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Title: Defining Biominerals and Organominerals: Direct and Indirect Indicators of Life
Article Type: Research Paper
Section/Category:
Keywords: Biominerals, organominerals, science definitions, linguistics, science language, desert varnish,
hot-springs, silica sinter, terminology, stromatolites, micro-fossils bacterial encrustations, philosophy of
science, definitions
Corresponding Author: Dr Randall S. Perry, PhD
Corresponding Author's Institution: Imperial College, University of London
First Author: Randall S. Perry, PhD
Order of Authors: Randall S. Perry, PhD; Nicola MCLoughlin, PhD; Bridget Y. Lynne, PhD; Mark A. Sephton,
PhD; Joan D. Oliver, MA; Carole C. Perry, PhD; Kathleen Campbell, PhD; Michael H. Engel, PhD; Jack D.
Farmer, PhD; Martin D. Brasier, PhD
Manuscript Region of Origin:
Abstract: By introducing the new term 'organomineral' to apply to minerals that are affected by organics,
mostly life-related, but not directly produced by living cells, we hope to increase the accuracy of the
terminology in use at present. We believe that the term 'biomineral' does not describe all mineral deposits
precisely enough and offer case studies to support instances where the use of a new, specific term
'organomineral' is more appropriate. We provide examples of some materials that are biominerals e.g.,
diatoms and human bones. We then attempt to show that this terminology can sometimes mislead
investigators, drive the direction and prejudice interpretations of scientific investigation. This is achieved by
presenting case studies of minerals that have been investigated as biominerals although they may not
actually be directly controlled by biology. We pay special attention to desert varnish, hot-spring siliceous
deposits, stromatolites, and bacterial encrustations. A detailed understanding of how organic compounds
are preserved and transformed in the mineral matrix is highly relevant to the search for the oldest evidence
of life on Earth.
Manuscript
Click here to download Manuscript: 6-21-06- organomineral Final.doc
Defining Biominerals and Organominerals: Direct and Indirect
Indicators of Life
RANDALL S. PERRY, 1& 2* NICOLA MCLOUGHLIN, 1 BRIDGET Y. LYNNE, 3 MARK A.
SEPHTON, 4 JOAN D. OLIVER, 2 CAROLE C. PERRY, 5 KATHLEEN CAMPBELL, 3
MICHAEL H. ENGEL, 6 JACK D. FARMER, 7 MARTIN D. BRASIER, 1 JAMES T. STALEY8
1
Earth Sciences, Oxford University, Parks Road, Oxford, OX1 3PR, United Kingdom
2
Planetary Science Institute, 6920 Roosevelt Way NE 177, Seattle, WA 98115 USA
3
Department of Geology, University of Auckland, Private Bag 92019 Auckland, New Zealand
4
Impacts and Astromaterials Research Centre, Department of Earth Science and Engineering,
South Kensington Campus, Imperial College London SW7 2AZ UK
5
Chemistry Division, The Nottingham Trent University, Nottingham, NG11 8NS, United
Kingdom
6
School of Geology and Geophysics, University of Oklahoma, 100 East Boyd St, Norman, OK
73019-1009
7
Department of Geological Sciences, Arizona State University, Tempe, AZ 85287-1404
8
Department of Microbiology, School of Medicine, University of Washington, Seattle, WA
98195-1310
* currently Impacts and Astromaterials Research Centre, Imperial College, London,
[email protected], 44 (0)207 594 6425, [email protected], 1-206 543-6267
Key Words: Biominerals, organominerals, science definitions, linguistics, science language,
desert varnish, hot-springs, silica sinter, terminology, stromatolites, micro-fossils bacterial
encrustations, philosophy of science, definitions
Running Title: Organominerals as indicators of life
ABSTRACT
By introducing the new term ‘organomineral’ to apply to minerals that are affected by
organics, mostly life-related, but not directly produced by living cells, we hope to increase the
accuracy of the terminology in use at present. We believe that the term ‘biomineral’ does not
describe all mineral deposits precisely enough and offer case studies to support instances where
the use of a new, specific term ‘organomineral’ is more appropriate. We provide examples of
some materials that are biominerals e.g., diatoms and human bones. We then attempt to show that
this terminology can sometimes mislead investigators, drive the direction and prejudice
interpretations of scientific investigation. This is achieved by presenting case studies of minerals
that have been investigated as biominerals although they may not actually be directly controlled
by biology. We pay special attention to desert varnish, hot-spring siliceous deposits,
stromatolites, and bacterial encrustations. A detailed understanding of how organic compounds
are preserved and transformed in the mineral matrix is highly relevant to the search for the oldest
evidence of life on Earth.
INTRODUCTION
We propose the term ‘organomineral’ for mineral products formed by the interaction of
organic and inorganic substances, for example in desert varnish. These are minerals that may be
indirectly formed or induced by biological activity e.g. the byproducts of some living bacteria
alter local Eh-pH conditions and induce encrustation. The complexation of inorganic materials
while in the presence of the byproducts of dead organisms, or abiogenic organic reactions such as
in meteorites, can affect chemical reactions that promote the formation of specific minerals. The
extension of the term ‘organomineral’ to geobiology provides a more precise definition of these
minerals and a way of distinguishing them from biominerals. Biomineralization is the uptake of
elements and their incorporation into mineral structures under direct biological control. It is the
method by which most higher organisms form exo- or endoskeletons, directly precipitating
minerals (e.g., silica, calcite, or hydroxyapatite). Precise terminology is efficacious both in
indicating the equivocal nature of new information and possibly shaping the development and
direction of future research. We present case studies of investigations that may have been
misdirected previously because of terminology. Examples include our latest research into hotspring siliceous deposits, desert varnish, endolithic trace fossils, stromatolites, and bacterial
encrustations. The distinction between minerals incorporated into functional structures directly
by organisms (biominerals) and minerals complexed with organopolymers, and bio(organic)
and/or organic compounds (organominerals), will aid us when ascertaining the presence of past
life, considering the veracity of Archaean fossils on Earth or evaluating whether evidence of life
is preserved in meteorites or on other Planets. Successful interpretations of such issues may rely
on our ability to identify minerals that are indicators of life.
Importance of definitions
In this article we are not only proposing the new use of the term ‘organomineral’ but also
reaffirming the necessity and importance of exact terminology and how it shapes our approaches
to problem solving. Terminology defines the object of study and places it within a taxon and its
precision is therefore paramount. However, with use, connotations attach themselves to the term
until the term shapes our response to what it denotes e.g., wetness and liquidity become part of
our response to the word ‘water’. The challenge lies in achieving the necessary precision in
definition while also evoking the response we wish others to have towards our subject. This is a
cultural problem and the study of the complex science of Terminology has become a discipline in
itself. Science is not a hermetically sealed discipline and is affected by changes in language.
Several scientists (Cleland and Chyba, 2002; Fosnot and Perry, 2005; Hedgecoe, 2003; Kuhn,
1996; Levit and Krumbein, 2003) have addressed this problem in relation to the use of
terminology in their own fields.
A useful scientific definition should facilitate achievable experiments, which, in the context of
this work, are those that look for evidence of life (Nealson and Conrad, 1999; Perry and Kolb,
2004 e). Currently there is no broadly accepted definition of ‘life’ (Cleland and Chyba, 2002) to
aid astrobiologists, so the detection of life in our universe is left as a remarkably ambiguous and
poorly defined objective (Oliver and Perry, in press). Scientific definitions inevitably evolve with
greater knowledge and ‘life’ now has specific definitions from the fields of biology,
mathematics, chemistry, microbiology, artificial life etc. However these do not, on the whole,
change the things to which we apply the term ‘life’. For instance, entities such as crystals, fire,
and computer systems displaying artificial intelligence have all been considered as examples of
life but currently these remain open to debate. Both Cleland and Chyba (2002) and
Uttamchandani (2001) use water as an example of how definitions and the names of substances
can change with developments in science. Kripke in his work “Naming and Necessity” argues
that names are rigid designators which are universal across space and time and so for example,
water in the year 1750 is still the liquid substance that we know today (Kripke, 1999). However,
proponents of a Kuhnian model of science (Kuhn, 1996) would counter this by saying that ice
and steam were not considered water in 1750 because their molecular make-up was unknown,
but that today water, ice and steam can all be defined by the chemical formula H2O
(Uttamchandani, 2001). In this way, Kuhn would argue that the meaning of a name or term can
change as new paradigms are adopted. It follows therefore that our understanding of the term
‘life’ will also evolve and possibly encompass more entities as our scientific knowledge increases
(Oliver and Perry in press).
In this study, when deciding whether something is a biomineral or an organomineral, we
are attempting to attach to the mineral substance a name that defines it as belonging to a certain
family with very precise characteristics. All this may seem self-evident and certainly in science,
naming does not seem to have the life and death importance that it acquires in other contexts, for
example, in Shakespeare’s ‘Romeo and Juliet’ where the tragedy ensues from the fact that the
lovers belong to different families with different names. But if the terminology is not absolutely
precise we run the risk of assuming or denying important properties, prejudices which may lead
investigators astray.
What are biominerals or how are they defined?
Biominerals are the products of the selective uptake of elements from the local
environment and their incorporation into functional structures under strict biological control
(Mann, 2001). Skinner and Jahren (2003) give the following definition: “Biomineralization is the
process by which living forms influence the precipitation of mineral materials.”
Biomineralization is a highly regulated process that produces, for example, the biominerals
bones, teeth, shell, and the intricate fabrics of diatoms (Fig. 1) and radiolarians (Lowenstam and
Weiner, 1989). Calcium carbonate, calcium phosphate, magnetite, and silica (Perry and KeelingTucker, 1998) are all important constituents in the formation biominerals (Table 1).
Proposed new definition of ‘organomineral’
We propose the use of the term ‘organominerals’ for any minerals precipitated under the
influence of organic or (bio)organic matter. Organic compounds and the remains of living
entities can have a variety of effects on the formation of minerals. In some cases they strongly
affect the chemical process of precipitation (e.g. Eh and pH) while in others they are simply
passively entombed or complexed in forming minerals.
Organominerals as natural products
Familiar examples of organominerals would be those formed from the by-products of
biological organic molecules that interact with inorganic compounds to form mineral precipitates
(Table 2). These abound on modern Earth, are synonymous with the fossil record and are
exciting tracers for life beyond Earth. Perhaps less obvious organominerals are those produced
by the interaction of non-biological organic matter with inorganic minerals (Table 2). These are
abundant in carbon-rich meteorites where organic compounds are found alongside water and
minerals. More recently it has also been appreciated that there are abiological processes, such as
the Fischer-Tropsch synthesis, that can generate simple chain organic compounds on modern
Earth (Sherwood et al., 2002) and that these may be the source for organic matter preserved in
ancient carbonaceous cherts (Brasier et al., 2004; Ferris, 1992). It should be noted, however, that
the Fischer-Tropsch synthesis is unlikely to have generated meteoritic organic matter (Sephton et
al., 2001). Hence, our definition of organominerals encompasses both those minerals formed by
the remains of terrestrial biota and by abiogenic organic matter. Distinguishing between these
two types of organominerals represents a fascinating future direction for research.
While there are many biominerals (selected biominerals Table 1), there is a plethora of
potential organominerals identified on Earth. Commonly, organominerals, as we propose here,
are formed by interaction with organopolymers, bio(organic), and/or non biological organic
compounds without direct evidence of skeletal, intracellular or extracellular formation. Organic
chemicals can have important chemical effects on polymerization and condensation processes
when organominerals are formed. Organominerals could be of special interest to microbiologists,
paleontologists, and astrobiologists when life’s chemical past-history is recorded in the mineral
matrix. Because organominerals by our definition are often associated with microbial systems,
they are important targets for scientists searching for life on other planets in our solar system.
