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www.rsc.org/chemsocrev Volume 41 | Number 16 | 21 August 2012 | Pages 5365–5568 Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05.

Themed issue: Prebiotic chemistry ISSN 0306-0012 Guest editors: Jean-François Lambert, Mariona Sodupe and Piero Ugliengo CRITICAL REVIEW H. James Cleaves II, Andrea Michalkova Scott, Frances C. Hill, Jerzy Leszczynski, Nita Sahai and Robert Hazen Mineral–organic interfacial processes: potential roles in the origins of life 0306-0012(2012)41:16;1-7 View Article Online

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Guest editors Jean-François Lambert, Mariona Sodupe and Piero Ugliengo

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

H. James Cleaves II,a Andrea Michalkova Scott,bc Frances 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 a Blue Marble Space Institute of Science, Washington, modern geochemical phenomena including petroleum forma- DC 20016, USA 1 2 b U.S. Army Engineer Research and Development Center (ERDC), tion and maturation and the global carbon cycle. These sorts Vicksburg, MS 39180, USA of interactions were potentially also important for the origin of c Interdisciplinary Nanotoxicity Center, Jackson State University, life on Earth,3–11 and on extra-terrestrial bodies. Jackson, MS 39217, USA d Department of Polymer Science, University of Akron, It is notoriously difficult to define ‘‘life’’, which causes Akron OH 44325, USA significant problems for efforts to understand its origin (see, e NASA Astrobiology Institute, University of Akron, Akron, for example, the special section in the journal Astrobiology Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. OH 44325, USA (2010) volume 10, pp. 1001–1042). One popular definition is f Carnegie Institution of Washington, 5251 Broad Branch Rd. NW, Washington, DC 20015, USA that life is a ‘‘self-sustained chemical reaction capable of w Part of the prebiotic chemistry themed issue. undergoing Darwinian evolution’’12 (i.e., one capable of

Dr Cleaves received his PhD Andrea Michalkova Scott was in chemistry in 2001 from the born in Slovak Republic. She University of California, received MS in Mathematics San Diego, then conducted and Chemistry in 1997 and post-doctoral research at the PhD in Inorganic Chemistry Scripps Institution of Oceano- in 2002 (working with Daniel graphy and the Carnegie Tunega) from Comenius Institution of Washington. University in Bratislava, His research concerns organic Slovakia. This was followed geochemistry, abiotic organic by nine years of post-doctoral synthesis, the question of how work in Jerzy Leszczynski’s life arose on Earth, methods group at Jackson State for detecting Life on other University, Jackson, MS. In planets and the interactions 2011 she joined the U.S. H. James Cleaves II of organic compounds with Andrea Michalkova Scott Army Engineer Research mineral surfaces. Presently he and Development Center is exploring the application of chemoinformatics to prebiotic (ERDC) in Vicksburg, MS where she works now as a chemistry and the analysis of extraterrestrial materials. He is a Research Chemist. research scientist at the Blue Marble Space Institute of Science.

5502 Chem. Soc. Rev., 2012, 41, 5502–5525 This journal is c The Royal Society of Chemistry 2012 View Article Online

replication with mutations which are able to be culled by general catalysis,18 albeit with low specificity and efficiency. The natural selection). According to some definitions, this system ubiquity of mineral–water interfaces at the surface of the Earth must also be membrane-bounded. renders it almost impossible to discount the role of interfacial The origin of life is generally envisioned as having pro- process with organic molecules relevant to the origin of life. ceeded from the formation of organic compounds from Modern biochemistry mainly uses protein enzymes, which environmentally-supplied precursors, to their self-organization are genetically-encoded polymers of a-amino acids, as cata- under various environmental conditions into self-replicating lysts. Many of these include a cofactor such as an organic and energy-transducing systems, and their further evolution coenzyme, a metal sulfide cluster or a metal ion. Some into modern biochemical systems.13,14 These ideas are open to enzymes have evolved to be almost perfect catalysts, in that experimental investigation, where the types of chemistry and they represent an exquisite balance between the affinity of the plausible geochemical environments must be given due con- catalyst for both substrate and transition state binding, and sideration. For example, models for the origin of life include product release.19–21 Such enzymes provide rate enhancements schemes for the origin of membranes,15 metabolic cycles10 and of as much as 1020 fold for specific chemical reactions, though nucleic acids (e.g., the RNA World16), many of which invoke more typical values are on the order of 106 to 1015-fold).22 The catalytic or functional roles for mineral surfaces. reasons evolution selected a-amino acids to construct catalysts Given the many likely available mineral types, and the hetero- remain speculative,23,24 but recent laboratory results suggest geneity of their surfaces in natural environments,17 mineral that once formed, such enzymes were able to explore an almost surfaces could potentially have provided almost any type of limitless catalytic space.25

Frances C. Hill is a native of Jerzy Leszczynski is a Cleveland Heights, OH. She Professor of Chemistry and received a BA in Chemistry the President’s Distinguished from Case Western Reserve Fellow at Jackson State University, MS in Geochemistry University (JSU). He joined from Purdue University, the faculty of the JSU Depart- and PhD in Mineralogy/ ment of Chemistry in 1990. He Geochemistry from Virginia directs the Interdisciplinary Tech. She completed post- Nanotoxicity CREST Center doctoral research at the at JSU. His broad research University of Notre Dame, interests include various and Rutgers University. She applications of computational spent eight years at the Army chemistry. Dr Leszczynski High Performance Computing obtained his MS and PhD Frances C. Hill Research Center in Minneapolis, Jerzy Leszczynski degrees at the Technical MN, as the lead computational University of Wroclaw in chemist. Since 2007 she has worked as a Research Chemist/ Poland, where he was also a fculty member from 1976–1986.

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. Team Leader for the computational chemistry team at the US In 1986 he moved to the USA, initially working at the University Army Engineer Research and Development Center (ERDC) in of Florida, Quantum Theory Project (1986–88) and at the Vicksburg, MS. University of Alabama at Birmingham (1988–1990).

Professor Nita Sahai has been Robert M. Hazen, Senior the Ohio Research Scholar Chair Research Scientist at the in Biomaterials, Department Carnegie Institution of of Polymer Science, University Washington’s Geophysical of Akron since August 2011. Laboratory and the Clarence Prior to this, she was a Robinson Professor of Earth Professor in the Department Science at George Mason of Geoscience, University of University, received the BS Wisconsin-Madison for 11 years. and SM in geology at the Prof. Sahai’s research focuses Massachusetts Institute of on the physical-chemical Technology (1971), and the aspects of cellular and bio- PhD at Harvard University molecular interactions at in earth science (1975). mineral surfaces, of relevance The Past President of the Nita Sahai to prebiotic chemistry, bio- Robert Hazen Mineralogical Society of mineralization and bone tissue America, Hazen’s recent engineering. Her research is supported by NSF, NASA and research focuses on the possible roles of minerals in the origin ACS-PRF. Prof. Sahai has been interviewed on National Public of life. He is also Principal Investigator of the Deep Carbon Radio’s, ‘‘To the Best of Our Knowledge,’’ for her research on Observatory (http://dco.ciw.edu). the origin of life.

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Biological systems are required for the production of dispersed throughout the observable universe. We briefly protein enzymes, so what molecules or phases could have review the formation of both types of compounds. catalyzed pre-biotic polymerization, ‘‘proto-metabolism’’ and Most of the chemical elements heavier than Li were pro- ‘‘proto-self replication’’? Abiotic organic catalysis might have duced in the interiors of large stars shortly after the Big Bang, been sufficient, but mineral surfaces could also have provided then dispersed later during supernova events.35 This process an almost limitless array of catalytic sites which could have resulted in a generally decreasing abundance with atomic contributed to prebiotic organic complexification. In contrast number, with exceptions that are attributable to fusion cycles to biological enzymes, however, mineral surfaces were likely that occur in stellar interiors. 56Fe is especially abundant, not genetic, in the sense that there were no feedback loops for because it is the most stable element that can be synthesized the regeneration of the catalyst and, thus, no Darwinian easily from a-particles. Silicon (Z = 14) and oxygen (Z =8) evolution in the strict sense. On the other hand, there have are also especially common as they are so-called ‘‘even-nuclei’’

been suggestions that minerals might initially have been elements and, thus, the silicates (containing SiO4 subunits) are genetic systems,26 and it has been suggested that metal-sulfide also cosmically abundant. co-factors may be relicts of primordial surface-promoted Much of the solar nebula was initially composed mainly of chemistry.27 Thus, mineral surfaces may have served to H and He, the two most cosmically abundant elements, but jump-start, if not sustain, the complexification of organic also included the entire periodic table of elements,36 resulting matter. in the elemental distribution known as the solar abundance. Minerals lack the enormous combinatorial diversity of During the formation of the solar system, molecular com- organic compounds. There are B4500 known naturally occur- pounds were sorted in terms of distance from the sun approxi- ring minerals,28 with formula weights on the order of a few mately according to their boiling points. Radial mixing, hundred to a few thousand daltons. This same molecular however, scattered these compounds in smaller amounts weight range includes a vastly larger number of organic throughout the early solar system. Lighter, more volatile compounds. For example, a recently computed set of com- compounds generally froze in the outer regions of the solar pounds containing only up to 13 total C, N, O, Cl or S atoms system, giving rise to the cometary bodies of the Oort cloud contained 9.77 108 compounds, and these were pre-filtered and Kuiper belt as well as the gas and ice giant planets and for their drug-like properties, greatly reducing the size of the their moons, whereas the heavier, more refractory elements final library.29 This relative paucity of combinations in terms were concentrated in the inner solar system giving rise to the of structure and composition may be a benefit in making the terrestrial planets, Mercury, Venus, Earth and Mars, and the experimental exploration of mineral surface catalytic potential asteroid belt. Asteroids are rocky bodies that did not accrete to considerably more tractable. the terrestrial planets, thus, being the ‘‘leftovers’’ of planet We review here the literature on the topic to date, and formation.36 attempt to highlight blind spots that could be addressed by The terrestrial planets are ‘‘rocky’’. Rocks are aggregates of experimental and computational approaches in future studies. minerals. A mineral is a naturally-occurring inorganic com- We will set the stage by exploring which kinds of minerals and pound that has a fixed chemical composition or range of organic compounds were likely on early Earth, and which compositions and a specific crystal structure. On Earth and geochemical environments might plausibly have brought them other rocky planets, primary minerals are formed from cooling

