Geochemical Influences
on Life’s Origins and
Evolution
Joseph V. Smith 1
T
he early Earth was hot and chaotic, bombarded intensely from 4.5 to
3.8 billion years ago. In ponds near the flanks of volcanoes, feldspars
and zeolites from volcanic flows and ash were alternately washed by
fluids and dried, fostering adsorption and catalytic processes. Some silica-rich
surfaces favored adsorption of organic molecules, including amino acids,
which were produced by lightning in volcanic clouds. Catalysis then promoted polymerization to generate more complex molecules. Dissolution of alkali
feldspars created a honeycomb of cavities, which may have acted as temporary cell walls, while phosphorus released from the weathering feldspar
framework was available for energy molecules. Following the emergence
of the first cells, geochemical processes continued to influence biological
evolution. Alkali-rich volcanoes introduced metallic elements, which served
as nutrients in the food supply and may also have accelerated the rate of
primate evolution prior to the appearance of hominids.
istry, therefore, represent plausible
scenarios for life’s emergence, not
a definitive history.
Extended Darwinian natural selection driven by competition
between evolving species, coupled
KEYWORDS: biochemical evolution, feldspars, mineral surfaces, primate evolution, with Mendel-Watson-Crick genetic
volcanoes, zeolites, adsorption, mineral catalysis inheritance/mutation, is a plausible basis for integrating the patchy
paleontological record with the
INTRODUCTION
increasingly complex biochemical zoo of the present Earth.
Geochemistry has exerted a profound influence not only However, understanding the chemical beginnings of life
on the origin of life, but also on its subsequent evolution- poses major challenges. How could the first self-replicating
ary development. In this essay I look at the geochemistry of and energy-supplying molecules have been assembled from
the Earth, particularly its volcanic processes, in relation to simpler materials that were undoubtedly available on the
life’s origins and subsequent Darwinian evolution. I first early protocontinents? Most scientists abhor spontaneous
examine the conditions on the chaotic early Earth, when generation, much less the wave of a magic wand from God
catalytic mineral surfaces promoted the polymerization of or the inheritance of living organisms from outer space.
organic molecules. I then consider the role of volcanism in They search for an integrated geological/biochemical basis
relation to nutrition, and end with a consideration of the that allows biological evolution to begin on Earth using scientific features testable in a chemical laboratory, and perevolution of primates in the East African Rift Valley.
haps even observable in geologic specimens.
Biological life began with the assembly of biochemical molecules at catalytically active mineral surfaces (Smith 1998; The chemical steps that led to life on Earth remain a matParsons et al. 1998; Smith et al. 1999) on a chaotic early ter of intense speculation. Plausible ideas can be tested by
Earth (Smith 1982; Nisbet and Sleep 2001). Life advanced experiments that mimic prebiotic processes, but few geowith the growing complexity of biomolecules in single- logical observations are available to support one hypothesis
celled Archaea and Bacteria, as well as a multitude of later versus another. Most surviving Archean rocks have been
multicellular species (Schopf 1983; Kutschera and Niklas metamorphosed to at least 500 K, which wipes out most
2004), finally reaching the amazingly complex biochem- biochemical evidence. Nevertheless, mineralogical and geoistry of humans and other Eukaryotes. Paleontologists have chemical observations set in the context of industrial
arranged the surviving fragments of bones, shells, and chemistry, cosmochemistry, and astrophysics provide ideas
other fossil materials into a plausible progression of species worth pursuing.
(Stanley 1998). However, the potential biochemical evidence on biological evolution throughout Earth history has
been severely degraded or erased, especially for the most
ancient fossils. These ideas from mineralogy and geochem1 Department of Geophysical Sciences and Center for Advanced
Radiation Sources, 5734 S. Ellis Ave, The University of Chicago,
Chicago, Illinois 60637-1434, USA
E-mail: [email protected]
ELEMENTS, VOL. 1,
PP
151–156
MINERAL CATALYSTS
Bernal (1949) suggested that life began by catalytic assembly on a mineral surface, but early attempts to formulate an
integrated scheme of physicochemical processes had a significant weakness. Concepts of catalysis that use organic
compounds originally dispersed in aqueous organic “soup”
require a mechanism for concentrating the organic species
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next to each other on a catalytic substrate. After catalysis,
the biochemically significant polymers such as polypeptides and RNA must then be protected from photochemical
destruction by solar radiation, as well as from excess heating. Only then could the energy-consuming replication/
mutation of polymers yield the first primitive organisms.