Importantly, organominerals have a much greater preservation potential than their organic
initiators, providing opportunities for gleaning paleobiological information from more ancient
and metamorphosed samples from the rock record.
EXAMPLES OF BIOMINERALS
The following are examples of the direct involvement of mineral formation by biology.
There are many other clear and interesting examples of biomineralization (Table 1) ranging from
the silica needles in nettles that inject toxins, to the love darts of gastropods composed of
aragonite (Mann, 2001). Silica and several calcium minerals dominate much of the hard parts we
see in shells, reefs, bones, and chalk and diatomaceous mineral deposits. Iron minerals add
strength to the teeth of limpets, chitons and to the tooth surface of beavers. Magnetite in tuna and
salmon allows magnetic navigation (Mann, 2001) as it does in magnetotactic bacteria.
Bones, teeth, and shells - calcium systems
Bones and shells are obvious examples of biominerals. They are calcium systems formed
under direct biological control. Bones and teeth (Fig. 1) are made from calcium phosphate in the
form of the mineral hydroxyapatite, which for all practical purposes can be denoted by the
formula Ca10(PO4)6(OH)2. Other phases of calcium phosphate may also be present, Ca8H2(PO4)6
in the bones and teeth of vertebrates and amorphous forms in for example, chitons, gastropods,
bivalves, and the milk of mammals. More than any other mineral, bone highlights the differences
between a ‘biomineral’ and an ‘organomineral’. Bones undergo continuous growth and
dissolution in response to internal biological signals. The mechanical properties of bone are
derived from hydroxyapatite with a matrix of proteins including for example, sugar side chains
(glycoproteins). Teeth, like bone, derive from a complex system of hydroxyapatite but contain
~65% versus ~95% in bone. Tooth enamel starts out with a high proportion of proteins, which
are gradually replaced by minerals as the tooth matures. Most shells are composed of calcium
carbonate or aragonite (Fig. 1) with the formula CaCO3. Usually the outer shells are composed
of crystals of calcium carbonate while the inner portions (nacre) are composed of aragonite
(Mann, 2001). The connection between calcium and its binding proteins and overall genetic
regulation is probably through protein phosphorylation and dephosphorylation and through cyclic
nucleotides (Frausto da Silva and Williams, 2001).
Diatoms and radiolarians - silica systems
Diatoms and radiolarians produce delicate, porous micro-skeletons. Amorphous silica
minerals (Mann and Perry, 1986; Mann et al., 1983; Perry et al., 2003a; Perry and KeelingTucker, 1998) may be better suited to forming molded structures than calcium minerals, because
crystal lattice planes might interfere with the manufacture of fine-scale, lace-like structures (Fig.
1). Morphogenesis of diatom frustules occurs when areolar vesicles are secreted, attached to cell
walls and provide the mold for silica.
Magnetite minerals
One of the best microbial examples of a biomineral (Fig. 1) is bacterial magnetite
(Lowenstam and Weiner, 1989; Mann, 2001; Skinner and Jahren, 2003). This is formed in
special membranes in the cytoplasm of the bacterium. The shape of the magnetite and its
location in the single-celled bacterium in which it is produced, varies from one species to
another, indicating that the bacterium is able to control its formation. The bacterium simply
needs to be able to grow in the habitat in which the substrates for growth and mineral formation
are available.
Magnetite is also formed by means other than under the direct control of biology. The
magnetite thus formed, however, is crystallo-chemically heterogeneous and is not a biomineral.
Magnetite single crystals, which are biominerals formed directly by organisms, have cubooctohedran, hexagonal and other distinctive crystal morphologies. They involve controlled
mineralization by living organisms, have species-specific crystallo-chemical properties and
consequently fit the definition for a biomineral. It is of particularly wide interest to space
scientists and especially to astrobiologists to assess whether or not the magnetite found in a
Martian meteorite ALH84001 was processed by bacteria (McKay et al., 1996).
Bacterial Spores
Some bacteria produce spores, which concentrate metal ions (e.g., Ca2+ and Mn4+) and
become encrusted with them when nutrients or water become unavailable. For example, on rock
surfaces during the summer months, hot dry conditions cause sporulating bacteria to form spores
with protective mineral coats, which allow their survival until more hospitable conditions occur.
The mechanisms for survival of sporulating bacteria in harsh environments makes them excellent
candidates for astrobiological studies of planetary protection issues (Horneck and BaumstarkKhan, 2002). The formation of these spore coatings appears to be under the control of the
bacteria and the spore coats formed are most appropriately termed biominerals.
Germination of spores is caused by multiple factors including exposure to organic
compounds such as the amino acid alanine (Sogin et al., 1972). When bacteria become
reconstituted, the cellular products preserved within spores germinate into bacteria. The
indurated spore coats, which contain organic polymers and metals, then demineralize and are
added to the environment. Their byproducts may become organominerals. This process is
suggested as a possible mechanism for concentrated metals such as manganese and calcium on
rock surfaces in desert varnish (Perry and Kolb, 2003). Further experiments are needed for
falsification of this hypothesis. Spore coats uniquely contain dipicolinic acid, which has not yet
been found in the rock coating desert varnish (Perry, 2004).
ORGANOMINERAL CASE STUDIES
The term ‘organominerals’ has been used in the coal and oil industries, by chemists, and in
agriculture, but we are also extending its essential meaning to geobiology. We apply it to natural
minerals as well as those rock materials formed in association with biotic amino acids and other
abiotic organic molecules associated with meteorites. The case studies for the substances that we
term ‘organominerals’, are presented here in detail to better illustrate how the new use of the
term produces a more precise description of them.
Particularly interesting case studies are those of desert varnish, hot-spring silica sinter and
bacterial encrustations because, in the past, many hypotheses have suggested that they may be
biominerals. Consequently, we pay special attention to their investigations and the way in which
those investigations may have been driven by the terminology.
Desert varnish and silica glaze
Desert varnish is a black oxide, silicon and detritus-rich and, to a lesser extent, a (bio)organic
and trace element-rich, layered rock coating (Fig. 2, 6) that is widespread in arid and semi-arid
regions on Earth (Allen, 1978; Darwin, 1871; Dorn and Oberlander, 1982; Engel and Sharp,
1958; Perry, 1979; Perry, 2004; Perry and Adams, 1978). Initially, bacteria were implicated in its
formation when it was described as a product of bacterial biomineralization (Dorn and
Oberlander, 1981). Other investigators, assuming the microbial hypothesis to be correct, also
looked for manganese oxidizing bacteria (Jones, 1991; Krumbein and Altman, 1973; Krumbein
and Jens, 1981; Perry et al., 2004; Perry and Kolb, 2003; Perry et al., 2005b; Taylor-George et
al., 1983). Microcolonial fungi (MCF) (Fig. 3) were found on rocks (Gorbushina and Krumbein,
2000; Gorbushina et al., 1993; Gorbushina et al., 2003), and are uniquely associated with desert
varnish (Perry, 1979; Perry et al., 2004 f; Staley et al., 1983; Staley et al., 1982; Taylor-George et
al., 1983). Although the bacterial populations are sparse, they have, nevertheless, been cultured
from desert varnish rock coatings by us and others notably Hungate et al. (1987), but there have
been no viable or testable models from either bacteria or MCF, for a direct microbial contribution
to the production of mineralized deposits. It should be noted that microbes might be more
prevalent in other geographical locations and environments not investigated by us. If no direct
involvement of biology is required, the question arises as to whether desert varnish should be
considered a ‘biomineral’. The presence of life-related organics does have a measurable effect in
mineral formation, e.g., polymerization and condensation of silica (Iler, 1979), but when living
cells are not direct causative agents, the existing term may be misleading.
Silica glazes are also found on rock surfaces in Hawaii (Curtiss et al., 1985; Farr and
Adams, 1984), Peru (Jones, 1991), and Oregon (Farr, 1981). They resemble manganese-rich
desert varnish in their luster, hardness, thickness and growth patterns. These two coatings have
usually been studied as separate phenomena, however silicon as silica (opal-A and or-CT) is an
important component of both desert varnish and glazes (Perry and Lynne, 2006). Since this is the
case, we now suggest that they should be considered as part of the same ‘family’, and our
approach to them undergoes a shift of perspective. Superficially, desert varnish is easy to
consider as a biomineral, although not all investigators have perused varnishes as biominerals,
notably Potter and Rossman (1977), but silica glazes ‘intuitively’ do not fit this into this
category. The simple addition of the element manganese has caused investigators to wonder how
it is enhanced (Jones, 1991; Potter, 1979; Potter and Rossman, 1979a; Potter and Rossman,
1979b), to hypothesize that the cause is microbial, and consequently to design experiments as
though desert varnish is a biomineral (Perry et al., 2004; Perry et al., 2003b).
The mechanism for formation of both silica glaze and desert varnish has remained
enigmatic. During the last three decades most investigations have focused on a biological
mechanism of formation for desert varnish. However, inorganic chemistry has been extensively
studied. Since manganese is often (but not always) present in large quantities, the focus since
nineteenth century investigators first identified manganese (Darwin, 1871; Humboldt, 1852) has
frequently been on questioning its concentration in coatings that have the classic black varnished
appearance. However, the redox environment, in which varnish forms, provides a possible
explanation for an inorganic mechanism of manganese enhancement (Krauskopf, 1957). A
similar experiment to those of Krauskopf (1957) was performed by Jones (1991), which provides
a geochemical manganese enhancement mechanism. Recently Thiagarajan has proposed a model
for an aqueous atmospheric concentration of manganese that is supported by analysis of
depletions and enrichments of rare-earth elements (REE) Potter and Rossman (1977) using IR
spectroscopy, identified clays and the manganese and iron phases, concluding that coatings were
composed of up to 70% clays, and hardened by the cementing together of clays and oxides
(Potter and Rossman, 1977; Potter and Rossman, 1979a). Until now it has been widely accepted
that the large quantities of silicon in desert varnish are present as clay minerals and that clays
make up the majority of varnish minerals. Clays have predictable ratios of Si/Al depending on
type and in one investigation (Perry, 2004) minimal clays were identified. However, in all
investigations by us varnishes were found to contain mostly silicon oxides in variable ratios of
silicon to aluminum (Fig. 2), and in some cases (Fig. 2b) aluminum is below detection limits,
suggesting varnish coatings are primarily composed of silica rather than clays. It is of course
expected that varnishes will contain variable amounts of clays as detrital deposits or as
weathering products but we do not find them to be involved in the primary formation
mechanism. Dorn and Oberlander (1981) reported from laboratory experiments that a
Metallogenium-like manganese-oxidizing bacterium was probably responsible for concentrating
manganese and thus forming coatings. Others have failed to duplicate this work. Several
investigations have searched for both a microbial formation mechanism and the presence of
microbes themselves within and on varnished rock surfaces. (Adams et al., 1992; Krumbein and
Jens, 1981; Palmer et al., 1986; Raymond et al., 1992; Staley et al., 1992; Taylor-George et al.,
1983) One report by a NASA team identified at least one fossilized bacterium in a varnish
coating (Flood et al., 2003). But our investigations (Perry and Kolb, 2003; Perry et al., 2005b;
Perry et al., in press) and those of others (Jones, 1991; Taylor-George et al., 1983) have noted
that microbes are rarely visible on surfaces except for that of the MCF (Krumbein and Jens,
1981; Palmer et al., 1987; Palmer et al., 1990; Perry, 2004; Perry et al., 2003c; Perry et al., 2004
f; Staley et al., 1983; Staley et al., 1982; Taylor-George et al., 1983). MCF (Fig. 3) are found
worldwide and uniquely associated with varnished rock surfaces. Consequently several
investigations, including ours, have searched for explanations of the involvement of MCF in
varnish formation, but as stated above, have found none. It is interesting, however, that MCF
appear to degrade and become part of coatings (Fig. 3).