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. together. We then review studies in mineral-organic inter- and crystallization of magma (a mixture of molten or semi actions of possible relevance to the origin of life, and conclude molten rocks, volatiles and solids). Transformation of primary with a more detailed discussion of some recent computational minerals by weathering and alteration at planetary surfaces approaches. produces secondary minerals. We will not consider the potential role of water or other Rocky planets are thought to be especially suited as abodes volatile ices on prebiotic chemistry. While ice is a recognized for life because they provide a solid surface that can support mineral species, and it is likely that ice interacted with the presence of liquid water and temperatures that allow for chemical species of relevance to the origin of life during the the existence of liquid water. These conditions may require a early history of the solar system, chemistry occurring in ice planet to be relatively near to its parent star, which would phases is complex, and may include ice surface promoted require the planet to be largely composed of refractory effects as well as eutectic concentration effects. For further (or high-boiling point) inorganic components such as metal description of ice chemistry of prebiotic relevance, the oxides and silicates. interested reader is referred to ref. 30–34. Liquid water on rocky planets. It is generally presumed that liquid water is a pre-requisite for life.37 The stability of liquid 2. Plausible minerals, organic compounds and water requires a planet to be close enough to its star that the environments on early Earth surface temperature is above freezing but distant enough to prevent boiling.38 Some of Earth’s water inventory is believed 2.1 Formation of the elements (nucleosynthesis), stars, the to have been delivered by bolides, including meteorites and solar system and minerals comets.39 Bolide impact rates would have been much greater Chemical compounds can be broadly classified as organic or early in Earth’s history when the planet was accreting from inorganic depending on the quantity and oxidation state of the rocky planetesimals similar to the asteroids.40 The Earth carbon they contain. Compounds of both types are widely 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 It remains possible that on the early Earth, as today, there underworld) eon, because Earth’s surface temperatures were were a variety of local and microenvironments in which a wide believed to have been much higher than the boiling point of range of conditions, such as pressure, temperature, pH, exposure water. Oxygen isotopes in the oldest known terrestrial zircons to light and oxidation state of volcanic out-gassing. 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 The prebiotic distribution of mineral species. The possible results push back to the earliest stages of Earth’s history and roles of mineral surfaces in protecting, selecting, concen- provide a considerably longer time-span for surface temperatures trating, templating, and catalyzing reactions of prebiotic compatible with liquid surface water (‘‘cool early Earth’’) and, organic molecules are recurrent themes in discussions of consequently, the self-assembly of organic molecules into life’s origins. Since the pioneering suggestions of Bernal5 and replicating systems. Goldschmidt,3 who independently speculated on the possible The bolide impact assumed to have been responsible for influences of various minerals in the origins of life, many formation of the Moon would have re-melted the entire Earth authors have proposed general principles and detailed scenarios B4.5 Ga, and there may have been a period called the ‘‘Late for mineral-assisted biogenesis.52–56 Heavy Bombardment’’ (LHB) B3.8 Ga when meteoritic Among the specific mineral groups that have been invoked, impact rates increased briefly and surface temperatures may clay minerals are the most frequently cited.57–69 Various have been frequently elevated above the boiling point of transition metal (e.g., Fe, Ni, Co and Cu) sulfide minerals water.43 While some have seen the LHB as a restriction for have also been proposed to have played key catalytic roles in when the origin of life could have occurred, others suggest life prebiotic organic synthesis.10,27,70–86 Many other minerals could have survived the LHB,44 and others have questioned have also been proposed, including quartz,87–89 feldspar,90,91 whether the LHB occurred as interpreted.45 zeolites,90,91 olivine,92,93 rutile,94,95 ferrous metal alloys,96 The oldest known accepted microfossils date from B3.5 Ga transition metal phosphides,97 transition metal hydroxides,8,98,99 and are associated with shallow marine evaporitic environments.46 micas,100 hydroxylapatite,101–103 alkaline earth metal carbonates104 Thus while early cells may have survived in sub-surface and borates.105,106 environments, which seems plausible given that modern In spite of these numerous proposals, few authors have bacteria have been found as deep as 2.8 km in mines,47 early addressed the question of which minerals might actually have life either rapidly colonized or re-colonized surface environ- been present on the prebiotic Earth (Tables 1 and 2) (see, ments. Alternatively, early life may not have survived the LHB however, ref. 107 and 108). If a particular mineral phase was and may have evolved a second time on Earth. In any event, rare or absent, then it is unlikely to have been a significant the presence of lower surface temperatures and liquid water on contributor to the origins of life. Earth’s surface would have resulted in rapid weathering of The hypothesis of ‘‘mineral evolution’’, which outlines Earth’s primary surface minerals, increasing the mineral types 10 stages of near-surface mineral diversification since the available for interaction with prebiotic organics. beginning of the Earth, offers some insight to this question.28,109 There is considerable evidence that Earth’s mantle and core The starting point of mineral evolution is a group of a dozen differentiated rapidly, and that the oxidation state of Earth’s ‘‘ur-minerals’’ that condensed during the cooling and expan- mantle has been at its current state since B4.35 Ga.48 The sion of the gaseous envelopes of supernovas and red giant

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. oxidation state of the mantle would have governed the oxida- stars—those that are enriched in ‘‘heavy’’ element (i.e., Z Z 6). tion state of the gases emitted by volcanism. It is, therefore, Diamond was probably the first mineral in the cosmos, owing to

often presumed that the amount of CO2,SO2 and NO2 in the its high temperature of crystallization (B4400 1C) and the atmosphere would have been much higher than in the modern significant concentration of carbon in the atmospheres of large atmosphere, and would likely have resulted in acidic oceans.49 active stars. The graphite polymorph of carbon; moissanite (SiC); 50,51 Alternative scenarios envision alkaline early oceans. 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 Metavolcanic komatiite, amphibolite, olivine, clinopyroxene, garnet, serpentine, antigorite, magnetite, talc, magnesite, epidote, rocks ultramafic rock orthopyroxene, biotite, chlorite, phlogopite, kyanite, chromite, rutile, ilmenite, sulfides, amphibole (hornblende) dolomite, calcite, K-feldspar, plagioclase, cordierite, apatite Banded iron BIF, ferruginous quartz, magnetite, amphibole clinopyroxene, orthopyroxene, olivine, garnet, chlorite, formation chert tremolite, calcite, magnesite, hematite, goethite, apatite, sulfi des, zircon, graphite Schist ferruginous shale, quartz, biotite, amphibole, muscovite, sillimanite, kyanite, staurolite, andalusite, (metapelite) mudstone, siltstone, garnet, chlorite cordierite, plagioclase, epidote, microcline, clinozoisite, argillite 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 and Metasomatic contact* quartz, siderite, dolomite, calcite, clinopyroxene, orthopyroxene, olivine, amphibole, garnet, metacarbonate hydrothermal edifice* ankerite, magnesite, magnetite phlogopite, biotite, feldspar, muscovite, chlorite, epidote, rocks fuchsite, apatite, hematite, sulfides, graphite

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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)4 Brucite Hydroxide Mg(OH)2 Calcite Carbonate CaCO3 2+ 3+ Celadonite Silicate, Illite group KMg0.8Fe 0.2Fe 0.9Al0.1Si4O10(OH)2 Chalcedony Oxide SiO2 Clinoptilolite Silicate, Zeolite group (Na,K,Ca)2-3Al3(Al,Si)2Si13O3612(H2O) Daphnite Silicate, Chlorite group (Fe,Mg)5Al(Si,Al)4O10(OH)8 Dawsonite Carbonate NaAl(CO3)(OH)2 Diaspore Hydroxide a-AlO(OH) Dolomite Carbonate (CaMg)CO3 2+ 3+ Greenalite Silicate, Serpentine group (Fe ,Fe )2-3Si2O5(OH)4 Gyrolite Silicate, Mica group Ca4(Si6O15)(OH)23H2O Magnesite Carbonate MgCO3 Mesolite Silicate, Zeolite group Na16Ca16(Al48Si72O240)6H2O Montmorillonite Silicate, Smectite group (Na,Ca)0.33(Al,Mg)2(Si4O10)(OH)2nH2O Nontronite Silicate, Smectite group Ca0.5(Si7Al0.8Fe.2)(Fe3.5Al0.4Mg.1)O20(OH)4 Portlandite Hydroxide Ca(OH)2 3+ Prehnite Silicate, Sheet silicate Ca2(Al, Fe )(AlSi3O10)(OH)2 Saponite Silicate, Smectite group Ca0.25(Mg,Fe)3((Si,Al)4O10)(OH)2n(H2O) Siderite Carbonate FeCO3 Stilbite Silicate, Zeolite group NaCa4[Al9Si27O72]30H2O

rutile (TiO2), corundum (Al2O3), spinel (MgAl2O4), hibonite and the subsequent processing in those planetesimals by (CaAl12O19); and the silicates, forsterite (Mg2SiO4) and thermal metamorphism, aqueous alteration, and impact enstatite (MgSiO3), have also been discovered as micro- or shocks, saw a cumulative total of approximately 250 different nano-particles in pre-solar dust grains (inter-planetary dust minerals.121,122 Among the key new minerals formed in stage 2 particles).110–113 All of these refractory minerals condensed at are the first significant accumulations of feldspars, phosphates, temperatures above B1900 1C and likely formed within the and clay minerals. All of these phases are found in meteorites, first hundred million years following the Big Bang. The and all have thus been present continuously at or near Earth’s refractory minerals have been present continuously on Earth surface for more than 4.5 billion years. since its formation.114 Subsequent mineral evolution on the young Earth resulted A principal objective of ‘‘mineral evolution’’ research is to from the sequential evolution of igneous rocks, including the document the mechanisms and timing by which these dozen stage 3 generation of basaltic magmas from partially molten minerals were processed in the solar nebula, planetesimals and peridotite, and the subsequent stage 4 generation of granitic on Earth to generate the more than 4500 mineral species melts by partial melting of basalt (e.g. ref. 123 and 124). known today. One significant result of this research is the Terrestrial mineralogical diversity also increased by the forma- proposal that the great majority of minerals—perhaps tion of hydrous minerals, notably hydroxides, clays and zeolite

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. 3000 species of the B4500 currently known—arose after the minerals, as well as localized deposits of evaporate minerals. Great Oxidation Event at B2.2 Ga and, thus, are a con- Hazen et al.28 estimated that igneous magmatic differentiation sequence of life’s influence on the chemical state of the oceans and near-surface processes resulted in B500 different mineral and atmosphere.28,115 Furthermore, many rare elements, species. However, subsequent mineralogical diversification including Li, B, Be, Hg, Se, As, Bi, Sb, U, and Th and many required significant time. For example, London125 estimated others, required at least a billion years of fluid-rock inter- that a billion years was required for the generation of complex actions to achieve sufficient concentration to form new pegmatites that represent eutectic fluids enriched in rare minerals.106,114,116–119 Thus as many as 1000 additional minerals elements. Approximately 500 minerals, including a variety of formed abiotically must postdate the time of life’s origins. We Li, Be, Cs, Nb, Ta, U, Th and other species, are unique to conclude, therefore, that the great majority of minerals— these deposits. Subduction and associated abiotic mineraliza- perhaps as many as 4000 of the 4500 known species—could tion associated with arc volcanism also generates hundreds of not have contributed to life’s origins. In that context, which new mineral species, for example massive sulfide deposits that mineral phases were present 4 billion years ago? contain more than 100 exotic sulfosalts (metal sulfide minerals Stage 1 of mineral evolution, which occurred during the first with one or more other chalcogenide elements, for example, few million years following the Sun’s earliest radiative phase Se, As, Sb, or Bi). However, recent studies suggest that (beginning B4.567 Ga),120 incorporates approximately 60 minerals subduction-driven plate tectonics, and associated continent that condensed in the early solar nebula to form the primitive formation and arc volcanism, did not become a significant chondritic meteorites.28,121 This includes all of the dozen process on Earth until approximately 3 billion years ago.126 ur-minerals, plus a variety of Mg–Al–Ca–Fe silicates and In summary, many of the minerals mentioned above which oxides, Ni–Fe–Mg–Mn–Ca sulfides, Fe–Ni phosphides, and are commonly-invoked for the origin of life were almost Fe–Ni metal alloys. certainly present on the surface of the early Earth. Various Stage 2, which encompasses mineralogical consequences of sulfides, most notably those of Fe and Ni, were ubiquitous if not the accretion of chondrites, the differentiation of planetesimals, plentiful, along with meteoritic Fe–Ni alloys and phosphides,