Mineral surfaces, which today are important in numerous
biological systems from lichens and bacteria to bones and
teeth, might have filled the critical roles of selection, protection, and catalysis.
Certain materials have internal surfaces that are both
organophilic and catalytic. This characteristic enables efficient capture of organic species for catalytic assembly into
polymers in a protective environment. These physicochemical surface features are at the forefront of research on
synthetic zeolite catalysts in the chemical industry, as well
as on naturally occurring zeolite and feldspar minerals. We
conclude that catalysis at mineral surfaces could generate
replicating biopolymers from simple chemicals supplied by
meteorites, volcanic gases, and photochemical gas reactions.
Zeolites
Many early ideas about the role of minerals in life’s origins,
for example hypotheses that exploit quartz surfaces, are
implausible in detail because the proposed mineral surfaces
strongly prefer water and other ionic species to organic
molecules. However, the synthetic molecular sieve silica silicalite (synthesized by Union Carbide = Al-free Mobil ZSM5 synthetic zeolite) has a 3D channel system (FIG. 1) whose
electrically neutral Si–O surface strongly adsorbs organic
species in preference to water. In silicalite, all silicon atoms
are surrounded by a tetrahedron of four oxygen atoms, and
the stereogeometry is such that the channels are lined by a
three-connected net with the fourth Si–O bond pointing
into the silica. Hence, no silanol (Si–OH) species project
into the channels. Silicalite can adsorb molecules up to 6 Å
across, including benzene, and it has a remarkable
organophilic/hydrophobic nature. Consequently, traces of
methanol, propanol, butanol, pentane, hexane, and other
organic species can be removed from water. Silicalite possesses an exceptional stability for a 33% porous crystal. Not
only is it impervious to most mineral acids, it is also stable
in air to over 1100°C and only slowly converts to an amorphous glass at 1300°C.
The reason for the organophilic/hydrophobic nature is quite
simple. Oil and water do not mix because polar water molecules prefer ionic bonding, whereas organic molecules of the
oil prefer van der Waals bonding. Hence, for a truly neutral
surface, water molecules remain bonded to each other in an
ionic environment, allowing the organic molecules to adsorb
onto the neutral zeolite surface by van der Waals bonding.
Any material with a truly neutral silica surface with no projecting silanols (Si–OH) should be organophilic/hydrophobic.
Quartz and various other silica polymorphs have outward
bonds that become silanols in an aqueous system; hence they
are not organophilic like silicalite.
The ZSM-5-type zeolite, mutinaite, occurs in Antarctica
with boggsite and tschernichite (Al-analog of Mobil synthetic Beta) as the product of low-temperature alteration of
volcanic glass. Archean mutinaite might have become dealuminated towards silicalite during hot/cold/wet/dry
cycles driven by lunar tides and solar night/day. Catalytic
activity of silicalite increases linearly with Al–OH substitution for Si, and Al atoms tend not to occur in adjacent tetrahedral positions. Adjacent organophilic and catalytic
Al–OH regions in nanometer channels might have scavenged organic species, which were then catalytically assembled into specific polymers that were thus protected from
rapid photochemical destruction by sunlight. Polymer
migration along the weathered silicic surfaces, for example
of micrometer-wide channels of feldspar perthites, might
thus have led to assembly of replicating-catalytic biomolecules and perhaps even primitive cellular organisms (Smith
et al. 1999).
Silica-rich, feldspar-bearing volcanic ash would have
occurred on the early Earth, ready for weathering into a
fine-grained mixture of zeolites and feldspars as in present
continental basins. Abundant chert from weakly metamorphosed Archean rocks might retain microscopic clues to
these proposed mineral catalysts, and it is worth detailed
study. Other framework silica minerals are possible, including ones with left- and right-handed channels that might
have induced the assembly of chiral polymers.