Notably, while searching for biochemical and molecular biological evidence we
reported finding a diverse group of biochemical and (bio)organic components in coatings
including amino acids (Perry et al., 2003b), DNA (Perry et al., 2004), and several polymorphic
organic compounds(Perry, 2004). The finding served to intensify the investigation of various
biological hypotheses e.g., that coatings might be caused by Mn-rich spores (Perry and Kolb,
2003) or decaying MCF (Perry et al., 2004 f) or amino acids found in the peptidoglycans of
Gram-positive bacteria (Perry et al., 2003b). While the biogenic (microbial) explanations seemed
more satisfying than their abiogenic (inorganic) counterparts, they failed to account for several
key features of varnish coatings and silica glazes i.e. they are hard like abiotic siliceous minerals
(Perry and Lynne, 2006; Perry et al., in press) and display unique botryoidal (Perry and Adams,
1978) and layered textures (Dorn, 1984; Perry and Adams, 1978).
Although these hypotheses were legitimate, testable and possible explanations for how
desert varnish forms, most were predicated on thinking of desert varnish as a biomineral. Silica
glazes were not seen as biominerals, no mechanism for their formation was put forth, and
importantly there seemed little or no connection between the two rock coatings. The term
biomineral was driving the thought process of desert varnish investigators toward biological
mechanisms, while the lack of a taxon for silica glazes produced no biogenic hypothesis.
The new paradigm for organomineral varnish formation is based on the suggestion of the
occurrence of silica and organic compounds in the varnish (Kuhlman et al., 2005; Kuhlman et al.,
2006; Perry, 2004; Perry et al., 2004; Perry and Kolb, 2003; Perry et al., in press; Schelble et al.,
2005). The simplified underlying model for varnish formation suggests that desert varnish and
silica glazes are closely related, as they are both silica-rich. Farr (1981) analyzed both Oregon
and Hawaiian glazes and found them primarily to contain silicon; other oxides are present as in
desert varnishes but in reduced quantities. A common mechanism is also suggested by the
finding in Oregon deserts of desert varnish and silica glazes in the same coating mineral matrix
Farr (1981). Adams (pers. comm., 2004) noted the presence of both silica glazes and desert
varnish in U.S. deserts, as did Jones (1991) in Peruvian deserts. Silica glazes may provide a
simplified model for more oxide-rich desert varnishes (Perry et al., 2005a; Perry and Lynne,
2006; Perry et al., in press).
Hot-spring siliceous sinter deposits
The question of biomineralization in siliceous sinter has also stirred debate. Do microbes
cause the silica to deposit, do they enhance its deposition, or do they have no impact on silica
deposition? In contrast to desert varnish (Fig. 2, 6), bacteria are plentiful in some sinter deposits
(Fig. 4) yet siliceous sinter, desert varnishes, and silica glazes maybe be cogeneric if silica is the
common substance (Perry and Lynne, 2006). Konhauser (2001) addressed this controversy and
more recent studies by Mountain et al. (2003) and Lynne et al. (2005) report deposition of silica
with or without microbial content. Currently researchers generally use the words ‘silica-microbe
interactions’ rather than biomineralization.
Thermal springs are common throughout geothermal regions of the world and siliceous
hot-spring deposits are particularly abundant wherever near neutral chloride waters discharge at
the surface after equilibrating with the underlying rocks at 175 ºC (Fournier and Rowe, 1966).
When waters cool to below 100 ºC, silica is often precipitated in the form of non-crystalline opalA (Lynne et al., in press). Thriving communities of microbes can occur, which are subjected to
rapid mineralization (Fig. 4) and have high preservation potential as molds and casts in the
geologic record (Cady and Farmer, 1996). Silica deposits on all biogenic and abiogenic surfaces
that come into contact with spring water, silicifying, entombing, and fossilizing various
materials, from microbes to pine cones to insects to rock surfaces. Previous studies have shown
that ancient subaerial, siliceous sinter deposits retain many of their primary macroscale textural
characteristics, such as in Drummond basin, Australia, (Walter et al., 1996) and Rhynie Chert,
Scotland (Rice et al., 1995; Trewin, 1994). Therefore, sinters can record many aspects of the
original paleohydrologic, paleobiologic and paleoenvironmental conditions. Hydrothermal
systems have been implicated as possible crucibles for the origin and evolution of early life
(Bock and Goode, 1996; Farmer, 2000; Farmer and Des Marais, 1999). They may also serve as
analogs for environmental conditions that prevailed on Earth or other planets billions of years
ago (Bock and Goode, 1996).
Over time sinters undergo a series of morphological and mineralogical changes (Campbell
et al., 2001; Herdianita et al., 2000a; Lynne and Campbell, 2003; Lynne and Campbell, 2004;
Lynne et al., 2005) affecting the texture and enclosed micro-components within the rock.
Recognition of biogenicity in ancient rocks is difficult and the distinction between diagenetic and
depositional changes must be understood (Lynne and Campbell, 2004) if we are to use the
ancient sinter geologic record in our search for the origins of life on Earth and potential life
signals on other planets.
The exact formation mechanisms of siliceous sinters are not fully understood. Inorganic
sinter formation mechanisms have been reviewed (Guidry and Chafetz, 2002), while other
studies have investigated the role of microbe-silica interactions (Hinman and Lindstrom, 1996;
Konhauser et al., 2001; Lowe et al., 2001; Lynne and Campbell, 2003; Mountain et al., 2003;
Schultze-Lam et al., 1995; Weed, 1889a; Weed, 1889b; White et al., 1956; Yee et al., 2003) in
sinter deposition. The chemistry of silica, its occurrence, dissolution and deposition, is examined
by Iler (1979) and the effects of organic compounds, pH, cation effects and biological influences
are reported.
Undoubtedly, microbes offer a site for silica accumulation, and their biosignals are an
important paleoenvironmental indicator, but they are probably not the cause of silica deposition.
Sinter formation is a complex interplay of multiple factors, therefore, the term ‘biomineral’
appears to be misleading and ‘organomineral’ is probably more appropriate for siliceous hotspring deposits.
Bacterial encrustations
Minerals that are formed on the outside of bacteria are examples of extracellular
encrustations. Many of the encrustations are formed as bacteria alter the local redox conditions.
For example when metabolic waste products such as H2S, produced by bacteria, interact with
metal cations and form precipitates (Fortin and Beveridge, 1997).The processes that induce
mineralization are usually the indirect result of changing environmental conditions (SchultzeLam et al., 1995), and differ from intracellular ones where oxides have a metabolic role, or in the
formation of the iron biomineral magnetite (Skinner and Jahren, 2003). It should be noted that
there is much to still learn about microbial encrustations and some may be the result of direct
cellular control for example to protect the microbe from its environment.
Archaea and Bacteria may both participate in mineralization processes. According to
Skinner and Jahren (2003) bacteria change their environment while sustaining themselves, and
their environment likewise has equal and important effects in return, a process which has been
given the new term “environmental equivalence”(Fosnot and Perry, 2005). According to Skinner
“…these simple forms accumulate, actively or passively, elements from their environment…” for
metabolic use. In so doing they alter their local environments and “some accumulations can
rightfully be labeled biomineralization in that these creatures are involved with precipitation of a
variety of minerals” (Skinner and Jahren, 2003). It remains an open question, however, whether
extracellular mineral precipitates on bacteria can qualify as biominerals formed under the direct
control of the organisms (Lowenstam and Weiner, 1989; Skinner and Jahren, 2003). Current
evidence suggests that they are indirectly the result of metabolic processes, not employed in
structures or other essential biofunctions and consequently, we would class them as
organominerals. However, microbes may have evolved protective silica and iron coats in order to
protect themselves against for example UV radiation in the early Archaean (Phoenix et al., 2001).
The metal oxide encrustations deposited outside the cells of many bacteria as they grow in
their natural habitats are examples of organominerals. Among the more common types are
oxides of iron and manganese but other metals can be involved as well. Spring outflows often
carry anoxic water to the surface where it is exposed to aeration. Iron and manganese bacteria
such as Gallionella and Leptothrix are commonly found at the mouth of such springs.
Gallionella is a vibrioid bacterium that produces a stalk from its concave surface and the stalk
becomes heavily encrusted with FeO(OH)2. Leptothrix is a sheathed filamentous bacterium that
is also found in springs and in sediments at the anoxic – oxic interface. Depending on the
species, this bacterium can deposit iron or manganese oxides on its sheath.
Manganese encrustations are found in aquatic environments and have been investigated as
bacterial encrustations of Metallogenium (Gregory et al., 1980; Zavarazin, 1964). The
morphology (Fig. 5) is suggestive of a radiating bacterium, but it consists primarily of
manganese oxides and perhaps organic polymers. This causes controversy as to whether it is a
microbe or an inorganic manganese precipitate. It looks like a microbe, is the right size and has a
microbial name. Consequently, principally microbiologists rather than geochemists have carried
out investigations. It has also been implicated in desert varnish formation (Dorn and Oberlander,
1981). This makes intuitive sense: a manganese oxidizing “bacteria” causing the formation of
manganese-rich desert varnish (Hungate et al., 1987; Palmer et al., 1986) appeared to be the
“magic bullet” looked for by many, including us, but it is no doubt incorrect. Again, following
our main theme, we would question whether “Metallogenium” is a bacterium or whether
terminology is shaping the direction of investigations.
The genus Pedomicrobium is also well known as an iron- and manganese-oxidizing,
budding bacterial genus. Thus P. ferrugineum deposits iron oxide on its cell surface. The cells
of this genus are interconnected through the cellular extensions (called prosthecae) upon which
buds are produced. This bacterium grows in pipes, which transport water from lakes and springs
that are rich in iron and manganese. The bacterium attaches to the inner surface of the pipe. As
it proliferates in the pipe, its cells become encrusted with the metal oxides, which accumulate on
the older cells, producing mineral deposits.
Microbial mats and stromatolites
The growth and metabolic activities of microbial mats and their post-mortem decay can
induce the precipitation of organominerals. The most volumetrically important of these is
laminated stromatolitic carbonate, which is extensively studied in modern environments (Reid et
al., 2000), the laboratory (Bosak and Newman, 2003) and the fossil record (Grotzinger and
Knoll, 1999). Related microbial mat organominerals include: tufas (Pedley, 2000), travertines
(Renaut and Jones, 2000), thrombolites (Shapiro, 2000) and dendrolites (Riding, 2000). This
biologically induced calcification occurs in oxic mat-surface environments by the uptake of CO2
and/or HCO3-, which raises the local pH and saturation of carbonate ions, promoting calcification
(Pentecost and Riding, 1986). Also in sub-mat microenvironments, the anaerobic decay of
organic material by heterotrophic bacteria can raise the local pH and induce CaCO3 precipitation
(Visscher et al., 1998). It is, therefore, not surprising that the abundance of microbial carbonates
is largely controlled by microbial and metazoan co-evolution and seawater carbonate saturation
(Riding and Liang, 2005). However, these microbially constructed stromatolites should not be
confused with chemically precipitated stromatolites, which are characterized by crystal fan
fabrics, laminae of uniform thickness, and extreme lateral continuity, and are thought to form in
the absence of microbial mats at times of seawater supersaturation (Pope et al., 2000). These
chemical stromatolites are positively not, therefore, biominerals but may still be composed of
organominerals.