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although the abundance of these latter categories may have mechanism of clay mineral production may have been the been limited to a lower steady-state concentration due to weathering of volcanic rocks in acidic surface environments, their lability. Feldspar, olivine, rutile, hydroxides and zeolite resulting in montmorillonite. In summary, serpentine and minerals would also have been readily available, and are thus montmorillonite would have been the dominant clay minerals reasonably invoked in origin of life scenarios. In contrast, before 3.5 Ga. neither quartz nor phosphates were volumetrically significant The above discussion suggests that most of the minerals prior to 4.0 Ga, but increased rates of granitization would invoked for origins of life research would have been present on have produced more quartz, alkali feldspar, and hydroxy- Earth prior to 3.5 Ga. In the following pages we consider lapatite from 4.0 to 3.5 Ga. The presence of Hadean and recent approaches to understanding the nature of those Paleoarchean (B3. 6–3.2 Ga) carbonates is as yet unconfirmed interactions. (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 Available early environments. The vast majority of Earth’s solubility of these minerals compared to the others discussed mass is contained in its core and mantle, yet the most above. important minerals with respect to the origin of life were those The diverse group of fine-grained layer silicates, collectively present at the surface from volcanism and extraterrestrial called clay minerals, deserve special mention. Clay minerals, delivery, and the corresponding secondary minerals produced especially from the montmorillonite group, are often from weathering at Earth’s surface.28 Most organic com- employed in origins of life experiments, because of their high pounds of modern biochemical relevance are composed of specific surface area and the ability of certain clay minerals to simpler moieties, and include heteroatoms such as nitrogen, absorb organic molecules. Confusion arises, however, because sulfur and oxygen, as for example in amino acids, sugars and there are more than 50 distinct approved phases, as well as nucleobases (NBs). It is widely believed that life formed from many mixed phases, such as bauxite, bentonite, phengite and these simpler organic compounds (see, for example, ref. 130). steatite that are sometimes characterized as clay minerals. Such molecules are, however, not particularly stable at high These diverse phases can be grouped into seven major clay temperatures for extended periods of time.131–133 Thus, it is the mineral groups, each of which is distinguished by its layered minerals that come into contact with Earth’s hydrosphere at atomic structure, its interlayer constituents and its relative moderate temperatures, which were likely of greatest relevance ability to expand in water.127,128 to origin of life. This assumption still leaves an enormous Elmore128 noted five principal mechanisms of clay mineral inventory of minerals of potential relevance, and numerous formation: (1) subsurface aqueous/hydrothermal alteration; plausible environments, with the two types most discussed in (2) authigenesis, described as in situ formation from a parent the literature being shallow evaporative environments and mineral, especially from pore-solution in marine sediments; submarine hydrothermal fields. (3) low-grade metamorphism to greenschist facies, representa- Modeling studies of basalt weathering under putative early tive of temperatures of B400 to 500 1C and depths of about atmospheric conditions suggest a complex suite of secondary 8 to 50 km, with subsequent exposure through orogenesis minerals107 (Table 1). Petrographic evidence suggests that the (mountain-building) related to plate tectonics; (4) near-surface minerals shown in Table 2 were already present on the surface weathering reactions, especially under oxic and/or acidic of the primitive Earth by 4.0–3.6 Ga, and perhaps somewhat

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. conditions; and (5) the rise of the biosphere, most notably earlier,108 confirming and extending the conclusions of the advent of soil-forming microbes, fungi and plants, and Schoonen et al.107 and Hazen et al.28 associated biological weathering. Of these five mechanisms, A variety of possible environments could plausibly satisfy only the first (via serpentinization) and anoxic near-surface the criterion of being in contact with the primitive hydrosphere weathering would have been significant prior to 3.5 Ga. Earlier at reasonably low temperatures. These include sub-aerial authigenesis (mechanism 2) was limited by the dearth of environments on nascent continents or island arcs including Hadean and Paleoarchean marine sediments; greenschist beaches and inland hydrothermal springs,134 as well as sea- facies rocks (mechanism 3) were rarely exposed at the surface floor environments including sediments and environments prior to the onset of plate tectonics which is estimated by some associated with rising mantle plumes or sea-floor spreading to have begun by at least B2.5 Ga; the atmosphere was devoid centers.135–137 Recently, the remarkable properties of pumice,

of O2, so oxic weathering (mechanism 4) could not have perhaps occurring in floating pumice rafts, as a possible site occurred; and there was no biologically-mediated weathering for the origin of life has been suggested.138 During eruption (mechanism 5). We conclude that most clay minerals observed pumice develops the highest surface-area-to-volume ratio in modern sediments would not have occurred in any signifi- known for any rock type and is the only known rock type cant volume prior to 3.5 Ga. Indeed, the only major clay that floats at the air–water interface. Pumice can be exposed to mineral species prior to life’s origins was probably serpentine, an unusually wide variety of conditions, including dehydration the product of aqueous alteration of olivine and other ferro- under atmospheric interfaces. As will be discussed, for many magnesian silicates in the ubiquitous mafic and ultramafic biochemically relevant condensation reactions, the elimination rocks of the early crust.129 Alteration of Ca–Al silicates, of water is particularly important. These porous rocks can including the plagioclase feldspar anorthite, must have adsorb metals, organics, and phosphates and host inorganic resulted in some production of montmorillonite, kaolinite as catalysts such as zeolites and titanium oxides. A caveat to well as halloysite, and mixed clay assemblages would also be the idea of pumice serving as an environment for the origin expected in such alteration zones. The only other significant of life, however, is that most pumices are acidic (felsic) to

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intermediate in composition, and basaltic compositions are what must have been rather dilute organics are not as obvious rarer. The abundance of typical acidic – intermediate compo- as in evaporitic environments. Mineral surface adsorption sition pumices on early Earth before widespread formation of offers one possibility. Recently, thermophoresis, in which continents is open to further investigation. organics are concentrated in mineral pores subject to thermal gradients, has been suggested as another possible mechanism,152 Evaporitic environments. Shallow surface environments, and some experiments support this idea.153 such as intertidal zones and inland lakes (e.g., the Great Salt Lake), offer the obvious advantages of being in direct contact Models for the origin of life. As mentioned above there is with atmospheric and extraterrestrial sources of prebiotic presently only a broad idea of how life originated on Earth. organics, and providing locations for concentration of molecules Most modern models for this process assume the presence and ions by evaporation.139 These environments, however, of one or more types of molecules found in present-day would also have been subject to higher ultraviolet radiation biochemistry, for example lipids, nucleic acids, amino acids (UV) fluxes, as it is generally believed that as the primitive or small metabolites such as Krebs cycle intermediates (for

atmosphere contained little free O2, and consequently little general reviews see ref. 154–156). ozone (O3), thus providing little shielding from the higher UV One major schism in modern hypotheses is that between output of the early Sun.140 On the other hand, other atmospheric replicator-first and metabolism-first models. Replicator – first and oceanic mechanisms may have offered UV-shielding.141,142 models (‘‘RNA world’’) generally assume that a primordial For example, even thin sediment layers in shallow or subaerial genetic molecule initiated Darwinian evolution, and thus consider environments could have completely shielded organic com- the prebiotic synthesis of RNA or some RNA-like molecule as the pounds form UV radiation.141,143 Seafloor environments would, central problem in the origin of life.154,155,157,158 Metabolism-first likewise, have shielded organics from UV exposure. models generally focus on the prebiotic synthesis of metabolic Mineral surface – catalyzed photolysis may have been a intermediates and their cyclic interconversion,10,159 or on the significant source of organics and reduced nitrogen species,144–146 synthesis of small catalysts such as peptides.63,160 The two models and may also have been a significant mechanism for organic need not be mutually exclusive,161 and mineral surface adsorption destruction. Indeed, minerals have been implicated via UV phenomena may have assisted both.162 induced photodegradation in explaining the absence of organic compounds on Mars.147 Likely available organics. A variety of processes likely Typical sedimentary minerals include clay minerals, zeolites, contributed to early Earth’s (and possibly early Mars’) organic oxyhydroxides of iron, aluminum and manganese, calcite, inventory, including processes such as atmospheric synthesis, diatomaceous silica, pyrite and various evaporitic minerals extra-terrestrial input, from bolide impact and geothermal and such as calcite, gypsum, epsomite, and halite (see Tables 1 planetary surface syntheses.163 and 2). Clay minerals are especially significant as they have The organic products of the action of ultraviolet light, high high specific surface areas and are often the final weathering energy radiation and electric discharges acting on various products of basaltic minerals, so adsorption of organic com- types of gas mixtures have been the subject of extensive pounds on clay minerals has been studied extensively. Clay investigation since Miller’s pioneering 1953 experiment.164 minerals appear to be common on the surface of Mars,148 as Extraterrestrial sources, such as meteorites, micrometeorites

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. do evaporitic minerals such as hydrated sulfates.149 Many and comets could also have been important sources of pre- other minerals also have high specific surface areas such as biotic organic compounds.40 Submarine hydrothermal systems zeolites, oxyhydroxides of iron, aluminum and manganese, have been offered as additional sites of organic synthesis.151 calcite, amorphous silica and pyrite, but these have not been Surface-water photochemistry may also have been an impor- studied as extensively in the origin of life literature. tant source of reduced organics, as it has been suggested that great quantities of ferrous iron (Fe2+) were present in the Submarine environments. Marine hydrothermal vents, both early oceans because of early Earth’s low atmospheric 2+ high – temperature sulfide – dominated ‘‘black smokers’’ and pO2. This Fe could have served as a reductant for lower – temperature carbonate – dominated ‘‘white smokers’’, bicarbonate, yielding appreciable amounts of reduced one- associated with submarine, ocean ridge spreading centers have carbon species.165 attracted a good deal of attention as possible sites for the Rather than describe all of the nuances and variations in origin of life.10,150,151 Such environments may provide a prebiotic synthesis that have been investigated over the years variety of advantages over subaerial locations, including the (for reviews of this topic see ref. 154, 156 and 166) we stress UV shielding problem. Hydrothermal vents also offer sites that some, but by no means all, biochemicals have robustly with continuous thermal and concentration gradients of demonstrated-prebiotic syntheses and could have been plau- molecules. It has, therefore, been proposed that the vents sibly present in certain terrestrial environments prior to the may be good sites for abiotic organic synthesis, especially origin of life. As an important cautionary note regarding the if the atmosphere was not particularly reducing. Mineral potential organic complexity in the primitive environment, a surface – catalysis provided by hydrothermal minerals such recent investigation of the Murchison meteorite has shown as sulfides has been suggested as an important aspect of the that there remain perhaps millions of as-yet-unidentified potential for organic synthesis in these environments.82,84 organic compounds which could also have been present.167 While submarine environments may offer an alternate loca- For the purposes of this review, neither the specific model tion for prebiotic organic synthesis, means of concentrating 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 Fig. 1 Schematic showing the general tendency for adsorption of molecules (spheres) to increase with increasing (a. - c.) solute mixtures, either by removing molecules which interfere in a concentration at a fixed volume to mineral surface (plane) area ratio. given solution-phase reaction, or by leaving undesirable The arrows in the figure represent the direction of motion of solute or molecules in solution, and concentrating desired ones in the solvent molecules. adsorbed state. Equilibrium adsorption is usually described using iso- and ionic strength. The amount adsorbed is assumed to be therms, or plots of the quantity of a given species per unit of the amount of solute lost from solution after interaction with solid adsorbant at various solution compositions and at a fixed the solid particle suspension. In many studies the results are temperature. Various units for the adsorbed species may be reported in terms of mass or moles of compound adsorbed per reported, including molecules, moles or mass. The choice of unit weight of mineral. This is unfortunate because the surface units for the adsorbing solid phase is, typically, given in units area of the mineral is of primary importance and determines