A Scenario for Biocatalysis
Part of the atomic framework of silicalite/mutinaite (after
Smith et al. 1999). Four glycine molecules in the zwitterion configuration encapsulated in 10-ring channels. Oxygen atoms are
red spheres, while T atoms are shown by yellow (Si) and pink (Al)
spheres. The glycine consists of a central carbon atom (grey) bonded to
two hydrogen atoms (white), one carboxyl COO group, and one amine
NH3 group. Three glycine molecules are in one 10-ring channel optimized to interact with each other by hydrogen bonding and by suspension from the oxygen atoms by van der Waals bonding. The fourth
glycine molecule is in an adjacent channel.
FIGURE 1
ELEMENTS
The present proposal does not provide detailed recipes for
catalytic formation of a replicating polymer, but plausible
recipes should emerge from laboratory experiments and
crystal-chemical modeling. It would be wonderful, of
course, if catalytic polypeptide or RNA chains were synthesized in actual experiments on these proposed organophilic
materials. It would be even more thrilling if a fragment of
the abundant chert or other sediments in surviving
Archean terranes had survived metamorphism to preserve
some convincing evidence of primary biocatalysis.
In nature, one can imagine volcanic ash falling around
ponds near a volcano (FIG. 2). Electrical storms generated
simple organic molecules, including amino acids, by the
Miller reaction (Miller and Urey 1959). Despite criticisms of
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A simple schematic diagram showing a pond at the base
of a volcano in the early Earth. Ash (with Miller-reaction
amino acids from electrical storms) and lava flows are erupting at the
top. A complex water-rich soup repeatedly fills the pond in response to
lunar tides.
FIGURE 2
the reduced methane–hydrogen–ammonia atmospheric
conditions employed in these experiments, oxygen isotope
data are consistent with the interior of the early Earth having an enstatite-chondrite composition. This result is important because the resulting volcanic gases should have contained reduced molecules containing carbon and nitrogen
—just what is required for production of simple amino acids
from electrical processes in the volcanic clouds. In tidal
ponds, the resulting aqueous solution of organic species was
repeatedly refreshed and evaporated by tidal action.
Volcanic ash, weathered into organophilic feldspars and
zeolites, adsorbed simple organic molecules ready for catalysis. In FIG.1, for example, amino acids are shown lined up
in a 10-ring channel of silicalite. As tides receded, zeolite
complexes became dried and heated, and polymerization
occurred. Indeed, it would be fascinating to construct an
experiment to simulate this process. If simple organic molecules are observed to polymerize into complex ones, then
this key step toward primitive life becomes more plausible.
The energy-rich biomolecules ADP and ATP require phosphorus, which is also available from the weathering of volcanic feldspar that typically contains a few tenths of a percent P (coupled with Al as a substitute for 2 Si). As the Al
atoms leave the feldspar, the P would also be released as
PO3OH, which would be available for catalytic binding to
organic molecules.
Feldspars may have played other life-giving roles, in addition to their contribution of nutrients. In some slowly
cooled rocks, feldspars develop perthitic intergrowths of
Na-rich and K-rich feldspars, which might provide a safe
home for complex organic molecules after preferential dissolution of one of the feldspars. These textures have been
beautifully photographed by Martin Lee and Ian Parsons in
the Shap granite (FIG. 3), in which bacteria occupy weathered cavities in alkali feldspar. On the early Earth, one can
imagine complex molecules concentrated in such a cavity,
with the silicate walls acting as the first protective cell wall.
Ultimately, a self-replicating cluster of molecules in such a
ELEMENTS
cavity might develop its own protective membrane
(Deamer 1997) and float off into the pond water as the first
living cell.
VOLCANOES, FOOD SUPPLY,
AND DARWINIAN EVOLUTION
The role of geochemistry in life’s development did not end
with the emergence of the first cells. Geochemical processes
have continued to influence the evolution of life throughout Earth’s history. In particular, all species need food, and
this nutritional requirement is intimately tied to mineralogy
and petrology.
At the beginning of Darwinian evolution, approximately
four billion years ago, life depended on solar radiation or
geochemical sources for energy, while volcanoes supplied
much of the carbon, sulfur, phosphorus, and other elements essential to life. As the Earth’s crust slowly became
more oxidized through hydrogen escape, the composition
of volcanic rocks gradually changed. Early volcanoes tended to emit lavas rich in magnesium silicate and low in the
biochemical elements, whereas volcanic rocks today range
from common alkali-poor continental basalts to less common alkali-rich basalts and a wide range of carbonatites.