The role of extra-cellular polymeric substances (EPS) in microbial mat
organomineralisation has also received much attention, as they provide abundant chelation sites
for carboxyl, hydroxyl, phosphate and metal groups (Decho, 2000). For example, the faithful
incorporation of certain rare earth element ratios into microbial carbonates has been used to
investigate ancient water chemistry (Kamber and Webb, 2001). The concentration of heavy
metals, especially uranium by microbial mats, has long been used to radiometrically date
Precambrian carbonates (Moorbath et al., 1987). Of most interest to this paper, and astrobiology
in general, is the question of whether this trace metal partitioning and the organic compounds
found in these carbonates can be used to confirm their biological affinity, and distinguish them
from prebiotic films. For example, it has been suggested that enrichments in elements such as
zinc, chromium or copper, which are important enzyme co-factors, may indicate the past
presence of microbial mats in ancient laminated stromatolites (pers. comm., Baltz Kamber and
Jake Bailey). However, much detailed work needs to be done to distinguish these trace metal
patterns from those that might be associated with prebiotic films (Westall et al., 2000). It remains
to be seen whether some of the oldest putative microbial mat remains from the ~3.5Ga Strelley
Pool Chert (Fig. 6) of Western Australia (Hofmann et al., 1999) and the ~3.5Ga Buck Reef Chert
of the Barberton (Tice and Lowe, 2004) preserve these signatures.
Post mortem permineralization
We would also regard organic-containing minerals that are found in association with, and
concentrated by, decaying organic matter as organominerals. For example, permineralised wood,
shell and bone that are often preserved in exquisitely fine detail by silica, carbonate (e.g., coal
balls) or pyrite (Boyce et al., 2001). Concretions are familiar examples that, in some instances,
form with decaying biomass. For example, an ammonite creates a modified geochemical
environment that catalyses the precipitation of early diagenetic minerals from circulating pore
waters (Raiswell and Fisher, 2000). A biological component to the formation of many such
concretions has long been recognised, given the presence of C and S isotopic fractionations that
are consistent with a role for methanogenic and or sulphate-reducing bacteria. Concretions have
also recently been found on Mars (Fig. 7); the so-called “Martian Blueberries” (Catling, 2004)
have been the focus of much attention. Despite the biological connotations of their name, they
are thought to be abiotic in origin and the result of a groundwater process that is also found on
Earth (Chan et al., 2004).
Endolithic trace fossils
Trace fossils preserve information regarding the behavioral interactions of an organism
with its substrate, for instance the tracks and trails an organism produces during feeding and
locomotion. The organisms responsible are only rarely preserved because they are often soft
bodied and not biomineralised. Trace fossils, however, may be associated with organominerals
that were precipitated in and around them. For example, metal enrichment and carbon
sequestration on burrow walls are likely causes of the preferential dolomitization of burrowed
sediments (Gingras et al., 2004). Of great astrobiological relevance are endolithic microborings
(McLoughlin this volume) created by the activities of rock boring micro-organisms that are
capable of tolerating extreme environmental stresses and are, therefore, excellent candidates for
life beyond earth. These form tubular cavities a few microns across and tens of microns long, in
marine carbonates (Green et al., 1988), volcanic basalts and glasses (Furnes and Muehlnbachs,
2003) that may be infilled by later (organo)minerals. Such microborings in modern oceanic
basalts contain nucleic acids, archaeal and bacterial RNA, that is suggestive of a biogenic origin
(Giovannoni et al., 1996). In the modern and fossil record they also contain thin, < 1.0 micron
wide organomineral enrichments in C, N and P on the microtube walls (Furnes et al., 2004) again
suggestive of microbial involvement. MCF also bore pits in rocks but on surfaces in arid regions
(Fig. 3). A related class of organominerals is that found in association with cryptoendolithic
microorganisms, which inhabit cavities within rock substrates. These are probably best
documented from Antarctic dry valley sandstones, where communities of fungi, lichen and
bacteria dwelling within the rock (Friedmann, 1993) are associated with iron hydroxides and
“biogenic” clays that precipitate on extra-cellular polymeric substances (EPS) and decaying
microbes (Wierzchos et al., 2005). These minerals are referred to in the current literature as
biominerals, but as they are a bioproduct of the metabolism and decay of the cryptoendoliths, we
here propose that they would be more usefully described as organominerals.
Meteorites
Carbonaceous meteorites consist of material derived from the solar nebula 4.5 billion years
ago. They also exhibit varying degrees of aqueous processing, thought to have occurred on a
parent body(s) in the region of the asteroid belt during the early stages of formation of the solar
system. Life appears to have existed on Earth for as far back in time as the rock record extends
(~3.800 my). Thus, the only records for the solar system organic inventory that preceded life’s
origin on Earth or possibly Mars are carbonaceous meteorites (Engel and Perry, 2003). In
particular, the CI and CM carbonaceous meteorites contain many of the building blocks for life
as we know it (Sephton, 2002). They provide the best analog for what organic synthesis and
aqueous processing may have been like on planetary surfaces prior to life’s origin. In
carbonaceous meteorites, organic matter is present within the fine-grained, inorganic meteorite
matrix, recording a general relationship between extraterrestrial organic matter and clay minerals
(Pearson et al., 2002) that are undoubtedly the products of parent body aqueous alteration
(e.g.Sephton et al., 2004) (Fig. 7). It is possible that minerals formed on the asteroidal parent
body during alteration have been influenced by the presence of abundant reduced organic matter.
This situation suggests a subdivision of our term organomineral, in that for specific samples
nonbiological organic matter may also influence mineral formation.
Summary
Microbes produce substances that can perturb the speciation of metallic compounds (Stone,
1997). When they die and then lyse, they release into the environment bio-compounds that form
complex reactions with inorganic compounds and minerals. The bio-compounds have
pronounced effects on the acceleration and retardation of chemical reactions. The combination of
organic substances produced in association with living organisms and ‘non-living’ byproducts
are organominerals. Meteorites and manufactured chemicals also are organominerals but they are
derived from organic compounds not produced by life. By redefining the term ‘organomineral’,
new investigative directions may be encouraged and a more precise and focused analysis of some
compounds may be initiated.
APPLICATIONS TO ASTROBIOLOGY
Recognizing the early stages of life’s evolution on Earth and other planets requires access
to geological model systems that mimic early biotic conditions. Can the signature of life
(biogenicity) be recognized in rocks (Gorbushina et al., 2002) from early Earth and Mars? This
question will not only drive NASA’s and ESA’s Martian rover and sample-return missions of the
coming decade, but it is at the crux of a controversy over claims that fossil microbial life is
present in a meteorite undoubtedly derived from Mars (Farmer et al., 2001; McKay et al., 1996).
It also guides the search for evidence of the earliest life on Earth (Brasier et al., 2002; Schopf et
al., 2002). These geological scenarios all have the potential to identify microbial biospheres from
billions of years ago. Rock coatings are relatively young, however the processes that preserve
labile organic compounds in silica have applications to hotspring sinter (~<20mya) and possibly
deep-time Earth fossils.
The unique finding of DNA in rock coatings (Kuhlman et al., 2003; Perry et al., 2004;
Perry et al., 2002) preserved in the minerals, requires a mechanism that sequesters and/or protects
fragile DNA. Mineralization processes generally have been shown to be detrimental to
preserving reproducible DNA, but this depends on the mineral (Eglinton, 1998). The
crystallization of DNA into a structure makes it more stable, acting like an inorganic crystal. The
major factor in protection of DNA after cell lysis is the use of small acid-soluble proteins
(SASPs). SASPs bind to DNA, altering its chemistry and making it more resistant to UV
damage, depurination, and oxidizing agents (Matheson and Brian, 2003). Condensing silicic acid,
which entombs or complexes DNA in a mineral matrix, ultimately may protect DNA from
destruction.
Organominerals as chemical or morphological biomarkers
A biosignature can be classed in two ways: 1) as an organomineral where the signature is a
chemical biosignatures e.g., organics in desert varnish and stromatolites 2) as a morphological
structure e.g. ‘Molar-tooth” ribbons found in silty, clayey, dolomites, forming in voids through
which microbial gasses flow and leaving cavities or morphological evidence of the presence of
life.
Microstromatilitic desert varnish and recent stromatolites are organominerals as they
contain organic compounds but they are also distinctive morphological biomarkers (Fig.s 2 and
6). Ancient stromatolites such as those from 3.4 Ga Strelley Pool chert in western Australia
display stromatolitic fabrics but it is difficult to find chemical markers.
The recognition of biominerals (or their remnant chemical signatures) in ascertaining the
presence of past life, is important when considering the veracity of Archean fossils, life
preserved in meteorites, or microbial deposits (e.g., Metallogenium).
Searching for evidence of life on Mars or for Earth’s earliest life, requires well-defined
chemical and morphological evidence. Can we clearly define which minerals (Gorbushina et al.,
2001) are indicators of life? Does the presence of chemical or morphological compounds support
the existence of past life?
Applications to the search for life’s signals on Mars and other planetary bodies
NASA and other space agencies are interested in the search for life on Mars. The early
Viking biology experiments are generally accepted to be unsupportive of life (Biemann et al.,
1977; McKay, 1998), although differences of opinion remain (DiGregorio, 1997). Viking and
Mars Pathfinder missions provided images of many Martian rocks showing their dark surfaces.
These resemble oxide-rich coatings, reminiscent of rock varnish (DiGregorio, 2002). DiGregorio
(2002) suggested that rock varnish might be a habitat for extant life on Mars. If desert varnish
were to be found on Mars, he suggested that it might prove the existence of past life, since desert
varnish was considered to be biologically formed, a biomineral, when he made his suggestions.
However, if organomineral coatings, e.g., desert varnish or glazes, were found on rocks or in any
other environment on Mars including cracks, caves, or soils, they could also provide information
about past life on Mars.
Cracks and deep crevices in rocks, perhaps deep below the surface where water once
penetrated, could serve to protect minerals harboring past environmental information. For
instance, it is suggested that manganese and iron oxides in caves resemble those of varnish
coatings (Boston et al., 2004; Northrup et al., 2003). They suggest that minerals in caves, if
present on Mars, could be used as indicators of previous biological activity and those of
subsurface caves as potentially illuminating a still-extant biosphere.
If novel forms of life exist on Mars, one needs to anticipate what chemical signatures
to look for (Shapiro and Feinberg, 1995). One of the most universal features of life must be its
inherent movement away from predictable equilibrium chemistry (i.e., its negative entropy). This
might be manifested in many ways, including complex structures, complex chemistry, and a
variety of unpredicted chemical products that accumulate as a result of life’s metabolism (Conrad
and Nealson, 2001; Nealson and Conrad, 1999; Perry and Kolb, 2004 e). In searching for ways to
detect life, we have thus focused many of our efforts on approaches that look for such
disequilibria.
