Download Emerging Frontiers in Geomicrobiology

Emerging Frontiers
in Geomicrobiology
Alexis Templeton1 and Karim Benzerara2
1811-5209/15/0011-0423$2.50
T
DOI: 10.2113/gselements.11.6.423
also use specific microsensors (e.g.
O2, sulfide, and pH) or fluorescent
probes to map chemical gradients
at the microscale. Substantial
advances in subcellular imaging
t e c h n i q u e s — h i g h - r e s o l ut i o n
scanning, tunneling and transmission electron and X-ray microscopies—allow GMG researchers
to probe cellular microenvironments, image the spatial relationships between organisms, and
analyze their localized chemical
or electrical activity or signaKEYWORDS : biomineralization; mineral exploration; biogeobatteries; electrontures. Future studies that make
transfer, fossilization
use of correlative microscopies will
result in more effective coupling
INTRODUCTION
between chemical and taxonomic imaging to visualize
The field of geomicrobiology and microbial geochemistry
the expression of genes, observe electron transfer, and see
(GMG) has made several orders of magnitude leaps over
any changes in the material properties around cells. Such
the past two decades—in terms of the number of research
advances will surely produce new paradigms regarding
scientists who self-identify with the field, to the number
microbe–mineral interactions and biosignature formation
of systems and specific processes under investigation, to
in natural environments.
the scales over which geomicrobiological processes can be
detected and connected. It is now becoming tractable to GMG approaches will profoundly influence such fields as
materials science, applied geochemistry, human health, and
use GMG approaches to ask questions such as: “How does
paleontology. Detailed mechanistic models of microbe–
the activity of a single cell influence the microbial commumetal and microbe–mineral interactions are, and will be,
nity and the wider geochemical and geophysical properties
crucial for not only understanding the function of modern
of their local environments?”, “What are the length- and
timescales across which the biological and geochemical marine and terrestrial ecosystems but also for deciphering
the deep-time record of major environmental transitions,
processes are interconnected?”, and, “To what degree do
the mechanisms of environmental geomicrobiological or for seeking direct evidence of early life and metabolisms.
Furthermore, microbial metal cycling, electron transfer,
processes provide insight into complex microbial function
and biomineralization processes have now been recognized
in engineered or human systems?”
in amazingly diverse biomes, including such environments
GMG researchers have developed new capabilities to probe
as the human body. This article will review and discuss
the microenvironment that surrounds living cells. Some of some of the many frontiers that GMG approaches are
the most sensitive measures of the environment surrounding
directly influencing.
microorganisms can now be obtained through multiple
techniques. For example, fluorescent in situ hybridization MICROBIAL BIOMINERALIZATION
secondary ion mass spectrometry (FISH-SIMS) simultane- AND MATERIALS SYNTHESIS
ously provides isotopic probes of biogeochemical activity
and single-cell phylogenetic identification. Voltammetry Over the last 15 years, material scientists have designed
enables one to measure the in situ transformation of many new routes for synthesizing diverse nanomaterials using
redox active species at the microscale; similarly, one can microorganisms or some type of microbe-inspired strategy.
This is based on the capability of some microorganisms
to form, by a process called biomineralization, mineral
particles with unique properties that cannot be otherwise
1 Department of Geological Sciences
produced under abiotic conditions (FIG. 1). Mineral partiUniversity of Colorado, Boulder CO 80309-0399 USA
cles with a variety of shapes, sizes, and chemical composiE-mail: [email protected]
tions can be synthesized intracellularly or extracellularly
2 Institut de Minéralogie, de Physique des Matériaux,
by microorganisms. This gives rise to materials with an
et de Cosmochimie (IMPMC)
associated variety of chemical, electrical, magnetic, and/or
Sorbonne Universités – UPMC, UMR CNRS 7590
photoconductive properties. A broad diversity of microorE-mail: [email protected]
ganisms—including bacteria, fungi, and viruses—produce
Muséum National d’Histoire Naturelle, IRD UMR 206
nanoparticles of Au, Ag, Pt, Pd, Te, or Se, as well as diverse
he interdisciplinary field of geomicrobiology and microbial geochemistry (GMG) has provided surprising insights into microbial function
and preservation in diverse environments. The emerging frontiers in
GMG are driven by recent discoveries in material sciences, economic geology,
human health, and paleontology. The length-scales and mechanisms by which
organisms can transfer electrons are being redefined, which have implications ranging from the formation of ore deposits to microbial function in the
human body. Pathways of biomineralization are a critical control for many
fossilization processes. Microbiologically produced materials also exhibit great
potential for technological and medical applications.