Volcanoes, Nutrition, and Biodiversity
From an evolutionary perspective, the greater the availability and variety of food, the greater are the chances of
Darwinian evolution into a cluster of species occupying
adjacent niches and specializing in their use of food. Food
supply and solar energy generally decrease from equator to
pole—a feature that explains the extreme biodiversity of
equatorial rain forests compared to arctic regions, for example, though local details depend on weather systems and
topography. Glacier-capped volcanic mountains next to a
hot rain-forest coast, as in East Africa (FIG. 4), offer the
greatest range of food supply and consequently the widest
variety of niches. As the weather changes, food supply
varies, and as climate changes, certain species may have difficulty surviving or may evolve into successor species, while
others expand.
Continental food supply depends ultimately on volcanoes
rejuvenating soils. Lava flows and ash deposits may wipe
out food supply initially, but weathering produces new soil
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and regenerates old soils, and also modifies the chemistry
of lake and stream water. Special types of alkaline volcanic
rocks, found in East Africa for example, carry abundant biochemically significant elements (i.e., minerals to dieticians)
in widely variable amounts. Key volcanogenic resources
include phosphorus and transition metals, which are
required for the metabolic functions of many multicellular
organisms, and for the brain chemistry of primates.
The influence of meteoritic impact is of special interest in
this regard. A large impact may initially decrease food supply and trigger extinction of certain groups of species.
Production of a large crater, however, results in gravitational readjustment of the mantle. This may trigger significant volcanic eruptions of rare, low-temperature basaltic
and carbonatitic melts enriched in biochemical elements,
followed by eruption of abundant higher-temperature
basalts that flood parts of continents. Is it possible that
such impacts ultimately foster biodiversity by creating geochemical variety and thus new niches?
Volcanoes and the Rate
of Primate Mutation
Because of this intriguing possible connection between volcanic rocks and the food supply, I conclude this article by
speculating on relationships between inorganic trace elements of geochemical significance (Fraústo da Silva and
Williams 1991) and organic biochemistry and nutrition
(Underwood 1977; Brody 1994; Williams 1997). My ideas
have been influenced by many emerging lines of investigation, notably the varied roles of Fe, Zn, Mn and other metals in biological processes, such as metabolism and gene
regulation, as well as in medicine (Cooper and Krawczak
1993; Cooper 1999; Roussel et al. 1999; Bertini et al. 2000;
Huffman and O’Halloran 2001). I propose that these considerations point to a previously unrecognized connection
between geochemistry and the evolution of large-brained
hominids, including Australopithicus and Homo (Bromage
and Schrenk 1999).
Consider the following three points:
➀ The active brain of modern humans uses more energy
per volume unit than does muscle, as reflected in its
two-fold higher content of energy-rich ATP and other
phosphorus-based molecules. Because the P-rich molecules in the brain normally use glucose supplied continuously from the rest of the body by the blood stream, a
daily food supply is highly desirable. Consequently, as
primate brains got larger, the food supply had to
become richer in phosphorus.
➁ The brain is characterized by relatively abundant transition metals, including Mn, Ni, and Cu, which form key
components of metalloproteins with various duties.
➂ The complex communication system in the brain
requires abundant Na and K together with Ca for the
nerves and membranes.
Thus, assuming some overall similarities in the functional
needs of both the human and the evolving Australopithecus
brain, high and constant intake of Na, P, Mn, Ni, and Cu,
as well as Fe and Zn, from foods derived from soils rejuvenated in the volcanic environment would have been beneficial for Australopithecus brain development. All these elements are abundant in the alkaline basalt/carbonatite
volcanic rocks of East Africa. I conclude from these observations that the distinctive geochemical features of the East
African Rift system were conducive to the emergence of the
advanced primate brain.
Trace-element nutrition was a necessary, but perhaps not
sufficient, step in the emergence of large-brained primates.
ELEMENTS
Scanning electron micrographs of weathered feldspar
from the Shap granite (Smith et al. 1999, Fig. 3). Top:
resin cast of honeycomb texture; Bottom: weathered feldspar surface
showing honeycomb and bacterium. Photos Martin Lee.