The first step in the search for life on Mars is still the search for organic molecules (Perry
and Hartmann, submitted), since no positive, undisputed evidence for them was found by any of
the previous space missions. Recent advances in analytical techniques and instrumentation,
miniaturization of computers, and robotics, make the technological component for the search for
life easier to achieve than in previous missions. However, the conceptual component for the
search for life is getting more complicated as exotic forms of life on Earth are being discovered,
such as extremophiles that are living in previously unimagined harsh conditions, and species that
reproduce extremely slowly such as endolithic microorganisms in Antarctica. It appears that we
have only touched the tip of the iceberg for analogs of unconventional “Earthly” life. Looking for
life in all the obvious places using standard methods should not prevent us from considering that
Martian life, at least theoretically could be based on a radically different biochemistry (Perry and
Kolb, 2004 e). While we might imagine such life to have self-replicating molecules based on a
genetic code and molecular recognition similar to our Earthly algorithm, the chemical
mechanisms could be quite different. How should we look for alien life signatures and how do
they differ from Earth’s biosignatures? Among the many possible approaches, mining for amino
acids and, if found, their relative abundance might be a starting point, especially considering the
ability of serine to complex and be preserved with silica (Perry et al., 2003b; Zubay, 2000). As
part of a broader search for organic polymers that may have potential for carrying bioinformation, we should look for amino acid based polymers in both biominerals and
organominerals.
CONCLUSIONS
Introducing the term ‘organomineral’ increases specificity and accuracy and allows us to
distinguish between substances that were all previously termed ‘biominerals’. Biominerals are
generated directly by an organism while organominerals are simply formed under the influence
of adjacent organic matter. The utility of our new definition is supported by examples of recent
research into mineral substances that that have been inappropriately approached as biominerals
such as desert varnish, silica sinter and stromatolites. Such scientific prejudice has been bolstered
by the imprecise terminology and data interpretation has been compromised. It is particularly
valuable to distinguish between biominerals and organominerals when we are looking for records
of past biological activity and associated environments in analytically challenging samples. For
example, desert varnish records pollen, polymorphic organic compounds from plants, lead from
industrialization (Perry, 2004), ore provinces (Lakin et al., 1963), atmospheric REEs
(Thiagarajan and Lee, 2004), and any other air-borne substances (Perry, 2004). Silica sinter
deposits fossilize and entomb microbes such as the bacteria pictured in Fig. 4. Stromatolites may
be formed by biology, or if in ancient Archaean environments, may be formed inorganically.
When formed without the aid of biology they will still contain information about the
environment that existed at the time of their formation, just like desert varnish. ‘Organominerals’
gives us a term, which enables us to investigate such substances distinctly from other
biominerals. “We are all prisoners of language” (Kuhn as quoted in (Uttamchandani, 2001)) and
terminology has a subliminal effect on the way we think. In particular it can enable us to ask the
right scientific questions and seek explanations to them. Juliet tries to persuade herself and us
that terminology does not matter,
“ What’s in a name? That which we call a rose
By any other name would smell as sweet.” (Shakespeare, 1914)
But would it? Any name chosen may be instrumental, for example, in ensuring the funding and
direction of scientific research. ‘Astrobiology’ was initially an offshoot of ‘exobiology’ and
although there is still a technical difference between them, the terms are often used
interchangeably. However, both funding and interest in astrobiology have increased to a far
greater extent than in exobiology.
In some ways, organominerals are to life as trace fossils are to body fossils-signatures of
life’s passing. If we use ‘biominerals’ to apply to an overly wide spectrum of substances, we will
concentrate on the biological aspects and will not give due attention to the special qualities of
organominerals. Future investigations may be limited or lead us along a diversionary route. New
definitions also allow one to look toward the future when (in development) a substance may
change from a biomineral to an organomineral, perhaps as in the case of stromatolites, given a
bifurcation emergence (Fosnot and Perry, 2005). Understanding the processes of
biomineralization and the preservation mechanisms in organominerals will aid us in evaluating
and formulating experiments to find answers about past life whether in the Archaean
environments on Earth, organic mineral complexes in and on meteorites or on other planets
especially Mars.
.
ACKNOWLEDGEMENTS
Special thanks to FEI Company at their world headquarters in Hillsboro Oregon, their UK
demonstration offices in Bristol, UK and their European headquarters, Eindhoven,
Netherlandsand to Accural Systems Inc. Special thanks to the National Science Foundation
International Fellowship program. Planetary Science Institute contribution number 385 and
Impacts and Astromaterials Research Centre contribution number 2006-___.
REFERENCES
Adams, J. B., Palmer, F. E., and Staley, J. T. (1992): Rock weathering in deserts: mobilization
and concentration of ferric iron by microorganisms. Geomicrobiology Journal 10, 99114.
Allen, C. C. (1978): Desert varnish of the Sonoran Desert-optical and electron probe
microanalysis. Journal of Geology 86, 743-752.
Biemann, K., Oro, J., Toulmin, P. I., Orgel, L. E., Nier, A. O., Anderson, D. M., Simmonds, P.
G., Flory, D., Diaz, A. V., Rusneck, D. R., Biller, J. E., and Lafluer, A. L. (1977): Results
from the Viking Lander Mission to Mars. Journal of Geophysical Research 82, 46414658.
Bock, G. R., and Goode, J. A. (1996): Evolution of hydrothermal systems on Earth (Mars?), pp.
334: Proceedings of the CIBA foundation symposium, Wiley, Chichester,UK.
Bosak, and Newman (2003): Microbial nucleation of calcium carbonate in the Precambrian.
Geology 31, 577-580.
Boston, P. J., Spilde, M. N., and Northrup, D. E. (2004): Detectable biosignatures for Mars:
biogenic Fe/Mn oxides in caves and surface desert varnish. International Journal of
Astrobiology Supplement 1, 116.
Boyce, C. K., Hazen, R. M., and Knoll, A. H. (2001): Nondestructive, in situ, cellular-scale
mapping of elemental abundances including organic carbon in permineralized fossils.
PNAS 98, 5870-5974.
Brasier, M. D., Green, O. R., Jephcoat, A. P., Kleppe, A. K., Van Kranendonk, M. J., Lindsay, J.
F., Steele, A., and Grassineau, N. V. (2002): Questioning the evidence for Earth's oldest
fossils. Nature 416, 76-81.
Brasier, M. D., McLoughlin, N., Green, O. R., Press, M., Perry, R. S., and Lindsay, J. F. (2004):
Testing the biogenicity of endolithic microborings on early Earth and Mars: new data
from western Australia. Geological Society of America: annual meeting abstracts.
Cady, S. L., and Farmer, J. D. (1996): Fossilization processes in siliceous thermal springs:
Trends in preservation along thermal gradients, pp. 150-173. In G. R. Bock, and J. A. Goode
(Eds): Evolution of Hydrothermal Ecosystems on Earth (and Mars?), Wiley, Chichester,
U.K.
Campbell, K. A., Sannazzaro, K., Rodgers, K. A., Herdianita, N. R., and Browne, P. R. L.
(2001): Sedimentary facies and mineralogy of the Late Pleistocene Umukuri silica sinter,
Taupo Volcanic Zone, New Zealand. Journal of Sedimentary Research 71, 727-746.
Catling, D. C. (2004): Planetary science: On Earth, as it is on Mars? Nature 429, 707-708.
Chan, M. A., Beitler, B., Parry, W. T., Ormö J., and Komatsu, G. (2004): A possible terrestrial
analogue for haematite concretions on Mars. Nature 429, 731-734.
Cleland, C. E., and Chyba, C. F. (2002): Defining 'Life'. Origins of Life and Evolution of the
Biosphere 32, 387-393.
Conrad, P. G., and Nealson, K. H. (2001): A Non-Earthcentric approach to life detection.
Astrobiology 1, 15-24.
Curtiss, B., Adams, J. B., and Ghiorso, M. S. (1985): Origin, development and chemistry of
silica-alumina rock coatings from the semi-arid regions of the island of Hawaii.
Geochimica et Cosmochimica Acta 49, 49-56.
Darwin, C. M. (1871): Natural history and geology. Appleton and Company. New York.
Decho, A. W. (2000): Exopolymer microdomains as a structuring agent for heterogeneity within
microbial biofilms, pp. 9-15. In R. Riding, and R. E. Awramik (Eds): Microbial
Sediments, Springer.
DiGregorio, B. E. (1997): Mars, The Living Planet. Frog Ltd. Berkeley.
DiGregorio, B. E. (2002): Rock varnish as a habitat for extant life on Mars, pp. 120-130. In R. B.
Hoover, G. V. Levin, R. R. Paepe, and A. Y. Rozaanov (Eds): Instruments, Methods, and
Missions for Astrobiology IV, SPIE, Bellingham Washington.
Dorn, R. I. (1984): Cause and implications of rock varnish microchemical laminations. Nature
310, 767-770.
Dorn, R. I., and Oberlander, T. M. (1981): Microbial origin of desert varnish. Science 213, 12451247.
Dorn, R. I., and Oberlander, T. M. (1982): Rock varnish. Progress in Physical Geography 6,
317-367.
Engel, C. G., and Sharp, R. P. (1958): Chemical data on desert varnish. Geological Society of
America Bulletin 69, 487-518.
Engel, M. H., and Perry, R. S. (2003): Analogs for the early synthesis of organic matter on Mars.
Third European Workshop on Exo/Astrobiology. Mars: The Search for Life, 134.
Farmer, J. D. (2000): Hydrothermal systems: Doorways to early biosphere evolution. . GSA
Today 10, 1-9.
Farmer, J. D., and Des Marais, D. J. (1999): Exploring for a record of ancient Martian life.
Journal of Geophysical Research 104, 26,977-26,995.
Farmer, J. D., Nelson, D., Greeley, R., and Kuzim, R. (2001): Mars 2003: Site Priorities for
Astrobiology, Abstract, First Landing Site Workshop for the 2003 Mars Exploration
Rovers, Jan. 24-25, NASA Ames Research Center, Mountain View, California,. Lunar
Planetary Institute Contribution No. 1079.
Farr, T. G. (1981): Surface weathering of rocks in semiarid regions and its importance for
geologic remote sensing, pp. 161: Geological Sciences, University of Washington,
Seattle.
Farr, T. G., and Adams, J. B. (1984): Rock coatings in Hawaii. Geological Society of America
Bulletin 95, 1077-1083.
Ferris, F. G. (1992): Chemical markers of prebiotic chemistry in hydrothermal systems. Origins
of Life and Evolution of Biosphere 22, 109-134.
Flood, B., E., Allen, C., and Longazo, T. (2003): Microbial fossils detected in desert varnish.
Astrobiology 2, 608.
Fortin, D., and Beveridge, T. J. (1997): Microbial sulfate reduction within sulfidic mine tailings:
formation of diagenetic Fe-sulfides. Geomicrobiology Journal 14, 1-21.
Fosnot, C. T., and Perry, R. S. (2005): Constructivism: a psychological theory of learning, pp. 838. In C. T. Fosnot (Ed.): Constructivism, Columbia Teachers Press, New York.
Fournier, R. O., and Rowe, J. J. (1966): Estimation of underground temperatures from the silica
content of water from hot springs and wet-steam wells. American Journal of Science 264,
685-697.
Frausto da Silva, J. J. R., and Williams, R. J. P. (2001): The biological chemistry of the elements:
The inorganic chemistry of life. Oxford University Press. Oxford.
Friedmann, E. I. (1993): Antarctic Microbiology. Wiley. New York.
Furnes, H., Banerjee, N. R., Muehlenbachs, K., Staudigel, H., and de Wit, M. (2004): Early life
recorded in Archaean pillow lavas. Science 304, 578-581.
Furnes, H., and Muehlnbachs, K. (2003): Bioalteration recorded in ophiolitic pillow lavas, pp.