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. of mass or specific surface area (area per unit mass of solid). the ratio of surface area to solution volume and concentration. It is important to recognize that the same mineral phase may For example, a given surface area of mineral will not adsorb have a widely varying specific surface area depending on its the same amount of solute from 1 ml of solution of a given source or means of synthesis. concentration as from 100 ml of a solution containing the Generally speaking, adsorption can be considered as an same concentration of solute. equilibrium between dissolved and adsorbed phases of the Adsorption can be often be described by a Langmuir type same species. The affinity of organic molecules for surfaces can isotherm, which displays a steady rise in adsorption with vary widely depending on their size, available functional increasing concentration of solute until reaching an asymptotic groups, solubility, and charge, as well as the properties of maximum representing a complete monolayer of adsorbed the mineral surface, such as surface charge, dielectric constant, species. In some cases, however, this is a gross over-simplification and crystal structure,169 under the conditions of the measure- and Langmuir-type adsorption behavior is commonly not ment. The experimental variables include, for example, pH, observed, as species may adsorb in multilayers or adsorb temperature, ionic strength, presence of inorganic ions which cooperatively either with other molecules of the same type or may facilitate adsorption by forming salt bridges and/or by with some other dissolved species, for example a dissolved modulating solvophobic effects, and all these factors may inorganic ion. Also, if the data follow a Langmuir-type affect the speciation of mineral surface sites. It is typically isotherm, it does not confirm the single-site, monolayer found, however, that the greater the solution concentration adsorption mechanism. Adsorption mechanisms must be of a species, the greater the number of surface adsorbed determined by spectroscopic analyses in situ. molecules (Fig. 1). Importantly for discussions of adsorption behavior in The simplest method for studying mineral–organic inter- natural environments, the higher the ratio of solvent-accessible actions is the batch isotherm method. In this type of study, solid surface area to solvent volume, the closer the adsorbed an aliquot of mineral powder is added to a solution containing molecules will be to one another. The closer the adsorbed an organic compound of interest, at a fixed solution pH molecules are to one another, the greater the likelihood that

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they will interact with one another, underscoring the need magnitude lower.166,171 At such low bulk oceanic concentra- for some sort of initial concentration mechanism such as tions, it is unlikely that organic compounds would have been evaporation or thermophoresis for pre-biotic synthesis. For significantly concentrated on mid-ocean sediments or minerals.162 homogeneous intra-molecular catalysis in solution, however, Simple concentration mechanisms such as evaporation, concentration need not be an important factor. provided subaerial land masses existed at that time, could Based on modern Earth’s radius, the Earth’s surface area is easily have circumvented this problem. The ease with which we B5.1 1013 m2, with B71% or 3.6 1013 m2, covered by can envision such mechanisms given modern surficial pro- water. The modern ocean volume is B1.3 1021 L, giving a cesses does not guarantee that these types of environments volume to surface area ratio of B3.6 106 Lm2. This ratio existed on the primitive Earth. could scale several tens of percent given that there was likely Adsorbed organics would likely modify surfaces presenting less continental surface area early in Earth’s history, and that entirely new adsorption phenomena, in some sense organic the ocean volume may have changed somewhat over time. coated surfaces are yet another type of mineral. It has been However, it is critical to recognize that Earth’s surface area is suggested that vast amounts of complex high-molecular highly fractal, with the ocean floor often being covered with weight organic polymers similar to melanoidans could have many meters of sediment, mud or ooze, giving a solvent- been deposited in marine sediments during the prebiotic accessible surface area thousands to millions of times greater, era.172,173 and a consequently greater ratio of solid surface area to water Temperature likely has an important effect on surface volume, presenting considerably more sites for adsorption. adsorption, with some species being more strongly adsorbed Lahav and Chang conducted an important early survey of at higher temperatures and others more weakly adsorbed. adsorption literature of possible relevance to the origin of Most studies are conducted at room temperature for practical life,162 and examined the interplay between solute concen- reasons, but adsorption could be drastically different at other tration, solute type and mineral surface area. An especially temperatures. Temperature affects surface acidity, isoelectric illustrative figure from their publication is reproduced in points of surfaces and ionic solutes, adsorption isotherms of Fig. 2. minerals, lipid bilayer fluidity, etc. The effect of temperature It has been estimated that the total concentration of amino on adsorption, with its obvious implications for various acids in the prebiotic oceans was on the order of 103 M under postulated early environments, remains a significant lacuna very favorable synthesis or bolide delivery conditions, while in our understanding of the potential for concentration of those of the nucleobases may have been several orders 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+

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. 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 Fig. 2 Relationship between mean intermolecular distance (reciprocal specific surface area and giving rise to new mineral veneers, density, or surface area occupied per adsorbed molecule) between with different adsorption properties than the mineral initially adsorbed molecules, equilibrium solute concentration, surface adsorp- being studied, for example via the oxidation of surface iron tion equilibrium constant (K) and mineral surface area (A). Brackets species. Careful characterization of surfaces before and after represent typical adsorption equilibria K values for A: several amino adsorption is seldom conducted, but may at times be necessary. acids such as alanine, glycine, leucine and serine, and glucose; B: most The complicated nature of mineral surface transformation in of the purine and pyrimidine bases and nucleosides; and C: the 180 aminoalkylated nucleotides studied by Burton et al.170 For example, more complex geomimetic environments was demonstrated at 103 M equilibrium solute concentration, an amino acid adsorbed using a hydrothermal vent reactor designed to test the models of 77 on clay (a high specific surface area mineral, right-hand y-axis) would Russell and colleagues. have its nearest neighbor between 100 and 1000 A˚ , or approximately Adsorption studies tend to focus on the solution conditions 10–100 molecular diameters distant. Adapted from ref. 162 that yield measurable changes over the time-scale of the experiment.

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The ratios of solution to surface area, and solution concen- The protective effects of organic adsorption on mineral tration to surface area must be appropriately balanced in surfaces may be important for preserving biomolecules as order to observe adsorption. Clay minerals have been favorite biosignatures, or for preserving organics for their concen- topics of study because they are significant components of soils tration on early Earth. These effects may be associated with (and thus are of interest for various agricultural funding the exclusion of water from the reaction milieu. The racemiza- sources); because they have extremely high specific surface tion of amino acids in carbonate mineral matrices was found areas (a gram of clay may have a surface area roughly to be roughly as fast as that occurring in solution.192 To this equivalent to a tennis court, whereas a gram of coarse sand end the types of evaporitic minerals found on the surface of may have a surface area of a few cm2); and clay minerals have Mars have attracted great interest, as they may dictate ionic exchange sites, and are thus reminiscent of ion exchange the types of mineralogies that might preserve early martian resins.57,181–183 biosignatures.193 The observed association of early bio- Organic adsorption to mineral surfaces may approximately signatures on Earth with evaporitic environments46 may also be generalized based on functional group chemistry. Because hold true on Mars, assuming that the Earth’s biosphere and a ionic bonds are relatively strong, and many biochemicals potential Martian biosphere followed similar evolutionary contain ionizable functional groups, interactions between trajectories. Aubrey et al.194 found some evidence for the amines, phosphates or carboxylic acids are often the focus of preferential preservation of amino acids in ancient (B25 Ma) adsorption studies. sulfate minerals which was later corroborated by Kotler et al.195 Mineral surfaces can be characterized by their points of zero charge (PZC), similar in concept to an isoelectric point. The Amino acids. Considerable effort has been focused on the PZC is the pH at which the net surface charge averaged over interactions of amino acids with mineral surfaces. Modern protein all sites is zero, but may possess balanced positive and negative enzymes contain 20 canonical a-amino acids, approximately charges. As the net positive or negative charge on a mineral half of which are considered not to have been primordial.24,196,197 surface changes as a function of pH, the surface becomes a The primordial amino acids are generally assumed to be the better or worse adsorbant for species of the opposite charge, structurally simplest (thus excluding the aromatics), so that and the net charges on adsorbing organic compounds may their interactions would have been governed primarily by also change as a function of pH.184 Solution pH is thus a electrostatic interactions. All amino acids exist as zwitterions fundamentally important parameter in adsorption studies. over a broad pH range, because they contain at least two Distinct from the classical batch adsorption studies, adsorp- ionizable groups, with pKa values ranging from 2–3 (for the tion affinity has also been studied in flow-through conditions carboxylic acid group) and 8–9.5 (for the amine group). using high-pressure liquid chromatographic techniques.174,185,186 Most studies have focused on investigating the adsorption Chromatography essentially depends on the interactions of of negatively-charged amino acids on positively-charged solutes, solvents and the stationary phase. Rather than the loss mineral surfaces or vice versa. This choice has been driven of the solute to adsorption, the retention of the solute by the mainly by the practical issue of being able to detect measur- stationary phase is measured, in terms of the lag time for the able amounts of adsorption. Since amino acids are typically solute to emerge in the solvent front. Adsorption of molecules zwitterions in solution, adsorption could result in the forma- as solvents flow past stationary mineral phases could also tion of a surface coated with solvent-exposed charges of the

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. result in the phenomenon of geochromatography, which has same polarity as the original surface and, in the case of amino been suggested to be a potential mechanism for sorting acids such as glutamic acid, high surface coating could result complex prebiotic mixtures.187 in the presentation of a surface coated in charges opposite to Adsorption is not always a mechanism for preserving the original surface’s. Thus a positively-charged mineral sur- organic molecules. Instead, adsorption may also result in face could become a good adsorbant for positively-charged degradation of the organics. Radioactive elements such as species if coated with zwitterionic organic species. This 40K+ (b-decay half-life = 1.25 109 years) were likely much cooperative phenomenon could lead to co-adsorption effects, more abundant on the primitive Earth. The K+ ion is highly as has been noted by Lambert and coworkers.198 water-soluble and adsorbs well to clay surfaces. Thus, organics concentrated on clay minerals by adsorption would have been Mineral surfaces as catalysts co-localized with a potent b-emitter, which may have made Minerals could be catalysts for a variety of potentially clay surfaces especially destructive environments for organics.188 important prebiotic reactions. However, it is important to Very low recovery of amino acids was obtained after adsorp- bear in mind that true catalysts promote reactions that are tion to clay minerals and irradiation with a 60Co gamma ray thermodynamically favorable, but kinetically inhibited, but source.189 lowering the energy barrier. Catalysts thus speed the approach Transition metal-containing mineral surfaces may also be to thermodynamic equilibrium, but do not alter that final capable of photocatalytic degradation of organics, because of equilibrium. However, minerals certainly alter the kinetic the presence of reactive oxygen species generated on the landscape of organic transformations over geological timescales. mineral surfaces by Fenton-like reactions. For example, adenine is readily oxidized on pyrite surfaces by peroxides Peptide formation catalyzed by mineral surfaces. A number generated from reaction of surface ferrous iron with water,190 of studies have been conducted exploring the potential for and copper-containing clay minerals increase the degradation mineral surfaces to catalyze peptide bond formation. Lahav rates of adenine and adenosine.191 and coworkers have shown that clay minerals including

