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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