415-426. In Y. Dilek, and P. T. Robinson (Eds): Ophiolites in Earth History, Sp. pub.
Geol. Soc Lon, London.
Gingras, M. K., Pemberton, S. G., Muelenbachs, K., and Machel, H. (2004): Conceptual models
for burrow related, selective dolomitization with textural and isotopic evidence from the
Tyndall Stone, Canada. Geobiology 2, 21-30.
Giovannoni, S. J., Fisk, M. R., and al., e. (1996): Genetic evidence for endolithic microbial life
colonizing basaltic glass-seawater interfaces. Proceedings of the Ocean Drilling Program
Scientific Results 148, 207-214.
Gorbushina, A. A., Boettcher, M., Brumsack, H.-L., Krumbein, W. E., and Vendrell-Saz, M.
(2001): Biogenic forsterite and opal as a product of biodeterioration and lichen
stromatolite formation in the table mountain systems (Tepuis) of Venezuela.
Geomicrobiology Journal 18, 117-132.
Gorbushina, A. A., and Krumbein, W. E. (2000): Rock Dwelling Fungal Communities: Diversity
of Life Styles and Colony Structure, pp. 317-334. In J. Seckbach (Ed.): Journey to
Diverse Microbial Worlds, Kluwer Acadmic Publishers, Dordrecht.
Gorbushina, A. A., Krumbein, W. E., Hamman, C. H., Panina, L., Soukharjevsky, S., and
Wollenzein, U. (1993): On the role of black fungi in colour change and biodeterioration
of antique marbles. Geomicrobiology Journal 11, 205-221.
Gorbushina, A. A., Krumbein, W. E., and Volkmann, M. (2002): Rock surfaces as life indicators:
new ways to demonstrate life and traces of former life. Astrobiology 2, 203-213.
Gorbushina, A. A., Whitehead, K., Dornieden, T., Niesse, A., Schulte, A., and Hedges, J. I.
(2003): Black fungal colonies as units of survival: hyphal mycosporines synthesized by
rock-dwelling microcolonial fungi. Canaduian Journal of Botany 81, 131-138.
Green, J. W., Knoll, A. H., and Swett, K. (1988): Microfossils from Oolites and Pisolites of the
Upper Proterozoic Eleonore Bay Group, Central East Greenland. J. Paleont. 62:835.
Journal of Paleontology 62, 835-852.
Gregory, E., Staley, J. T., and Perry, R. S. (1980): Characterization, distribution and significance
of Metallogenium in Lake Washington. Microbial Ecology 6, 125-140.
Grotzinger, J. P., and Knoll, A. H. (1999): Stromatolites in Precambrian Carbonates:
evolutionary mileposts or environmental dipsticks? Annual Review of Earth and
Planetary Sciences 27, 313-358.
Guidry, S. A., and Chafetz, H. S. (2002): Factors governing subaqueous siliceous sinter
precipitation in hot springs: Examples from Yellowstone National Park, USA.
Sedimentology 49, 1253-1267.
Hedgecoe, A. H. (2003): Terminology and the construction of Scientific Disciplines. The Case
for Pharmacogenomics. Science Technology and Human Values 28.
Herdianita, N. R., Browne, P. R. L., Rodgers, K. A., and Campbell, K. A. (2000a): Mineralogical
and textural changes accompanying ageing of silica sinter. Mineralium Deposita 35, 4862.
Hinman, N. W., and Lindstrom, R. F. (1996): Seasonal changes in silica deposition in hot spring
systems. Chemical Geology 132, 237-246.
Hofmann, H. J., Grey, K., Hickman, A. H., and Thorpe, R. I. (1999): Origin of 3.45Ga coniform
stromatolites of the Warrawoona Group, Western Australia. Geological Society of
America Bulletin 111, 1256-1262.
Horneck, G., and Baumstark-Khan, C. (2002): Astrobiology, The Quest for the Conditions of
Life, Springer-Verlag, Berlin, Germany.
Humboldt, A. (1852): Personal narrative of travels to the equinoctial regions of America during
the years 1799-1804, pp. 243-246, Henry Bohn, London.
Hungate, B., Danin, A., Pellerin, N. B., Stemmler, J., Kjellander, P., Adams, J. B., and Staley, J.
T. (1987): Characterization of manganese-oxidizing (MnII-MnIV) bacteria from Negev
Desert rock varnish: implications in desert varnish formation. Canadian Journal of
Microbiology 33, 939-943.
Iler, R. K. (1979): The Chemistry of Silica: Solubility, polymerization, colloid and surface
properties, and biochemistry. John Wiley and Sons. New York.
Jones, C. E. (1991): Characteristics and origin of rock varnish from the hyperarid coastal deserts
of Northern Peru. Quaternary Research 35, 116-129.
Kamber, B. S., and Webb, G. E. (2001): The geochemistry of late Archean microbial carbonates:
implications for ocean chemistry and continental erosion history. Geochimica et
Cosmochimica Acta 65, 2509-2525.
Konhauser, K. O., Phoenix, V. R., Bottrell, S. H., Adams, D. G., and Head, I. M. (2001):
Microbial-silica interactions in Icelandic hot spring sinter: Possible analogues for some
Precambrian siliceous stromatolites. Sedimentology 48, 415-433.
Krauskopf, K. B. (1957): Separation of manganese from iron in sedimentary processes.
Geochimica et Cosmochimica Acta 12, 61-84.
Kripke, S. A. (1999): Naming and necessity. Harvard University Press. Cambridge.
Krumbein, W. E., and Altman, H. J. (1973): A new method for the detection and enumeration of
manganese oxidizing and reducing microorganisms. Helgolander wiss. Meeresunters 25,
347-356.
Krumbein, W. E., and Jens, K. (1981): Biogenic rock varnishes of the Negev Desert (Israel): an
ecological study of iron and manganese transformation by cyanobacteria and fungi.
Oecologia 50, 25-38.
Kuhlman, K. R., Allenbach, L. B., Ball, C. L., Fusco, W. G., La Duc, M. T., Kuhlman, G. M.,
Anderson, R. C., Erickson, I. K., Stuecker, T., Benardini, J., and Crawford, R. L. (2005):
Ultraviolet (UV-C) resistant bacteria isolated from rock varnish in the Whipple
Mountains, California. Icarus 174, 585-595.
Kuhlman, K. R., Fusco, W. G., La Duc, M. T., Allenbach, L. B., Ball, C. L., Kuhlman, G. M.,
Anderson, R. C., Erickson, I. K., Struecker, T., Benardini, J., Strap, J. L., and Crawford,
R. L. (2006): Diversity of microorganisms within rock varnish in the Whipple Mountains,
California. Applied and environmental microbiology 72, 1708-1715.
Kuhlman, K. R., La Duc, M. T., Kuhlman, G. M., Anderson, R. C., Newcombe, D. A., Fusco,
W., Steucker, T., Allenbach, L., Ball, C., and Crawford, L. (2003): Preliminary
Characterization of a microbial community of rock varnish from Death Valley,
California. Third Mars Polar Science Conference.
Kuhn, T. S. (1996): The structure of scientific revolutions. The University of Chicago Press.
Chicago.
Lakin, H. W., Hunt, C. B., Davidson, D. F., and Oda, U. (1963): Variation in minor-element
content of desert varnish. U. S. Geological Survey, professional papers, 28-31.
Levit, G., and Krumbein, W. E. (2003): Is There An Adequate Terminology Of Biofilms and
Microbial Mats? Ch 22 in Fossil and Recent Biofilms. A Natural History of Life on
Earth ed by Krumbein W E, Paterson D W, Zavarzin G A. 2003.
Lowe, D. R., Anderson, K. S., and Braunstein, D. (2001): The zonation and structuring of
siliceous sinter around hot springs, Yellowstone National Park, and the role of
thermophilic bacteria in its deposition, pp. 143-166. In A.-L. Reysenbach, M. Voytek,
and R. Mancinelli (Eds): Thermophiles: Biodiversity, Ecology and Evolution, Kluwer
Academic/Plenum Publishers, New York.
Lowenstam, H. A., and Weiner, S. (1989): On Biomineralization. Oxford University Press.
Oxford.
Lynne, B. Y., and Campbell, K. A. (2003): Diagenetic transformations (opal-A to opal-CT) of
low- and mid- temperature microbial textures in siliceous hot-spring deposits, Taupo
Volcanic Zone, New Zealand. Canadian Journal of Earth Sciences 40, 1679-1696.
Lynne, B. Y., and Campbell, K. A. (2004): Morphologic and mineralogic transitions from opal-A
to opal-CT in low-temperature siliceous sinter diagenesis, Taupo Volcanic Zone, New
Zealand. Journal of Sedimentary Research 74, 561-579.
Lynne, B. Y., Campbell, K. A., Moore, J. N., and Browne, P. R. L. (2005): Diagenesis of 1900year old siliceous sinter (opal-A to quartz) at Opal Mound, Roosevelt Hot Springs, Utah,
U.S.A. Sedimentary Geology 119, 249-278.
Lynne, B. Y., Campbell, K. A., Perry, R. S., Browne, P. R. L., and Moore, J. N. (in press):
Acceleration of sinter diagenesis in an active fumarole, Taupo Volcanic Zone, New
Zealand. Geology.
Mann, S. (2001): Biomineralization-Principles and concepts in bioinorganic materials
chemistry. Oxford University Press. Oxford.
Mann, S., and Perry, C. C. (1986): Structural aspects of biogenic silica. Ciba foundation
symposium 121. Silicon Biochemistry, pp. 40-58.
Mann, S., Perry, C. C., Williams, R. J. P., Fyfe, C. A., Gobbi, G. C., and Kennedy, G. J. (1983):
The characterization of the nature of silica in biological systems. Journal of Chemical
Society, Chemical Communications 1314, 168-170.
Matheson, C. D., and Brian, D. (2003): The molecular taphonomy of biological molecules and
biomarkers of disease, pp. 127-142. In C. Greenblatt, and M. Spigelman (Eds): Emerging
Pathogens, Oxford University Press, Oxford.
McKay, C. P. (1998): Life on Mars, pp. 386-406. In A. Brack (Ed.): The Molecular Origins of
Life, Cambridge University Press, Cambridge.
McKay, D. S., Gibson, E. K., Jr., Thomas-Keprta, K. L., Vali, H., Romanek, C. S., Clement, S.
J., Chiller, X. D. F., Maechling, C. R., and Zare, R. N. (1996): Search for past life on
Mars: possible relic biogenic activity in Martian meteorite ALH84001. Science 273, 924930.
Moorbath, S., Taylor, P. N., Orpen, J. L., Wilson, J. F., and Treloar, P. (1987): First direct
radiometric dating of Archean stromatolitic limestone. Nature 326, 865-867.
Mountain, B. W., Benning, L. G., and Boerema, J. A. (2003): Experimental studies on New
Zealand hot spring sinters: rates of growth and textural development. Canadian Journal of Earth
Sciences 40, 1643-1667.
Nealson, K. H., and Conrad, P. G. (1999): Life: past, present and future. Philosophical
Transactions of the Royal Society of London, B 354, 1923-1939.
Northrup, D. E., Spilde, M. N., Schelble, R. T., Dano, K. E., Crossey, L. J., Connolly, C. A.,
Boston, P. J., Natvig, D. O., and Dahm, C. N. (2003): Diverse microbial communities
inhabiting ferromanganese deposits in Lechuguilla and Spider Caves. Environmental
Microbiology 5, 1071-1086.