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kaolinite and bentonite speed the rate of formation of oligo- favors formation of higher oligomers. The effects of the glycine when these were cyclically dried together and heated.63 specific clay mineral were found to depend both on the nature The final species distribution was compatible with the attain- of the mineral and the solution phase reactants. ment of thermodynamic equilibrium, suggesting that the clay surface is indeed acting as a true catalsyst. Marshall-Bowman Lipid and membrane formation catalyzed by mineral surfaces. et al.199 showed that several likely common prebiotic mineral Fatty acids and polyprenol phosphates spontaneously form surfaces, such as hematite, pyrite, rutile and amorphous silica, micelles and vesicles in aqueous solution when placed at the promote the hydrolysis of peptides over the background appropriate pH, lipid concentration and salt concentrations. solution rate. This phenomenon has been used to argue that lipid-like Using a combination of experimental and computational materials may have been involved in the formation of the techniques, Lambert et al. investigated the mode of amino acid earliest cells.33 covalent adsorption in the dry state on minerals, and how Ourisson and coworkers have shown several addition reac- these amino acids might form polypeptides when heated.200 tions catalyzed by minerals which lead to higher isoprenoids Schreiner et al.201 examined the ability of amino acids to be lipid compounds, for example the conversion of farnesol to 209 oigomerized by carbonyl sulfide (COS) on pyrite surfaces squalene over iron(III) sulfide, and the synthesis of geraniol

using computational methods. COS has been demonstrated and its isomers from the condensation of C5 monoprenols in to assist short peptide formation in fairly concentrated the presence of montmorillonite.210 solution.202 Schreiner et al. found that the pyrite surface was Hanzyc et al.65 offered compelling micrographic evidence able to change the free energy landscape of the elementary that clay mineral surfaces can speed up the formation of reaction steps, and that the mineral could directly participate vesicles over very short (minutes to hours) timescales. The in some of the reaction steps, changing the reaction mecha- minerals apparently provide nucleation sites for vesicle for- nism compared to the situation in bulk water. These computa- mation after adsorption of the fatty acids. It is not clear that tional results have not been tested experimentally. such systems would overcome the limitations to vesicle for- Kawamura et al.203 examined peptide formation in a hydro- mation imposed by the critical vesicle concentration (CVC), thermal flow reactor at 275 1C and near neutral pH at contact which is the concentration at which vesicles become the more times limited to a few seconds. It was found that a preformed stable form of dissolved fatty acids compared to the mono-

alanine tetramer (Ala4) could cross-react to form higher pep- meric dissolved state. In fact, as a new phase (the mineral tides to a greater extent in the presence of some minerals, in surface) is added to the system, which may remove fatty acids particular, the carbonates calcite and dolomite. Tourmaline, from solution, the presence of minerals may make the CVC galena, apatite, mica, sphalerite, quartz, chalcopyrite, and higher. In evaporative environments, this effect is likely of pyrite did not enhance longer peptide yields. However, the marginal importance, as the concentration of fatty acids could total available surface area of the minerals was not strictly range from extremely dilute to solid. controlled, thus hampering comparison across these minerals. The integrity or rupture of phospholipid vesicles and the All of the minerals also significantly catalyzed the degradation affinity of bilayers in contact with oxide mineral surfaces has

of the starting Ala4, in agreement with the results of Marshall- been examined by bulk adsorption isotherms, atomic force Bowman et al.199 microscopy, neutron reflectivity, and classical DLVO theory

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. Clay mineral suspensions in alternating drying-heating modeling.211–215 The head-group charge of the lipids as well as (to 85 1C)-wetting cycles were also found to promote the oxide surface charge, solution ionic strength and effect of oligomerization of glycine up to the pentamer, and shorter divalent Ca2+ ions was examined. It was found that phospho- mixed oligomers of Asp-Gly and Val-Gly.204 A similar cata- lipid vesicles are more stable in contact with positively-charged lytic effect was observed for aluminum oxides with GlyGlu mineral surfaces such as corundum rather than negatively- peptides.205 Rimola et al. conducted calculations suggesting charged minerals surface such as quartz. The results of Sahai that feldspar surfaces might also enhance peptide elongation and co-workers are consistent with the work of Hancyzc et al. rates.206 (2003) in showing that mineral surface chemistry can affect The coupling of mineral hydration to organic oligomeriza- protocell stability. It is recognized that phospholipids are tion has been investigated inspired by the observation that biologically-produced molecules but these are routinely used many biological polymerization reactions are dehydration in protocell studies, as alternatives to fatty acids or oil condensations.207 To test this hypothesis, glycine was mixed droplets.

with simple anhydrous salts (MgSO4, SrCl2, BaCl2 and The formation of C–O–P ether bonds in phospholipids is a Li2SO4) at 140 1C for up to 20 days, which promoted Gly high energy reaction and is catalyzed in biology by enzymes. polymerization. Oligomers up to Gly6 were synthesized from The formation of phospholipids is, therefore, considered to be

Gly–MgSO4, with concomitant hydration of the mineral. The one of the major knowledge gaps in the origins of life. total yield was about 200 times larger than that from heating Extending the work of Oro´ on the dehydrative synthesis of Gly alone. more complex membrane lipids such as acylglycerols,216 Salt induced peptide formation coupled with peptide chain Maheen et al. were able to show the synthesis of glycerol elongation on clay minerals starting from dipeptides and phosphates under hydrothermal conditions.217 dipeptide/amino acid mixtures was investigated by Rode and coworkers.208 It was shown that both reactions can take place Chirality. Biochemistry is remarkable in its preference simultaneously and that the presence of mineral catalysts 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 of RNA, although again no effort was made to normalize for this chiral preference has received a great deal of attention in surface area in this study. the field. Since the pioneering work of Louis Pasteur, it has The adsorption of NBs to graphite, likely a minor mineral been known that mineral crystals can occur in different chiral phase but perhaps a general model for a non-ionic surface, forms, and the various surfaces of a mineral may be asym- showed the general trend that purines are adsorbed more metric. Globally, the various mirror-image surfaces of a given strongly than pyrimidines,239 consistent with other studies mineral are likely to be balanced but, locally, mineral surfaces for adsorption on clay minerals (bentonite, kaolinite, and may present interesting environments for chiral selection. montmorillonite)240 and rutile.241 Enantiomeric excesses have been observed for some amino Theng and coworkers242 conducted a study on the adsorp- and hydroxy acids in carbonaceous chondrites, including non- tion of NBs, ribose and phosphate (Adenine (A), Cystosine biological amino-acids such as isovaline, some of which could (C) and Uracil (U, hereafter referring to uracil, rather than the be due to mineral effects.218 Hazen et al. were able to demon- element uranium)) to Mg2+-exchanged montmorillonite and strate a preference for the adsorption of aspartate enantiomers found that the isotherms were typically of the C-(constant on chiral calcite surfaces.104 Activated nucleotide monomers partitioning) type, where the amount adsorbed increased may preferentially form homochiral oligomers when elongated linearly with the equilibrium solute concentration. The bases over homoionic montmorillonite.219 were proposed to adsorb by coordination to Mg2+ ions through On the other hand, zirconium dioxide surfaces have been water bridges. Little ribose was adsorbed, again indicating the shown to catalyze the racemization of secondary alcohols,220 importance of ionic interactions. Phosphate adsorption showed and montmorillonite has been shown to catalyze the racemiza- an L- (Langmuir) type isotherm, indicating strong chemi- tion of amino acids.221 adsorption and a saturation phenomenon. The plateau value of adsorption for phosphate (B0.012 mmol g1) showed that Nucleic acids and their components. Saladino and coworkers phosphate adsorbed on the edge surfaces of montmorillonite. have conducted a number of studies examining the effects of The differences in adsorption behavior of ribose and phosphate various mineral phases on the reactions of neat formamide were interpreted to reflect differences in ionizibility, size and (FA), and shown that many minerals, including iron sulfides, solubility, underscoring the importance of strong ionic inter- montmorillonite, and rutile are catalysts for the formation of actions, which have been suggested to have been a selective nitrogen heterocycles, including some of those found in nucleic pressure for biology’s choice of the coded amino acids.243 acids.222–227 Kamaluddin and co-workers have conducted a number of The so-called formose or Butlerov reaction,228 involving the studies on the adsorption of mononucleotides and found alkaline oligomerization of formaldehyde,229 has long been similar adsorption isotherms for several metal oxides.244,245 held to be the most important prebiotic source of sugars, The phosphate moiety was found to be especially important especially of ribose, for the development of a primordial for adsorption, in agreement with other studies. There is, RNA World. A wide variety of minerals including clay however, some discrepancy as to the role of other functional minerals and calcite have been shown to catalyze the formose groups in adsorption as compared with the conclusions of reaction.230,231 other authors.241 These nuances in adsorption modes are Early studies of mineral-catalyzed formose reactions were important in determining the ability of the mineral surface

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. somewhat disappointing with respect to the origin of an RNA to serve as a scaffold for higher-order oligomerization and World because, despite catalytic effects, ribose was always templating reactions.246 found to be a minor component of a complex product The adsorption of ssDNA on olivine, pyrite, calcite, hematite, mixture.232 More recently, however, Prieur233 and Ricardo and rutile was examined at pH 8.1 and room temperature. et al.105 have shown that conducting the formose reaction over Results showed that when normalized for surface area, there borate mineral surfaces results in enhanced synthesis of ribose- was little difference in the adsorption of short (B30 nucleotide) borate adducts. Although there has been debate over the oligonucleotides on surfaces, suggesting that most minerals abundance (hence, relevance) of borates in prebiotic contexts,106 become equivalent for nucleic acid adsorption at a relatively silicates have also been found to have a stabilizing effect on short oligonucleotide length.247 ribose at high pH.234 The question of how borate- or silicate- An enormous amount of research has been conducted over ribose adducts were selectively stripped of borate or silicate, the years demonstrating the catalysis of oligonucleotide for- nucleosidated and phosphorylated merits further study. The mation from activated RNA monomers by mineral surfaces, further influence of molybdate and carbonate on these reac- most notably by Ferris and coworkers, frequently using tions was also reported.235 Clay minerals such as perlite were montmorillonite.219,248–251 Using activated phosphoimidazolides, shown to catalyze the formation of sugar phosphates by montmorillonite has been shown to speed oligomerization Maheen et al.,236 however Baldwin et al. showed conversely reactions, and in some cases to be able to do so in a manner that minerals including several metal oxides and hydroxides that enriches homochirality. An important gap in the field is to can be catalysts for the hydrolysis of phosphate ether C–O–P address how the RNA monomers or phosphoimidazoles bonds.237 would have been activated in the prebiotic environment. Borate minerals have been shown to stabilize ribose.105 The Swadling and coworkers252 examined the adsorption of nucleic ability of borate minerals to stabilize RNA in water or acid oligomers on layered double hydroxide minerals compu- formamide has also been studied.238 Most borate minerals tationally and concluded that DNA has some significant were found to either have no effect or to catalyze degradation advantages over RNA or PNA (peptide nucleic acid).

