrees

with those for the adsorption of these NBs on dickite350 and

for the adsorption of FA on kaolinite and dickite.335,336,351

Moreover, the interaction energy of water with the hydroxy-

lated kaolinite surface is �13.1 kcal mol�1 while that of water

with the silicate surface is �4.1 kcal mol�1.352 Adsorption on

the hydrated octahedral surface of kaolinite was found to be

the most stable with interaction energies of B�36 kcal mol�1.

To help determine the energetics of sorption complexes of

the NBs on clay minerals, the maps of electrostatic potential

(MEPs) between the adsorbate and substrate were calculated.

MEPs for the main six-membered ring of the most stable

structures of T adsorbed on K(3t)Na, K(3t)NaW, K(3o)Na,

K(3o)NaW fragments are illustrated in Fig. 6.

The MEPs confirm the binding described above for both

target molecules with the mineral, which is the most favorable

with strong negative basins located above the O2 and O4

atoms. Addition of water only slightly changes the EP of the

surface but decreases the negative EP value located above

the T O2 atom involved in the Na� � �O2 bond in the octahedral

systems. Water increases the polarization strength of this

interaction in the tetrahedral system. The cation substitution

in both mineral fragments changes the surface potential, so

that the negative EP highs in the octahedral systems appear

at the surface oxygen atoms, which are in the vicinity of the

Al/Mg substitution. Minimum negative EP values in the

tetrahedral systems are observed above all basal oxygen atoms

and O2 and O4 atoms of U and T.

Conclusions drawn from computational studies

The adsorption of FA335–338,351 and NBs350,353 on the surfaces

of minerals of the kaolinite group and montmorillonite340,341

depends on the molecule’s structure and physico-chemical

properties, and the chemistry of the surface. All of the studied

molecules are stabilized better by octahedral mineral sites than

tetrahedral ones. T adsorbs more strongly with the clay sur-

face than U340,350,353 or FA.335–338,351 G and C on the external

surfaces of Na-montmorillonite show larger adsorption

energies than the remaining three canonical NBs.340 The

predicted characteristics of NBs and FA depend on their

orientation toward the surface and on the presence of water

and cations leading to multiple modes of interaction with

different mineral surfaces. The adsorption of NBs is signifi-

cantly influenced by substitutions in the mineral layer and the

presence of counter-ions.335,350,351,353 The explicit addition of

a water molecule to the kaolinite mineral surface only slightly

changes NB adsorption properties compared to the addition

of an inorganic cation.353 The large affinity of clay minerals for

the adsorption of NBs could be an indication of the potential

for catalytic properties of these materials possibly relevant to

the origin of life, suggesting that mineral fragments with well

defined edges may have played an important role in the

adsorption of NBs and their derivatives on early Earth.

The above summarized theoretical studies of the mineral-

organic interfacial processes related to the origin of life focus

on the vital characteristics of intermolecular interactions,

interaction energies and structural parameters. The main

criticism that can be made of such studies is that most of

these investigations were performed using only isolated

complexes. Moreover, the environmental effects were only

partially taken into account (for example water microsolvation353)

despite the fact that they play an important role in the

determination of the properties and reactivity of such com-

plexes. Therefore, we suggest that future studies concentrate

on sorption from aqueous solution and consider environ-

mental effects including temperature, pressure and other con-

ditions resembling those that may have been present in

relevant early Earth environments.

In most of the reported studies the cluster approach and

DFT methods were employed due to their computational

efficiency and reasonable accuracy. However, the cluster

approach is limited by the size of the model used. Thus, methods

employing translational periodicity are recommended (as for

example in ref. 340 and 341) to obtain a more complete picture

of the properties of calculated systems. For future studies

a combination of quantum mechanical–molecular mecha-

nical (QM-MM) or completely classical models is suggested,

Fig. 6 Calculated maps of the electrostatic potentials of T adsorbed

on the non-hydrated (a – K(3t)Na-T; b – K(3o)Na-T) and hydrated

(c – K(3t)NaW-T; d – K(3o)NaW-T) tetrahedral and octahedral surfaces

of kaolinite. Figure reproduced from ref. 353 with permission of the

PCCP Owner Societies.

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which can be used for calculations of large systems in extended

molecular dynamics or Monte Carlo simulations. DFT methods

are known to have difficulties dealing with systems where

dispersion competes with other effects (e.g. in biomolecules).361

This may significantly affect the accuracy of DFT results, at least

when used alone and uncorrected. Use of newly developed DFT

functionals (for example, M05-2X, as in ref. 353) is one way to

overcome these problems. However, this introduces another

difficulty because DFT results are hampered by dependence on

differences in the functional used. Thus, calculations based on

the Møller–Plesset perturbation theory of the second order

(MP2)362 should be carried out at the same time for comparison.

Conclusions

The potential roles of mineral–organic interactions in pre-

biotic chemistry are clearly quite complex, and studies have

thus far only scratched the surface with regard to the types of

effects which may ultimately prove important.