Oliver, J. D., and Perry, R. S. (in press): Definitely life but not definitively. Origins of Life and
Evolution of the Biospheres.
Palmer, F., Emery, D. R., Stemmler, J., and Staley, J. T. (1987): Survival and growth of
microcolonial rock fungi as affected by temperature and humidity. New Phytologist 107,
155-162.
Palmer, F. E., Staley, J. T., Murray, R. G., Counsell, T., and Adams, J. B. (1986): Identification
of manganese-oxidizing bacteria from desert varnish. Geomicrobiology Journal 4, 343360.
Palmer, F. E., Staley, J. T., and Ryan, B. (1990): Ecophysiology of microcolonial fungi and
lichens on rocks in northeastern Oregon. New Phytologist 116, 613-620.
Pearson, V. K., Sephton, M. A., Kearsley, A. T., Bland, P. A., Franchi, I. A., and Gilmour, I.
(2002): Clay mineral-organic matter relationships in the early solar system. Meteoritics
and Planetary Science 37, 1829-1833.
Pedley, M. (2000): Ambient Temperature Freshwater Microbial Tufas, pp. 179-186. In R.
Riding, and R. E. Awramik (Eds): Microbial Sediments, Springer.
Pentecost, A., and Riding, R. (1986): Calcification in cyanobacteria, pp. 73-90. In B. S. C.
Leadbetter, and R. E. Riding (Eds): Biomineralization in lower Plants and Animals,
Systematics Association, Clarendon Press, Oxford.
Perry, C. C., Belton, D., and Shafran, K. (2003a): Studies of biosilicas; structural aspects,
chemical principles,model studies and the future. Progress in Molecular and Subcellular
Biology 33, 269-299.
Perry, C. C., and Keeling-Tucker, T. (1998): Aspects of bioinorganic chemistry of silicon in
conjunction with the biometals calcium, iron and aluminium. Journal of Inorganic
Biochemistry 69, 181-191.
Perry, R. S. (1979): Chemistry and structure of desert varnish 62, pp. 62: Geology, University of
Washington, Seattle.
Perry, R. S. (2004): Biological Chemicals in Rock Coatings, pp. 224: Earth and Space Sciences,
University of Washington, Seattle.
Perry, R. S., and Adams, J. B. (1978): Desert varnish: evidence for cyclic deposition of
manganese. Nature 276, 489-491.
Perry, R. S., Dodsworth, J., Staley, J. T., and Engel, M. H. (2004): Bacterial Diversity in Desert
Varnish. Third European Workshop on Exo/Astrobiology, Mars: the Search for life ESA
Publications Netherlands. SP-545, 259-260.
Perry, R. S., Dodsworth, J., Staley, J. T., and Gillespie, A. (2002): Molecular analyses of
microbial communities in rock coatings and soils from Death Valley California.
Astrobiology 2, 539.
Perry, R. S., Engel, M. H., Botta, O., and Staley, J. T. (2003b): Amino acid analyses of desert
varnish from the Sonoran and Mojave Deserts. Geomicrobiology Journal 20, 427-438.
Perry, R. S., Gorbushina, A. A., Engel, M. H., Kolb, V. M., Krumbein, W. E., and Staley, J. T.
(2003c): Accumulation and deposition of inorganic and organic compounds by
microcolonial fungi. Third European Workshop on Exo/Astrobiology, Mars: the Search
for life, ESA Publications, Netherlands, 76-77.
Perry, R. S., Gorbushina, A. A., Engel, M. H., Kolb, V. M., Krumbein, W. E., and Staley, J. T.
(2004 f): Accumulation and deposition of inorganic and organic compounds by
microcolonial fungi. Third European Workshop on Exo/Astrobiology, Mars: the Search
for life, ESA Publications, Netherlands SP-545, 55-58.
Perry, R. S., and Hartmann, W. K. (submitted): Mars primordial crust: Unique sites for
investigating proto-biologic properties. Origins of Life and Evolution of Biospheres.
Perry, R. S., and Kolb, V. M. (2003): Biological and organic constituents of desert varnish:
review and new hypotheses, pp. 202-217. In R. B. Hoover, and A. Y. Rozanov (Eds):
Instruments, Methods, and Missions for Astrobiology VII, SPIE, Bellingham.
Perry, R. S., and Kolb, V. M. (2004 e): On the Applicability of Darwinian Principles to Chemical
Evolution that Led to Life 2004e. International Journal of Astrobiology 3, 45-53.
Perry, R. S., Kolb, V. M., Ajish, P. I., Lynne, B. Y., McLoughlin, N., Sephton, M. A., Wacey,
D., and Green, O. R. (2005a): Making silica rock coatings in the lab: synthetic desert
varnish, pp. 265-275. In R. B. Hoover, G. V. Levin, A. Rosanov, Y., and R. G. Gladstone
(Eds): Astrobiology IX, SPIE, Bellingham.
Perry, R. S., and Lynne, B. Y. (2006): New insights into natural recorders of planetary surface
environments: the role of silica in the formation and diagenesis of desert varnish and
siliceous sinter. Lunar and Planetary Science XXXVII.
Perry, R. S., Lynne, B. Y., McLoughlin, N., Kolb, V. M., Sephton, M. A., Olendzenski, L.,
Engel, M. H., Brasier, M. D., and Staley, J. T. (2005b): How Desert Varnish forms?, pp.
276-287. In R. B. Hoover, G. V. Levin, A. Y. Rosanov, and R. G. Gladstone (Eds):
Astrobiology IX, SPIE, Bellingham.
Perry, R. S., Lynne, B. Y., Sephton, M., Kolb, V. M., Perry, C. C., and Staley, J. T. (in press):
Baking black opal in the desert sun: The importance of silica in desert varnish. Geology.
Phoenix, V. R., Konhauser, K. O., Adams, D. G., and Bottrell, S. H. (2001): Role of
biomineralization as an ultaviolet shield: Implications for Archaean life. Geology 29, 823826.
Pope, M. C., Grotzinger, J. P., and Schreiber, B. C. (2000): Evaporitic subtidal stromatolites
produced by in situ precipitation: textures, facies associations, and temporal significance.
Journal of Sedimentary Research 70, 1139-1151.
Potter, R. M. (1979): The tetravalent manganese oxides: clarification of their structural variation
and relationships and characterization of their occurrence in the terrestrial weathering
environment as desert varnish and other manganese oxides concentrations, pp. 254:
Geology, California Institute of Technology, Pasadena.
Potter, R. M., and Rossman, G. R. (1977): Desert varnish: the importance of clay minerals.
Science 196, 1446-1448.
Potter, R. M., and Rossman, G. R. (1979a): The manganese- and iron-oxide mineralogy of desert
varnish. Chemical Geology 25, 79-94.
Potter, R. M., and Rossman, G. R. (1979b): Mineralogy of manganese dendrites and coatings.
American Mineralogy 64, 1219-1226.
Raiswell, R., and Fisher, Q. J. (2000): Mudrock hosted carbonate concretions: a review of growth
mechanisms and their influence on chemical and isotopic composition. Journal of the
Geological Society of London 157, 239-251.
Raymond, R. J., Guthrie, G. D. J., Bish, D. L., Reneau, S. L., and Chipera, S. J. (1992):
Biomineralization of manganese and rock varnish, pp. 321-336. In H. C. W. Skinner, and
R. W. Fitzpatrick (Eds): Biomineralization - Processes of iron and manganese, CATENA
VERLAG, Cremlingen-Destedt.
Reid, R. P., Visscher, P. T., Decho, A. W., Stolz, J. F., Bebout, B. M., Dupraz, C., Macintyre, I.
G., Paerl, H. W., Pinckney, J. L., Prufert-bebout, L., Steppe, T. F., and DesMarais, D. J.
(2000): The role of microbes in accretion, lamination and early lithification of modern
marine stromatolites. Nature 406, 989-992.
Renaut, R. W., and Jones, B. (2000): Microbial precipitates around continental hot springs and
geysers, pp. 187-195. In R. Riding, and R. E. Awramik (Eds): Microbial Sediments,
Springer.
Rice, C. M., Ashcroft, W. A., and Batten, D. J. (1995): A Devonian auriferous hot spring system,
Rhynie, Scotland. Journal of the Geological Society London 152, 229-250.
Riding, R. (2000): Microbial carbonates: the geological record of calcified bacterial-algal mats
and biofilms. Sedimentology 47, 179-216.
Riding, R., and Liang, L. (2005): Geobiology of microbial carbonates: metazoans and seawater
saturation state influences on secular trend during the Phanerozoic. Palaeogeography,
Palaeoclimatology and Palaeoecology 219, 101-115.
Schelble, R. T., McDonald, G. D., Hall, J. A., and Nealson, K. H. (2005): Community structure
comparison using FAME analysis of desert varnish and soil, Mojave Desert, California.
Geomicrobiology Journal 22, 353-360.
Schopf, J. W., A.B., K., Agresti, D. G., Wdowiak, T. J., and Czaja, A. D. (2002): Laser-Raman
imagery of Earth's earliest fossils. Nature 416, 73-76.
Schultze-Lam, S., Urrutia, M. M., and Beveridge, T. J. (1995): Metal and silicate sorption and
subsequent mineral formation on bacterial surfaces: subsurface implications, pp. 111-147.
In H. E. Allen (Ed.): Metal Contaminated Aquatic Sediments, Ann Arbor Press, Chelsea,
Michigan.
Sephton, M. A. (2002): Organic compounds in carbonaceous meteorites. Natural Products
Reports 19, 292-311.
Sephton, M. A., James, R. H., and Bland, P. A. (2004): Lithium isotope analyses of inorganic
constituents from the Murchison meteorite. Astrophysical Journal 612, 588 - 591.
Sephton, M. A., Pillinger, C. T., and Gilmour, I. (2001): Normal alkanes in meteorites: molecular
δ13C values indicate an origin by terrestrial contamination. Precambrian Research 106,
47-58.
Shakespeare, W. (1914): Romeo and Juliet. Oxford University Press. Oxford.
Shapiro, R., and Feinberg, G. (1995): Possible forms of life in environments very different from
the Earth, pp. 165-172. In B. Zuckerman, and M. H. Hart (Eds): Extraterrestrials, Where
are They, Cambridge University Press, Cambridge.
Shapiro, R. S. (2000): A Comment on the Systematic Confusion of Thrombolites. Palaios 15,
166-169.
Sherwood, L., B., Westgate, T. D., Ward, J. A., Slater, G. F., and Lacrampe-Couloume, G.
(2002): Abiotic formation of alkanes in the Earth's crust as a minor source for global
hydrocarbon reservoirs. Nature 416, 522-524.
Skinner, H. C. W., and Jahren, A. H. (2003): Biomineralization, pp. 117-184: Treatise on
geochemistry, Elsevier.
Sogin, M. L., McCall, W. A., and Ordal, J. Z. (1972): Effect of heat activation conditions on the
germinal response of Bacillus cereus T spores, pp. 471. In H. O. Halvorson, R. Hanson,
and L. Campbell (Eds): Spore V, American Society of Microbiology, Washington D. C.
Staley, J. T., Adams, J. B., and Palmer, F. E. (1992): Desert varnish: a biological perspective, pp.
173-195. In G. Stotsky, and J.-M. Bollag (Eds): Soil Biochemistry, Marcel Dekker Inc.,
New York.
Staley, J. T., Jackson, M. J., Palmer, F. E., Adams, J. B., Borns, D. J., Curtiss, D. J., and TaylorGeorge, S. (1983): Desert varnish coatings and microcolonial fungi on rocks of the
Gibson and Great Victoria Deserts, Australia. BMR Journal of Australian Geology and
Geophysics 8, 83-87.