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Mineral surfaces as reactants and complications surrounding anaplerotic reactions (those in which the intermediates must be cyclically regenerated) have Several proposals have been put forward in which mineral attracted appreciable skepticism.261,265–267 Ross’ thermo- surfaces undergo irreversible stoichiometric reactions that dynamic calculations268 suggest that the presence of FeS is could have contributed to prebiotic chemistry. As mentioned not enough to drive CO reduction. above, Fe2+ in solution or at mineral surfaces may have been 2 an important photo-reactant for organic synthesis, resulting in oxidized Fe3+ iron and reduced carbon in a stoichiometric Clay mineral adsorption modeling manner. Hydrothermal redox reactions of reduced iron species Clay minerals may have characteristics conducive to the with dissolved nitrogen species has also been shown to be a concentration of precursor organic molecules for the synthesis potential source of reduced nitrogen in the primitive of biomolecules on early Earth. Kaolinite and dickite are clay seas.80,94,253 More recently, sphalerite-assisted photochemistry minerals with a 1 : 1 dioctahedral layered structure.269,270 The (ZnS) has been proposed as an important prebiotic synthetic layers consist of a tetrahedral sheet formed from SiO tetra- process.146 Many of the carbon fixation reactions central 4 hedra and an octahedral sheet consisting of AlO octahedra. to Wa¨ chtersha¨ user’s surface metabolism model are also 6 Dickite differs from kaolinite in layer stacking. The unit cell of stoichiometric,74 with carbon reduction being coupled to iron dickite consists of two kaolinite layers and is twice as large as or sulfur oxidation. the unit cell of kaolinite. Layers are held together by hydrogen Schreibersite ((Fe,Ni) P, has been proposed as a stoichio- 3 bonds between surface hydroxyl groups on the octahedral metric source of phosphorylated and phosphonylated organic side and the basal oxygen atoms on the tetrahedral side. compounds on the primitive Earth.254 This synthesis over- Montmorillonite is a 2 : 1 clay mineral belonging to the comes some of the previous objections to phosphate minerals smectite group.269,270 Each layer is composed of two tetra- such as apatite serving as prebiotic phosphorylating reagents, hedral silica sheets sandwiching an octahedral alumina sheet. such as their insolubility and non-reactivity.255 It is important In all of these minerals, isomorphic substitution can occur in to note, however, that schreibersite is a rare mineral on Earth, the octahedral sheet (the most common being replacement of though common in iron–nickel meteorites. Mg2+ by Al3+) and/or in the tetrahedral sheet (with Al3+ substituted for Si4+).271 These substitutions can lead to the Computational studies of experimental results and theoretical presence of permanent negative charges or local charge models defects,272 which are compensated by cations such as Na+273 Common nickel and iron sulfide (Ni–Fe–S) minerals of hydro- present between adjacent tetrahedral–octahedral–tetrahedral 2+- thermal origin, such as greigite (Fe3S4) and violarite (Fe sandwich layers. The broken edges of the clay platelet-like 3+ Ni2 S4) have been proposed as catalysts in metabolism-first particles expose silicate and aluminate sites, called edge sites. models for the origin of life256 (see also ref. 257 and 258 for Protons can adsorb at edge sites, resulting in pH-dependent reviews). Wa¨ chtersha¨ user’s ‘‘metabolism first’’ theory for the surface charge. origin of life proposes surface adsorbed primordial metabolic Reactions of formamide (FA), a simple polar prebiotic

cycles driven by oxidative formation of pyrite (FeS2) from molecule, have been studied with a wide array of mineral ferrous sulfide (FeS) and confined to the Ni–Fe–S and Fe–S surfaces.222–225,274–277 FA can serve as a building block for

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. mineral surfaces.10 Based on Raman spectroscopic studies, several compounds of biological interest, possibly by dehydration violarite nanocrystals were suggested to act as a carbon to form cyanide as an intermediate.278,279 When heated in the

monoxide dehydrogenase (in place of pentlandite, (Fe,Ni)9S8), presence of a variety of mineral catalysts, including kaolinite, because in violarite the sulfur atoms on the surface are likely to zeolites, olivines, phosphate minerals, TiO2 and cosmic dust be hydrogenated, leaving the nickel and iron sites available for analogues,224 FA condenses into a variety of nitrogen hetero- reaction.259 cycles, including many of the canonical NBs.222–225,280,281 A few studies have investigated the mechanism of the Horvath et al. recently summarized results from vibrational 260 FeS/H2S redox system and its properties. Kalapos criticized spectroscopy and X-ray powder diffraction studies of kaolinite the notion of surface-adsorbed metabolic cycles261 based on organo-complexes, including kaolinite-FA.282 The kaolinite energetic considerations (an aspect not addressed in recent surface may be altered through chemical reactions by insertion reviews by Anet262 or Cody84). Interestingly, a new stoichio- of FA.283 The degree of intercalation of FA depends on metry was proposed, and the energetics of this novel reductive whether kaolinite is ordered (low defect) or disordered (high citric acid cycle were compared with those in the original defect).284 FA is also known to adsorb on minerals of the version.72 Thermodynamic analysis of this putative archaic kaolinite group by hydrogen bonds between the CQO group

chemoautotrophic CO2 fixation cycle and its self-organization of FA and mineral surface inner sphere (covalent) hydroxyl in hydrothermal systems was conducted.263 group complexes.285–289 Edge sites are mainly involved in these One problem with this model is that the synthesis of citric adsorption interactions, while basal surfaces remain essentially 290 acid from CO2 on FeS catalysts has thus far proven elusive unoccupied. IR spectroscopy studies indicate that inner- (see ref. 264 and references therein). One of the reasons for the sphere bonding between the hydroxyl groups and organic failure is that for redox reactions, favorable thermodynamics molecules is weaker for FA than for N-methylformamide.291 alone are not sufficient to ensure the formation of significant The prebiotic availability of purine and pyrimidine base deriva- amounts of products; kinetics must also be considered.264 The tives from hydrogen cyanide-based chemistries seems likely,292–295 lack of thermodynamic calculations for the individual reactions, with synthesis perhaps mediated by eutectic concentration.296–298

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Both organic and inorganic soil components may be impor- with protons to ensure electroneutrality of the entire system. tant for the surface adsorption of NBs.299 Depending on their Solvating water molecules were initially placed close to the composition, NBs can have markedly different affinities for Na+ ions as this position was shown to be the most favorable mineral surfaces.300 Polyvalent cations, especially alkaline on the mineral surfaces.314 earth cations,301,302 can also promote NB adsorption.303 At Calculations of systems involving NBs with water, cations higher concentrations these cations can interact with NBs, so and clay minerals were performed using density functional as to disrupt inter-NB hydrogen bonding and compromise the theory (DFT).315 Several DFT functionals (B3LYP (Becke, structural integrity of nucleic acid polymers.304–306 In the three-parameter, Lee–Yang–Parr), BLYP316,317 and M05-2X318) presence of cations, purines adsorb more readily to some clay were used. Application of the B3LYP functional in studies of surfaces than pyrimidines do.162 For most studied minerals at large systems has become popular in the area of adsorption neutral pH, nucleotides were adsorbed most strongly, followed on clay minerals; however, this functional has some unsatis- by nucleosides and free NBs. This sequence depends on factory performance issues such as underestimation of the mineral type and solvent conditions, such as pH, temperature energies for weak non-covalent interactions.319 Binding and ionic strength, which can alter the mineral surface proper- energies were therefore also calculated using the M05-2X ties, such as net charge and charge density.307 functional. M05-2X is a hybrid meta-exchange–correlation Clay mineral surfaces efficiently adsorb amino acids308 and functional319 derived from the M05 functional,320 which NBs. Some pyrimidines, which are not normally adsorbed adds a kinetic energy component to the exchange–correlation onto clay minerals, may interact with purines and co-adsorb functional. on clay surfaces. NBs interact with the interlayer cations of Several basis sets, including two Ahlrichs valence split basis clay minerals by various exocyclic functional groups and ring sets321 and pseudopotential LANL2DZ322–324 were used to nitrogen atoms,309 where adsorption is partially governed by calculate the modeled reactions involving small Fe–S clusters. van der Waals interactions and H-bonds.310 U adsorption on Employing an electron core potential (ECP) basis set such as 241 rutile (TiO2) was significantly weaker than that of A or C, LANL2DZ (Los Alamos National Laboratory 2 double z possibly due to the involvement of electrostatic interactions. for transition metals) has become popular in computations U was suggested to adsorb cooperatively, edge-on, rather than of transition metal-containing systems. The medium size parallel, to the surface.241 The surface site density for different 6-31G(d) basis set325 was employed due to the large size of minerals can vary significantly allowing possible adsorption of calculated models in the case of adsorption of NBs on clay a complete monolayer of U.311 The adsorption of NBs and mineral surfaces. their derivatives can vary in the entire range from 0–100% Topological characteristics of electron density distribu- depending on experimental conditions.188 tion were obtained using Bader’s ‘‘Atoms in Molecules’’ approach,326 which gives insight into the nature of bonds. 4. Computational models and methods An occurrence of the (3,1) critical point of the electron density between two atomic centers indicates the presence of Computational approximations involving model clusters or a stabilizing interaction, generally interpreted as the existence periodic systems can be used to predict interactions of model of a chemical bond.327,328 The charge density (r(r)) and the prebiotic molecules with mineral surfaces. A cluster model of a Laplacian of the electron density (r2r(r)) at such points were

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. single kaolinite layer was prepared using experimental crystal also calculated. In the case of closed-shell electron interactions structure data in order to study the adsorption of FA and NBs (ionic bonds, van der Waals interactions or hydrogen bonds) a on kaolinite group minerals.312 Each cluster was constructed small r(r) and a large and positive r2r(r) are typically as a cut-off from the periodic structure of the mineral. Both observed. The maps of electrostatic potential of the NBs tetrahedral and octahedral clay surfaces were mimicked in adsorbed on clay minerals were calculated using the Molekel order to investigate which surfaces preferentially interact with program package.329 The values of the interaction energy the studied molecules. These models consist of one ring of the (Eint) of the systems studied were obtained as differences

tetrahedral sheet formed from six SiO4 tetrahedra, and/or one between the energy of the complex and the sum of the energy ring of the octahedral sheet containing six AlO6 octahedra. values of the adsorbate and adsorbent subsystems. The Eint Dangling bonds at the edges of the clusters were saturated value was corrected (Ecorr) for basis set superposition errors with protons. Several initial positions of the adsorbate were using the counterpoise method.330 tested to investigate which orientation toward the mineral Solvation of the system was modeled in two different ways. surface, such as parallel or perpendicular orientations, First, the supermolecular approximation was applied, which mediated by cation–p or cation–heteroatom interactions, is involves the explicit consideration of microsolvation by water preferred. Substitution of Al3+ by Mg2+ in the octahedral molecules. Second, solvent molecules were replaced by a fragment and Si4+ by Al3+ in the tetrahedral sheet was also dielectric continuum with a permittivity, e, surrounding the modeled. Following substitution, the model was made electro- solute molecules outside of a molecular cavity (Conductor-like neutral by addition of Na+. Screening Model).271 Water with a relative dielectric constant