FIGURE 3
Therefore, I suggest that consideration be given to a possible link between volcano-driven food supply and an accelerated rate of gene mutations. This idea is speculative, but
some of the trace elements essential to primate brain function are also known to be mutagenic. For example, Mg is
known to stabilize the bending of DNA into particular
curved structures, but when Mn or other divalent cations
are substituted for Mg, the error rate of nucleotide incorporation increases (Bertini et al. 2000). Perhaps an increase in
environmental transition metals provided the necessary
chemicals for increased brain function, while simultaneously increasing the rate of mutations, some of which led
to a fortuitous further increase in brain function. Relating
gene mutation to biochemistry, geochemistry, and volcanology is a scientific study in its infancy, and my broad
suggestions may well turn out to be wrong. Nevertheless,
there may be a way to test at least some of these ideas.
A Test: Trace Elements
in Teeth Enamel and Bone Fragments
Trace elements preserved in fossil teeth and bones may provide a way to test my ideas about the importance of transition metals in the food supply of East African mammals.
The part of a primate body most resistant to chemical
degradation is the enamel of teeth, consisting of ~97%
apatite crystals and only ~2% organic matrix; bone, by contrast, has ~70% apatite and other phosphate material and
~20% protein. During fossilization and diagenesis, chemical exchange would have occurred with the soil at burial
sites in East Africa, and apatite crystals may have undergone ion exchange that altered the original chemistry, even
in the case of tooth enamel. However, advanced synchrotron X-ray techniques (Smith and Rivers 1995) offer some
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FIGURE 4
View of the Oldoinyo Lengai carbonatite eruption of
August 1996, East Africa. By permission of J. B. Dawson.
hope that a tomographic X-ray fluorescence/diffraction
study with one-micrometer spatial resolution could test the
crystalline integrity and yield the trace-element content for
at least the most retentive elements of surviving parts of the
enamel. Indeed, preliminary examination (unpublished, SR
Sutton and JVS) reveals that a dozen trace elements are
detectable above the part-per-million level. A non destructive-synchrotron XRF reconnaissance of mammal teeth
studied by other techniques is therefore desirable.
CONCLUSIONS
The importance of mineralogy and geochemistry for
Darwinian evolution has changed greatly over geologic
time. Four billion years ago, only the most primitive molecular assemblages could have occurred, triggered by catalytic reactions at organophilic mineral surfaces. Eventually, by
processes as yet poorly understood, a self-replicating biochemical system emerged from the geochemical milieu.
The resulting first living cells marked the transition from a
geochemical to a biochemical world.
The first cells were subjected to new competitive stresses
and thus underwent Darwinian evolution. Complex variations in food supply and environmental conditions, possibly including changes related to bolide impact and subsequent volcanism, allowed this evolution to proceed in fits
and starts.
In this long evolutionary history of life, the development of
large-brained primates remains of special interest. About 30
million years ago, the East African Rift opened up at the
north, releasing magmas especially rich in biochemically
important elements from the mantle. Volcanic mountains
grew larger, ultimately generating a rich mosaic of local
conditions. Whether there were bursts of genetic evolution
as a result of the enhanced food supply linked to this
unusual volcanic activity is not testable with present data.
ELEMENTS
On a global basis, other parts of the tropical zone have a
similar year-round warm climate essential for primitive primates, but only in the volcanic zone of East Africa was
there the combination of an evolving large-brain primate
population and an abundant supply of biochemical nutrients from active volcanism. The rest of the tropical world,
including the East Indies, South America, and West Africa,
lack this crucial combination.
Caution is a virtue for scientists thinking about evolutionary processes. I hope to see detailed testing, reworking,
extension, and correction of my ideas. For example, a
model catalytic reactor could be assembled cheaply to
mimic the conditions proposed for early ponds near the
flanks of volcanic mountains. Jumping ahead several billion years, the great challenge of deciphering human evolution—why the Australopithene/Homo lineage split from
that of the African great apes ~6 M years ago—may also rest
in the geochemistry of volcanism. Was this event related to
the coincidence of a global climatic catastrophe (Stanley
1996) and increased volcanism (and, consequently, higher
food supply) during the opening of the northern part of the
East African Rift? Perhaps alkaline basalt/carbonatite volcanism began to have a major effect on food supply and
gene expression as the climate changed. Was there a burst
of volcanism associated with each subsequent major evolutionary event in the Homo lineage? If so, then systematic
dating of piles of volcanic ash using K-Ar techniques on
surviving feldspar macrocrysts might shed light not only
on Earth’s geochemical cycles but also on key events in
human evolution.