Staley, J. T., Palmer, F. E., and Adams, J. B. (1982): Microcolonial fungi: common inhabitants
on desert rocks? Science 215, 1093-1095.
Stone, A. T. (1997): Reactions of extracellular organic ligands with dissolved metal ions and
mineral surfaces, pp. 309-341. In J. E. Banfield, and K. H. Nealson (Eds):
Geomicrobiology: Interactions beween microbes and minerals, Mineralogical Society of
America.
Taylor-George, S., Palmer, F. E., Staley, J. T., Borns, D. J., Curtiss, D. J., and Adams, J. B.
(1983): Fungi and bacteria involved in desert varnish formation. Microbial Ecology 9,
227-245.
Thiagarajan, N., and Lee, C.-T. A. (2004): Trace-element evidence for the origin of desert
varnish by direct aqueous atmospheric deposition. Earth and Planetary Science Letters
224, 131-141.
Tice, M. E., and Lowe, D. R. (2004): Photosynthetic microbial mats in the 3,416-Myr-old ocean.
Nature 431, 549-552.
Trewin, N. H. (1994): Depositional environments and preservation of biota in the Lower
Devonian hot-springs of Rhynie, Aberdeenshire, Scotland. Transactions of the Royal
Society of Edinburgh, Earth Sciences 84, 433-442.
Uttamchandani, M. (2001): Kripke and Kuhn on Essentialism.
Visscher, P. T., Reid, R. P., and Bebout, B. M. (1998): Microscale observations of sulphate
reduction: Correlation of microbial activity with lithified micritic laminae in modern
marine stromatolites. Geology 28, 919-922.
Walter, M. R., Des Marais, D., Farmer, J. D., and Hinman, N. W. (1996): Lithofacies and
Biofacies of Mid-Paleozoic thermal spring deposits in the Drummond basin, Queensland,
Australia. Palaios 11, 497-518.
Weed, W. H. (1889a): Formation of travertine and siliceous sinter by vegetation of hot springs.
U.S. Geological Survey, 9th Annual Report 1887-1888, 613-676.
Weed, W. H. (1889b): On the formation of siliceous sinter by the vegetation of thermal springs.
American Journal of Science 37, 351-359.
Westall, F., Steele, A., Toporski, J., Walsh, M., Allen, C., Guidry, S., McKay, D., Gibson, E.,
and Chaftez, H. (2000): Polymeric substances and biofilms as biomarkers in terrestrial
materials: Implications for extraterrestrial samples. Journal of Geophysical Resources
105 E, 24511-24527.
White, D. E., Brannock, W. W., and Murata, K. J. (1956): Silica in hot-spring waters.
Geochimica et Cosmochimica Acta 10, 27-59.
Wierzchos, J., Garcia, S. L., and Ascaso, C. (2005): Biomineralisation of endolithic microbes in
rock from the McMurdo Dry Valleys of Antarctica: implications for microbial fossil
formation and their detection. Environmental Microbiology 7, 566-575.
Yee, N., Phoenix, V. R., Konhauser, K. O., Benning, L. G., and Ferris, F. G. (2003): The effect
of cyanobacteria on silica precipitation at neutral pH: Implications for bacterial
silicification in geothermal hot springs. Chemical Geology 199, 83-90.
Zavarazin, G. A. (1964): Metallogenium Symbioticum. Zeitschrift fur Allgemeine Mikrobiologie
11, 390-395.
Zubay, G. (2000): Origins of life on the Earth and in the cosmos. Academic Press. San Diego.
Abstract
Click here to download Abstract: Final abstract.doc
By introducing the new term ‘organomineral’ to apply to minerals that are
affected by organics, mostly life-related, but not directly produced by living cells, we
hope to increase the accuracy of the terminology in use at present. We believe that the
term ‘biomineral’ does not describe all mineral deposits precisely enough and offer
case studies to support instances where the use of a new, specific term
‘organomineral’ is more appropriate. We provide examples of some materials that are
biominerals e.g., diatoms and human bones. We then attempt to show that this
terminology can sometimes mislead investigators, drive the direction and prejudice
interpretations of scientific investigation. This is achieved by presenting case studies
of minerals that have been investigated as biominerals although they may not actually
be directly controlled by biology. We pay special attention to desert varnish, hotspring siliceous deposits, stromatolites, and bacterial encrustations. A detailed
understanding of how organic compounds are preserved and transformed in the
mineral matrix is highly relevant to the search for the oldest evidence of life on Earth.
Table
Click here to download Table: Final Table 1 biominerals.doc
TABLE 1. SELECTED BIOMINERALS
_______________________________________________________________________
Mineral
Formula
Organism
Type
_______________________________________________________________________
Calcite
CaCO3
Foramnifera
Shell
Molluscs
Shell
Birds
Eggshells
Echinoderms
Shell/spines
Mg-Calcite
(Mg,Ca)CO3
Octocorals
Spicules
Corals
Exoskeleton
Aragonite
CaCO3
Molluscs
Shell
Gatropods
Love dart
Cephalopods
Shell
Vertebrates
Bone
Hydroxyapatite
Ca10(PO4)6(OH)2
Mammals
Teeth
Fish
Scales
Diatoms
Exoskeletons
Silica
SiO2·nH2O
Radiolarians
Skeleton
Plants
Spines & Leaves
Limpets
Teeth
Bacteria
Magnetotaxis
Magnetite
Fe3O4
Chitons
Teeth
Tuna/Salmon
Magnetic navigation
Lepidocrocite
γ-FeOOH
Chitons
Teeth
Animals/Plants
Ferritin
Ferrihydrate
5Fe2O3·9H2O
Beaver/rat/fish
Tooth surface
Jellyfish
Gravity receptor
Gypsum
CaSO4·2(H2O)
Barite
BaSO4
Chara
Gravity receptor
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Table 2
Click here to download Table: Final TABLE 2.doc
TABLE 2. ORGANOMINERALSδ
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Category
Type
Location Example
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Permineralized
Petrified Wood
Petrified Forest, Arizona
Carbonate
Bahamas
Silicified subaerial lichens Forsterite
Tepuis, Venezuela
Microcolonial fungi
Desert Varnish
Most worldwide deserts
Stromatolites
Ancient
Strelley Pool, Australia
Cave Deposits
Manganese/silica
Lechuguilla, New Mexico
Trace fossils
Microtubles
Karoo, South Africa
Microtubles ~3.6 bya
Pilbara, Western Australia
Bacterial Encrustations
Gallionella
Springs worldwide
Leptothrix
Springs worldwide
Mettalogenium
Aquatic habitats
Pedomicrobium
Aquatic habitats
Hot-spring (forming)
Siliceous sinter
Taupo Volcanic Zone, NZ
Travertine
Yellowstone, Wyoming
Hot-springs (extinct)
Siliceous sinter
Steamboat Srings, Nevada
Silica-rich coatings
Desert varnish
c.f. Namibian, Negev Deserts
Glazes
Silica
c.f. Hawaii, Oregon, Antarctica
Oceanic microborings
Microtubles
Ontong Java Plateau
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δ
With the current state of knowledge the above examples are best defined as organominerals,
however some bacterial encrustations or for example forsterite may in the future be proved to be
better characterized as biominerals
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Captions
FIG. 1 (a) Bones and teeth of mammals are composed calcium phosphates combined
with proteins,(b) shells are composed of calcium carbonate (fibrous polymorph) in the
bivalve shell. (c) SEM image of a diatom on the surface of a desert varnish coated rock
from the Mojave Desert, California. (d) Magnetite in a bacterium, adapted from
Devouard et al. (1998), American Mineralogist V. 83, 1387-1398.
FIG. 2 (a) Botryoidal desert varnish, from Death Valley, California, forms in depressions
on rock surface (white arrows). Micro-surface textures vary from area to area, and not all
varnish coatings display mounded surface morphologies. (b) Scanning transmission
electron micrograph (STEM) image of a Focused Ion Beam (FIB,“DualBeam”) prepared
wafer of desert varnish from Death Valley, California. The section was cut normal to the
varnish surface. STEM improves chemical contrast with lower atomic numbered
elements appearing dark and higher ones appearing lighter. In typical oxide-rich white
areas, EDAX (i), there is ~4.3 wt % oxide of SI and ~3.17 wt % oxide of Al. In contrast,
gray areas in this EDAX sample (ii), typically contain ~32.6 wt % oxide of Si and no
detectable Mn or Al. Figured is adapted from Perry et al. in press, Geology.
FIG 3. MCF are often associated with rocks in arid areas. The MCF pit rock surfaces, as
shown in (a) a desert varnish coated rock from Death Valley, California and (b) a desert
varnish coated rock, with surface MCF, from the Gobi Desert. (c) MCF have melanin
pigments (the dark gray areas outside the cell) mixed with copious quantities of EPS. (d)
Degrading MCF on desert varnish coated rock from Bishop, California, show mineral
platelets that have adhered to EPS and appear to have become part of coatings.
FIG 4. Scanning electron microscope (SEM) images of silicified microbes in opal-A
siliceous sinter. (a, b) Cryostage SEM images of microbes from Orakei Korako, Taupo
Volcanic Zone, New Zealand. (a) Initial stages of silicification with opal-A spheres of
mid-temperature (35-49 ºC) sized microbes. (b) low-temperature (<35 ºC) microbes
surrounded in a network mesh of exopolymeric substances (EPS). (c, d) Low-temperature
(<35 ºC) sized filamentous microbes in opal-A siliceous sinter from Steamboat Springs,
Nevada. (c) Longitudinal view of segmented filamentous microbe. (d) Cross-sectional
view of a community of filamentous microbes. Adapted from Rodgers et al 2004 Earth
Science Reviews 66, pages 1-61
Figure 5. Optical micrograph of manganese encrusted ‘Metallogenium’ from Lake
Washington, Seattle, Washington. It has the morphology of a bacteria, however it is still
disputed whether it is a microbe (Gregory et al., 1980, Zavarazin 1964) or an inorganic
manganese precipitate.
FIG 6. (a)Ultra-thin section (~<10 µm) of varnish coating cut normal to the surface.
White arrows point to abundant trapped detrital grains. This sample shows botryoidal
structures in several orientations. Dark areas within stromatolitic-like structures are
enriched in manganese oxide, while light areas are relatively deficient in manganese
oxides. (b, c) ~3.5 GA year old stromatolites from the Strelley Pool Chert, Pilbara
Craton, Western Australia.
FIG 7. (a) X-ray maps of a OsO4 impregnated surface of the Murchison meteorite
(Pearson et al., 2002). Os-stained organic matter (gray) is concentrated in the
phyllosilicate-rich chondrule rim and matrix (Fe = lighter areas, Si = darker areas in the
chondrule, Os = gray). (b) A ‘Martian Blueberry’, image taken near a rock outcrop called
Stone Mountain from Mars Exploration Rover (provided by NASA and JPL). A typical
diameter of a spherule is ~ 4 millimeters, roughly the size of a small blueberry. The
origin of the tiny spherules is debated, and whether their shape has to do with a slow
accumulation of sediments suspended in water, or flash-frozen rock expelled during a
meteor impact. Most interestingly, they might be "concretions," which form when a
fluid, possibly water, carrying dissolved minerals flows through a rock and "precipitates"
a grain that typically grows into a sphere. See text on post mortem permineralization.
Figure 1
Figure 1
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Figure 7
Figure 7