Models of Ni–Fe sulfide were constructed as truncations of of er = 78.39 was used as a solvent. The values of interaction the crystal structure of violarite.313 Due to changes caused by enthalpy (DH), Gibbs free energy (DG) and entropy (SDT) optimization, the original model was modified. The new model were calculated using the rigid rotor-harmonic oscillator-ideal consisted of one Fe atom, one Ni atom, and six sulfur atoms. gas approximation based on the vibrational frequencies of the Dangling bonds on four of the sulfur atoms were saturated 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 Wa¨chterha¨user’s surface metabolism model Despite the impact of Wa¨ chterha¨ user’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: CH SH + CO + H O - CH COOH + H S (3.1) 3 2 3 2 Fig. 3 Modeling of the carbon fixation pathway catalyzed by the This reaction can be divided into two separate sub-reactions as Fe–Ni–S model. The DGr values (kcal mol1) are calculated at the shown below: B3LYP/TZVP level of theory. Reprinted from ref. 333 with permission from Elsevier. CH3SH + CO - CH3COSH (3.2) In contrast, several studies calculated the Gibbs free energy of CH3COSH + H2O - CH3COOH + H2S (3.3) the formation of pyrite (FeS2)fromH2S and iron monosulfide The sequence of transformations of adsorbed reactants on (FeS) to be exergonic at standard state (–10.0 kcal mol1,334 1 72 1264 Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. the NiS–FeS surface and the thermodynamics of each step of 9.2 kcal mol , and 7.5 kcal mol ). Physico-chemical this mechanism were calculated.333 Fig. 3 shows the Gibbs free analysis based on thermodynamic potentials predicts this energy of reaction (DGr) for each step of the proposed value to be 3.3 kcal mol1 at room temperature.263 Ross,268 mechanism of the carbon fixation pathway. however, calculated that the conversion of FeS does not The addition of carbon monoxide into the Fe–Ni–S model provide enough energy to drive CO2 reduction. by binding with the iron center (forming an Fe–CO center) These results do not allow a conclusive discussion of

and addition of the CH3SH molecule are characterized by possible reaction pathways. Laboratory kinetic studies need positive DGr values. The most endergonic step is migration of to be performed under conditions mimicking those in hydro-

the CH3 group to a surface Fe site. The total DGr value of all thermal settings to confirm the feasibility of these reactions. reactions (expressed by eqn (3.2)) is positive by 37.7 kcal mol1, Interactions of FA with minerals of the kaolinite group which means the reaction is not feasible as modeled, at least in the gas phase, at 373 K. Intercalation and adsorption of FA on two clay minerals, Most of the remaining steps of the putative cycle are dickite and kaolinite were investigated using both cluster

characterized by negative DGr values (binding of the CH3 (intercalation and adsorption) and periodic (intercalation) group to the carbonyl group anchored to the Fe center, approaches.335–337 The intercalation of FA in dickite was dissociation of a water molecule and formation of acetic acid). found to be strongly specific. The structure having two FA If one considers only the reaction described by eqn (3.3) molecules in the same orientation is more stable than the

(formation of acetic acid and H2S from CH3COS acid and structure with different orientation of a pair of FA molecules water), this process is exergonic by 21.0 kcal mol1. How- within the same interlayer space.336 Formations and orienta- ever, the DGr value of the overall reaction summarized by tions of hydrogen bonds between intercalated or adsorbed FA eqn (3.1) is positive by 16.7 kcal mol1 (see Fig. 3 for details). and mineral layers were found to be similar in all of the This result suggests that the proposed cycle will not proceed studies. Moreover, the orientation and interactions of the spontaneously under the modeled conditions. adsorbed FA molecule with the octahedral surface are similar

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than 12 kcal mol1 for five different configurations.338 The difference in the binding energies for different geometries amount to 5.6 and 2.9 kcal mol1, 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/ Fig. 4 The optimized structure of formamide adsorbed (A–D-FA displaced, and cation/heteroatom interactions. Dispersive forces (ads)) (A) and intercalated (B–D-FA(int)) (B) on dickite. Reproduced between the NBs and the surface were shown to be essential for from ref. 335 with permission from Elsevier. stabilizing the adsorbed complexes in the face-to-face and cation/ p-displaced configurations. The preferred mode of adsorption for as found for the intercalated model.335 The FA oxygen atom guanine (G) and C with bidendate coordination is the cation/ was shown to play the main role in the formation of contacts heteroatom configuration due to electrostatic interactions, which with atoms of the aluminosilicate layer and in the energetic corresponds to larger adsorption energies than those found for stabilization of all intercalated/adsorbed systems. A, U and T. T and U display a preference for the cation–p/ Fig. 4 illustrates the optimized structure of the FA-dickite displaced configuration. The gas phase interaction energies, adsorbed (A – D-FA(ads)) and intercalated systems computed at the B3LYP/6-311+G(2df, 2p) level for the alkali (B – D-FA(int)). FA is placed close to the center of the metal cation interacting with isolated C or G, and for O4 tetrahedral (and octahedral) ring in both intercalated coordination of T and U were calculated to be nearly twice as FA-dickite and FA-kaolinite systems. FA forms four hydrogen large.342 Adsorption of NBs on surfaces without Na+,eitherin bonds with both surfaces.335,338 Two of these H-bond contacts face-to-face or orthogonal orientations, is sizable for all of the are formed between surface hydrogen atom and FA carbonyl NBs studied, with adsorption energies ranging from 3.7 to oxygen atom, in which the FA oxygen atom behaves as a 11.3 kcal mol1, due to the stabilizing effect of dispersion proton-acceptor. In both intercalated and adsorbed systems, interactions. All bases except G show a preference for the face-to- FA forms additional H-bonds with the octahedral surface face configuration. The orthogonal orientation was found to be between the FA carbonyl oxygen atom, the –NH group335–337 2 more favorable for G due to its large dipole moment and the and/or nitrogen atom336,338 and the surface hydroxyl groups. formation of weak hydrogen bonds with the surface. The NH group of FA acts as a proton-donor and the surface 2 In the case of alkali metal cation-NB binding in the gas oxygen atom behaves as a proton-acceptor. In intercalated phase,343–348 the rotation of the exocyclic amino groups of A complex H-bonds are also formed between the NH group of 2 and C is revealed, which rehybridize from sp2 to sp3 to FA and the siloxane surface (see Fig. 4 in ref. 335). The bond coordinate the metal cation. This sp3 rehybridization is not Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. lengths of groups of adsorbed and intercalated FA, which observed in solution349 nor in the above discussed study.340 participate in the formation of H-bridges with the surface The most favorable coordination environments for other NBs (CQO, N–H1 and N–H2), are enlarged compared to those in interacting with alkali metal cations in the gas phase corre- isolated FA. Generally, it can be concluded that both inter- spond to the most stable orientations found in ref. 340. calation and adsorption lead to structural changes in FA, which Mignon and Sodupe studied the adsorption of A, G and C correspond to an effort to form the maximum number of on octahedral (Osub) and tetrahedral (Tsub) substituted forms attractive interactions with both mineral surfaces. of montmorillonite.341 Adsorption was shown to involve The interaction energy for adsorbed FA on dickite is spontaneous proton transfer to the NB. The results related –14.6 kcal mol1.335 This value is larger than the binding energy to the binding energy are consistent with other published for the water molecule adsorbed on the aluminum-oxygen site of studies on the adsorption of NBs on mineral surfaces since the kaolinite (value of –10.4 kcal mol)1.339 Thus the FA molecule NBs were shown to interact more strongly by B10 kcal mol1 forms very strong interactions with this type of surface. The with Osub than with Tsub complexes. This is likely due to the calculated intercalation energy of FA-dickite335 is higher than greater acidity of Osub surfaces and the stronger stabilization the adsorption energy for the water-kaolinite system.339 The provided by hydrogen bonding. Binding of NBs in co-planar difference between the adsorption and intercalation energy of orientation was found to be as strong as in orthogonal ones. the FA-dickite system was found to be B5–6 kcal mol1.This G and A were adsorbed more strongly by B6 kcal mol1 on difference represents an additional stabilization of the FA the acidic surface than C (50 vs. 44 kcal mol1). molecule in the interlayer space of dickite. The interaction energies predicted using both approaches (periodic and cluster) Interactions of T and U with dickite differ by only 0.3 kcal mol1, indicating that the cluster model of dickite used to study the FA-dickite systems is likely a good Robinson et al. studied interactions between T and U and approximation.335 On the other hand, the intercalation energy dickite using the ab initio cluster approach (DFT method).350 of FA-kaolinite obtained at the PM3/6-31G(d) level is less Both molecules adsorb in a similar manner, which implies that