ACKNOWLEDGEMENTS
I thank Ian Parsons for feldspar photos and Barry Dawson
for collaboration on East African geology, including supply
of photographs. I also thank Robert Hazen and the editors
of Elements for their advice. .
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REFERENCES
Bernal JD (1949) The physical basis of life.
Proceedings of the Royal Society of London
357A: 537-558
Bertini I, Sigel A, Sigel H (2000) Manganese
and its Role in Biological Processes. Marcel
Dekker, New York, 432 pp
Brody T (1994) Nutritional Biochemistry.
Academic Press, London, 658 pp
Bromage T, Schrenk F (1999) African
Biogeography, Climate Change, and
Human Evolution. Oxford University Press,
New York, 485 pp
Cooper DN (1999) Human Gene Evolution.
BIOS/Academic, San Diego, 490 pp
Cooper DN, Krawczak M (1993) Human
Gene Mutation. BIOS/Academic, San
Diego, 402 pp
Deamer DW (1997) The first living
systems: a bioenergetic perspective.
Microbiology and Molecular Biology
Review 61: 239-261
Fraústo da Silva JJR, Williams RJP (1991)
The Biological Chemistry of Life.
Clarendon Press, Oxford
Huffman DL, O’Halloran TV (2001)
Function, structure, and mechanism of
intracellular copper trafficking proteins.
Annual Reviews of Biochemistry 70: 677701
Kutschera U, Niklas KJ (2004). The modern
theory of biological evolution: an expanded
synthesis. Naturwissenschaften 91: 255-276
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Miller SL, Urey HC (1959) Organic
compound synthesis on the primitive
earth. Science 130: 245-251
Nisbet E, Sleep NH (2001) The habitat and
nature of early life. Nature 409: 1083-1091
Parsons I, Lee MR, Smith JV (1998)
Biochemical evolution. II. Origin of life in
tubular microstructures on weathered
feldspar surfaces. Proceedings of the
National Academy of Sciences 98: 1517315176
Roussel AM, Anderson RA, Favier AE (1999)
Trace Elements in Man and Animals.
Kluwer Academic/Plenum, New York,
1172 pp
Schopf JW ed (1983) Earth’s Earliest
Biosphere. Its Origin and Evolution.
Princeton University Press, Princeton,
543 pp
Smith JV (1982) Heterogeneous growth of
meteorites and planets, especially the Earth
and Moon. Journal of Geology 90: 1-48
Smith JV (1998) Biochemical evolution: I.
Polymerization on internal, organophilic
silica surfaces of dealuminated zeolites and
feldspars. Proceedings of the National
Academy of Sciences 95: 3370-3375
Smith JV, Arnold FP Jr, Parsons I, Lee MR
(1999) Biochemical evolution. III.
Polymerization on organophilic silica-rich
surfaces, crystal-chemical modeling,
formation of first cells, and geological
clues. Proceedings of the National
Academy of Sciences 96: 3479-3485
156
Smith JV, Rivers ML (1995) Synchrotron xray microanalysis. In: Potts PJ, Bowles JFW,
Reed SJB, Cave MR (eds.) Microprobe
Techniques in the Earth Sciences,
Chapman and Hall, London, pp 163-233
Stanley SM (1998) Macro-evolution. Johns
Hopkins University Press, Baltimore,
382 pp
Underwood EJ (1977) Trace Elements in
Human and Animal Nutrition. Academic
Press, New York, 545 pp
Williams S (1997) Nutrition and Diet
Therapy, 8th ed. Mosby, New York, 850 pp
.
RESEARCH PAPER HONORED
A
paper entitled “Role of
Microbes in the smectite-toillite reaction” by J. Kim, H.
Dong, J. Seabaugh, S. Newell
and D. Eberl (Science, 2004, vol.
303, p. 380-382) was selected to
receive an award at the annual
Alan Berman Research Publications
Award Dinner held in March,
2005 by the Naval Research
Laboratory.
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