There are many outstanding questions which remain prime

research targets for surface science studies with respect to the

origin of life. Many of these questions are complicated by the

fact that we do not know how life originated or which

geochemical environments were available on primitive Earth.

Nevertheless, the questions can be posed proceeding from the

most general to the more specific. Did mineral surfaces

significantly alter the kinetic landscape of important reactions

leading to the origin of life relative to reactions occurring in

bulk heterogeneous solution? Are there environments and

specific minerals which should be preferred targets of study?

For example, do clays, evaporitic minerals or minerals

associated with hydrothermal systems offer more favorable

environments for chemical evolution, or is this largely an

irrelevant question given first-principles analysis of adsorption

phenomena? Is there a generalizable effect of temperature on

adsorption or catalysis? If so, what types of compounds or

reactions would low or high temperature environments favor

or disfavor? Can enough inference be drawn from the experi-

mental studies which have thus far been conducted to allow

for useful computational predictions to be made? How can

these inferences be improved?

In spite of these unresolved questions, some general conclu-

sions that may be drawn are that some mineral surfaces can

indeed be strong and specific adsorbants for a variety of

organic compounds, and could enhance preservation or

degradation depending on numerous factors such as environ-

mental conditions (pH, water activity, temperature, the presence

of light or ionizing radiation, etc.). For small molecules,

adsorption could lead to productive collisions between

molecules in fairly concentrated solutions, which implies the

primacy of some environments, such as sea-floor sediments,

evaporitic lakes or tidal pools, over others. This would depend

on the activation energy barriers for these reactions and thus,

the temperatures at which they occur, the degree to which

mineral surface catalysis can alter these energy barriers and

the degree to which water interferes with or facilitates these

reactions.

The results of theoretical studies lead to a number of inter-

esting conclusions regarding the interactions of NBs with water,

cations and minerals, and the feasibility of Wachtershauser’s

proposed C-fixation cycle (the production of acetic acid from

CO and CH3SH).74 This scheme was shown to be partially

catalyzed by model Fe–Ni–S surfaces through the creation of

surface coordination complexes.333 Synthesis of formic acid

from CO2 and H2S in the presence of pyrite was found to be

endergonic under modeled conditions and the studied reaction

pathway did not lead to a significant amount of the product in

isolated gas-phase systems. The degree to which these results

mimic aqueous conditions remains to be determined.

The studies summarized above are only the first step in

attempting to computationally understand the interaction of

NBs with mineral surfaces and the possible roles of mineral

surfaces as catalysts for their formation. Besides the effects

summarized above, several other factors may influence

adsorption, such as initial equilibrium concentration of

adsorbates; type of mineral and NB; the chemical environ-

ment, including the pH and ionic strength of the solution; the

presence of specific cations and anions; redox potential; and

external physical conditions, such as temperature and pressure.

Additional comprehensive investigations need to be performed

to gain more insight into these phenomena and to understand

in depth the interactions of lipids, amino acids, peptides,

NBs, nucleosides, nucleotides and DNA molecules (and their

analogues) with mineral surfaces. Future studies should also

focus on other types of minerals by considering the influence

of different size, shape and properties of adsorbents to indicate

the effect of surface sites and adsorption states on binding and

energetics. Other topics worthy of investigation include

whether reactions can occur between NBs and mineral sur-

faces during specific adsorption, how complex multi-step

reaction mechanisms proceed, and how the nature of the

intermediates in these and their transition states are affected

by adsorption. These goals result in an enormous combinatorial

space of organic molecule-mineral, organic molecule-solvent,

solvent-mineral and other environmentally-determined condi-

tions which deserve study. Classical experimental methods of

studying adsorption make this a daunting challenge and the

development of high throughput methods could undoubtedly

have a significant impact on the field.

Acknowledgements

HC, JL and AM were supported in part by the National

Science Foundation (NSF) and NASA Astrobiology Program,

under the NSF Center for Chemical Evolution, CHE-1004570.

HC also acknowledges support from the NASA Astrobiology

Institute – Director’s Discretionary Fund (NAI-DDF). NS

acknowledges support from NSF EAR CAREER award

(EAR 0346889), American Chemical Society Petroleum

Research Fund (41777-AC2), NAI-DDF, a Wisconsin Alumni

Research Foundation (WARF) award from the University

of Wisconsin, and start-up funds from the University of

Akron. RH acknowledges support from the NSF, NAI, the

Alfred P. Sloan Foundation, and the Deep carbon Observatory.

The use of trade, product, or firm names in this report is for

descriptive purposes only and does not imply endorsement by

the U.S. Government. The tests described and the resulting

data presented herein, unless otherwise noted, were obtained

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from research conducted under the Environmental Quality

Technology Program of the United States Army Corps of

Engineers by the USAERDC. Permission was granted by the

Chief of Engineers to publish this information. The findings of

this report are not to be construed as an official Department of

the Army position unless so designated by other authorized

documents.

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