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the methyl group of T does not influence binding between the T and U were physisorbed on both hydrated and non- NB and the mineral surface. NBs are less stably adsorbed on hydrated kaolinite surfaces interacting with the Na+ through the tetrahedral surface (denoted as D(t)) than on the octahedral the O2 atom (Fig. 5). Such binding was also found for NBs surface (denoted as D(o)) as was found for the adsorption interacting with bare alkali metal cations343,344 but the NaO of FA335,336,351 and other small molecules352 on minerals of distance was shorter by about 0.1–0.2 A˚ .343,344,355 This attrac- the kaolinite group. Another similarity found in these tive interaction contributes the most to the NB adsorption studies335–338,350–353 is that the most important components strength, depending on several other factors such as the sur- of the intermolecular interactions are hydrogen bonds of face type and orientation of the target molecule on the surface. the O–HO, N–HO and C–HO type. The octahedral Hydrogen bonds between the target molecule and the surface system with T forms a larger number of hydrogen-bonds than hydroxyl groups or the basal oxygen atoms additionally the octahedral systems do with U.350 stabilize the studied complexes. Two hydrogen bonds are T and U adsorb to the octahedral mineral fragments and formed between the adsorbate N1–H1 and C6–H6 groups hydrated tetrahedral mineral fragments by their N3–H groups and two different oxygen atoms of the octahedral site (Os) and O2 and O4 atoms similar to the way in which they interact in or of the tetrahedral site (Ob). In all K(3o)Na-T, K(3o)Na-U, A:T and A:U base pairs.354 The presence of proton donors (the K(3t)Na-T and K(3t)Na-U complexes the N1–H1O bond hydrogen atoms of the OH groups of the octahedral surface or (denoted as HB1 in Fig. 5) is calculated to be stronger than the water) and proton-acceptors (the oxygen atoms of the octahedral C6–H6O bond (denoted as HB2 in Fig. 5). surface or water) governs adsorption. For tetrahedral systems the Addition of Na+ leads to significant stabilization of the presence of only proton-acceptors causes the pyrimidine N1–H tetrahedral systems, which can be seen from comparison of proton-donor surrounded by other proton-donors (the C–H the interaction energy values for T and U adsorbed on groups) to play the main role in intermolecular binding. different mineral surfaces (Na+ free montmorillonite (6to The presence of water has a large effect on the adsorption of 11 kcal mol1),340 including Na+-non-hydrated and hydrated NBs on the cation-free dickite surface. T and U are most tetrahedral surface of kaolinite (24 to 28 kcal mol1),353 and strongly adsorbed on the hydrated octahedral surface. The Na+ free non-hydrated and hydrated surface of dickite (1to adsorption changes the geometrical parameters and atomic 9 kcal mol1)350). The same is true for adsorption on the charges of the adsorbates. This influence is largest for adsorp- octahedral surface of kaolinite. The adsorption energies for tion on the hydrated octahedral surface. The molecular geo- K(3t)Na-T and K(3t)Na-U are larger than those for T and U metry of the studied complexes is modified more significantly binding with Na-montmorillonite.340 They are also larger than for the systems with U while the atomic charges change more those for pyridine adsorbed on dry surfaces of Na-smectite for the systems containing T. (17.2 kcal mol)1314 and for pyridine on a clay cluster substituted with Mg2+.356 Interactions of T and U with kaolinite The explicit inclusion of water as solvent in the calculations has only a small influence on the adsorption of the NBs in the The optimized structure of T adsorbed on the non-hydrated + and hydrated (W) tetrahedral (K(3t)) and octahedral (K(3o)) presence of Na (the oxygen and hydrogen atoms of water kaolinite surfaces with Na+ is shown in Fig. 5.353 These will be denoted hereafter as Ow and Hw). Orientation of the NBs by O2 toward Na+ remains the most favorable in all systems are denoted K(3t)Na-T, K(3o)Na-T, K(3t)NaW-T Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. KNaW systems (see Fig. 5c and d). A water molecule on both and K(3o)NaW-T, respectively. 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 OwH–Os H-bridges and one Ow–HwOs 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–HwOandN–HOw) with isolated water359,360 having Fig. 5 The optimized structures of T adsorbed on the non-hydrated the Ow and Hw atoms in a co-planar position with the (a – K(3t)Na-T, b – K(3o)Na-T) and hydrated (c – K(3t)NaW-T, T molecule. If a cation is added to a system with an isolated d – K(3o)NaW-T) tetrahedral and octahedral surfaces of kaolinite base and water, then one ionic bond with a bond length 2.1 A˚ 355 obtained at the B3LYP/6-31G(d) level of theory. Reproduced from is formed between U and the cation. It can be concluded ref. 353 by permission of the PCCP Owner Societies. that along with the substitution, the surface oxygen atoms also

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govern binding with the adsorbent, cation and water. This the T O2 atom involved in the NaO2 bond in the octahedral influence is also seen for the basal oxygen atoms, which help to systems. Water increases the polarization strength of this stabilize the water molecule by the formation of hydrogen interaction in the tetrahedral system. The cation substitution bonds.314 Addition of water leads to a decrease of the inter- in both mineral fragments changes the surface potential, so action energy of T and U adsorbed on the tetrahedral kaolinite that the negative EP highs in the octahedral systems appear surface,353 but increases the Ecorr value for K(3o)NaW-T. at the surface oxygen atoms, which are in the vicinity of the Therefore, T and U are most stable on the hydrated octahedral Al/Mg substitution. Minimum negative EP values in the surface of kaolinite with an interaction energy of about tetrahedral systems are observed above all basal oxygen atoms 36 kcal mol1. and O2 and O4 atoms of U and T. The NBs interact more strongly with the octahedral than with the tetrahedral surface of kaolinite. The energy difference Conclusions drawn from computational studies is 6 to 7 kcal mol1 for the non-hydrated fragments and 9 to 12 kcal mol1 for the hydrated systems.353 This result agrees The adsorption of FA335–338,351 and NBs350,353 on the surfaces with those for the adsorption of these NBs on dickite350 and of minerals of the kaolinite group and montmorillonite340,341 for the adsorption of FA on kaolinite and dickite.335,336,351 depends on the molecule’s structure and physico-chemical Moreover, the interaction energy of water with the hydroxy- properties, and the chemistry of the surface. All of the studied lated kaolinite surface is 13.1 kcal mol1 while that of water molecules are stabilized better by octahedral mineral sites than with the silicate surface is 4.1 kcal mol1.352 Adsorption on tetrahedral ones. T adsorbs more strongly with the clay sur- the hydrated octahedral surface of kaolinite was found to be face than U340,350,353 or FA.335–338,351 G and C on the external the most stable with interaction energies of B36 kcal mol1. surfaces of Na-montmorillonite show larger adsorption To help determine the energetics of sorption complexes of energies than the remaining three canonical NBs.340 The the NBs on clay minerals, the maps of electrostatic potential predicted characteristics of NBs and FA depend on their (MEPs) between the adsorbate and substrate were calculated. orientation toward the surface and on the presence of water MEPs for the main six-membered ring of the most stable and cations leading to multiple modes of interaction with structures of T adsorbed on K(3t)Na, K(3t)NaW, K(3o)Na, different mineral surfaces. The adsorption of NBs is signifi- K(3o)NaW fragments are illustrated in Fig. 6. cantly influenced by substitutions in the mineral layer and the The MEPs confirm the binding described above for both presence of counter-ions.335,350,351,353 The explicit addition of target molecules with the mineral, which is the most favorable a water molecule to the kaolinite mineral surface only slightly with strong negative basins located above the O2 and O4 changes NB adsorption properties compared to the addition atoms. Addition of water only slightly changes the EP of the of an inorganic cation.353 The large affinity of clay minerals for surface but decreases the negative EP value located above 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-

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. 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 Fig. 6 Calculated maps of the electrostatic potentials of T adsorbed employing translational periodicity are recommended (as for on the non-hydrated (a – K(3t)Na-T; b – K(3o)Na-T) and hydrated example in ref. 340 and 341) to obtain a more complete picture (c – K(3t)NaW-T; d – K(3o)NaW-T) tetrahedral and octahedral surfaces of the properties of calculated systems. For future studies of kaolinite. Figure reproduced from ref. 353 with permission of the a combination of quantum mechanical–molecular mecha- PCCP Owner Societies. nical (QM-MM) or completely classical models is suggested,

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which can be used for calculations of large systems in extended cations and minerals, and the feasibility of Wa¨ chtersha¨ user’s molecular dynamics or Monte Carlo simulations. DFT methods proposed C-fixation cycle (the production of acetic acid from 74 are known to have difficulties dealing with systems where CO and CH3SH). This scheme was shown to be partially dispersion competes with other effects (e.g. in biomolecules).361 catalyzed by model Fe–Ni–S surfaces through the creation of This may significantly affect the accuracy of DFT results, at least surface coordination complexes.333 Synthesis of formic acid

when used alone and uncorrected. Use of newly developed DFT from CO2 and H2S in the presence of pyrite was found to be functionals (for example, M05-2X, as in ref. 353) is one way to endergonic under modeled conditions and the studied reaction overcome these problems. However, this introduces another pathway did not lead to a significant amount of the product in difficulty because DFT results are hampered by dependence on isolated gas-phase systems. The degree to which these results differences in the functional used. Thus, calculations based on mimic aqueous conditions remains to be determined. the Møller–Plesset perturbation theory of the second order The studies summarized above are only the first step in (MP2)362 should be carried out at the same time for comparison. attempting to computationally understand the interaction of NBs with mineral surfaces and the possible roles of mineral Conclusions surfaces as catalysts for their formation. Besides the effects summarized above, several other factors may influence The potential roles of mineral–organic interactions in pre- adsorption, such as initial equilibrium concentration of biotic chemistry are clearly quite complex, and studies have adsorbates; type of mineral and NB; the chemical environ- thus far only scratched the surface with regard to the types of ment, including the pH and ionic strength of the solution; the effects which may ultimately prove important. presence of specific cations and anions; redox potential; and There are many outstanding questions which remain prime external physical conditions, such as temperature and pressure. research targets for surface science studies with respect to the Additional comprehensive investigations need to be performed origin of life. Many of these questions are complicated by the to gain more insight into these phenomena and to understand fact that we do not know how life originated or which in depth the interactions of lipids, amino acids, peptides, geochemical environments were available on primitive Earth. NBs, nucleosides, nucleotides and DNA molecules (and their Nevertheless, the questions can be posed proceeding from the analogues) with mineral surfaces. Future studies should also most general to the more specific. Did mineral surfaces focus on other types of minerals by considering the influence significantly alter the kinetic landscape of important reactions of different size, shape and properties of adsorbents to indicate leading to the origin of life relative to reactions occurring in the effect of surface sites and adsorption states on binding and bulk heterogeneous solution? Are there environments and energetics. Other topics worthy of investigation include specific minerals which should be preferred targets of study? whether reactions can occur between NBs and mineral sur- For example, do clays, evaporitic minerals or minerals faces during specific adsorption, how complex multi-step associated with hydrothermal systems offer more favorable reaction mechanisms proceed, and how the nature of the environments for chemical evolution, or is this largely an intermediates in these and their transition states are affected irrelevant question given first-principles analysis of adsorption by adsorption. These goals result in an enormous combinatorial phenomena? Is there a generalizable effect of temperature on space of organic molecule-mineral, organic molecule-solvent, adsorption or catalysis? If so, what types of compounds or solvent-mineral and other environmentally-determined condi-

Published on 28 June 2012. Downloaded by University of Wisconsin - Madison 21/08/2017 21:11:05. reactions would low or high temperature environments favor tions which deserve study. Classical experimental methods of or disfavor? Can enough inference be drawn from the experi- studying adsorption make this a daunting challenge and the mental studies which have thus far been conducted to allow development of high throughput methods could undoubtedly for useful computational predictions to be made? How can have a significant impact on the field. these inferences be improved? In spite of these unresolved questions, some general conclu- Acknowledgements sions that may be drawn are that some mineral surfaces can indeed be strong and specific adsorbants for a variety of HC, JL and AM were supported in part by the National organic compounds, and could enhance preservation or Science Foundation (NSF) and NASA Astrobiology Program, degradation depending on numerous factors such as environ- under the NSF Center for Chemical Evolution, CHE-1004570. mental conditions (pH, water activity, temperature, the presence HC also acknowledges support from the NASA Astrobiology of light or ionizing radiation, etc.). For small molecules, Institute – Director’s Discretionary Fund (NAI-DDF). NS adsorption could lead to productive collisions between acknowledges support from NSF EAR CAREER award molecules in fairly concentrated solutions, which implies the (EAR 0346889), American Chemical Society Petroleum primacy of some environments, such as sea-floor sediments, Research Fund (41777-AC2), NAI-DDF, a Wisconsin Alumni evaporitic lakes or tidal pools, over others. This would depend Research Foundation (WARF) award from the University on the activation energy barriers for these reactions and thus, of Wisconsin, and start-up funds from the University of the temperatures at which they occur, the degree to which Akron. RH acknowledges support from the NSF, NAI, the mineral surface catalysis can alter these energy barriers and Alfred P. Sloan Foundation, and the Deep carbon Observatory. the degree to which water interferes with or facilitates these The use of trade, product, or firm names in this report is for reactions. descriptive purposes only and does not imply endorsement by The results of theoretical studies lead to a number of inter- the U.S. Government. The tests described and the resulting esting conclusions regarding the interactions of NBs with water, data presented herein, unless otherwise noted, were obtained

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