4 Place Jussieu, F-75005 Paris, France
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PP.
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1 µm
of interest. Thus, several different scientific communities
have a common goal of better understanding all the genetic
steps involved in the formation of intracellular magnetite.
Three types of bacterially formed mineral phases.
(LEFT) Amorphous CaCO3 particles formed within
the cyanobacterial cells. (M IDDLE) Photoactive arsenic sulfide
nanotubes formed outside the cell walls of a Shewanella sp. IMAGE
CREDIT : H. G. H UR . (R IGHT) Monodomain magnetite crystals formed
within the cells of Magnetobacterium bavaricum. IMAGE CREDIT:
A. ISAMBERT, E. L ARQUET, AND N. M ENGUY.
FIGURE 1
sulfide or oxide nanoparticles, such as CdS, ZnS, AsS, FeS2,
Fe3O4, Co3O4, or UO2 (Narayanan and Sakthivel 2010).
Microbial controls on nanoparticle formation can involve
a variety of molecular processes that include redox catalysis, confi nement in microcompartments, or nucleation
on organic polymers with a specific architecture. Such
microbiological materials can be used for a wide range
of applications in optoelectronics, electronics, and sensor
technologies, as well as medical science.
Most microorganisms that are used for materials synthesis
applications have been cultivated from natural environments where biomineralization is ubiquitous. For example,
Southam and Beveridge (1996) studied the formation of
octahedral gold nanoparticles by Bacillus subtilis. In order
to make the synthesis of microbiomaterials and their
properties more efficient, GMG approaches are required
to provide material scientists with a detailed understanding
of the molecular processes that control biomineralization.
Understanding molecular processes is also a crucial objective for geomicrobiologists in order to track and quantify
the impact of biomineralization in modern environments,
as well as to reconstruct the geological history of such
processes through phylogenetic analyses.
An emblematic example of the connections between
GMG and material sciences is provided by magnetotactic
bacteria, which have been extensively studied by geomicrobiologists. These bacteria, found in a variety of aquatic
environments, are able to align themselves along Earth’s
magnetic field lines (Lefevre and Bazylinski 2013). Their
compass consists of intracellular magnetic nanocrystals of
magnetite (Fe3O4) or greigite (Fe3S 4), which have narrow
and controlled size ranges (35–120 nm) and shapes. These
intracellular nanocrystals are crystallographically aligned
and form chains within the cells along specific proteins.
Isambert et al. (2007) proposed that microbially formed
magnetites contain durable features indicative of their
biotic origin and can, therefore, be tracked as traces of life
in ancient and/or extraterrestrial rocks. For material scientists, there is great interest in how magnetotactic bacteria
control the distribution, shape, and size of nanoparticles
in order to optimize magnetic properties. These bacteria
may provide an inspiration for how to synthesize magnetic
nanoparticles with highly regulated shapes (Prozorov et
al. 2013). Several applications for these types of magnetic
nanoparticles have been proposed: the development of
new, high density, magnetic storage devices; the medical
use of these nanoparticles as delivery vectors or as seeds
for inducing hyperthermia in cancer treatment; or to
magnetically label, immobilize, and/or separate molecules
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The immobilization of arsenic by microbially formed
minerals provides another ongoing connection between
geomicrobiology and material sciences. For a long time, the
formation of orpiment (As2S3) was considered to be a phase
that only formed abiotically under hydrothermal conditions. The discovery that the bacteria Desulfotomaculum
auripigmentum was able to form this phase (Newman et al.
1997) illustrated that microorganisms could catalyze the
formation of orpiment at lower temperatures and thereby
provide a biogeochemical sink for As(III). From a materials
science perspective, Lee et al. (2007) studied the bacterial
formation of certain chalcogenides and found that another
species, Shewanella sp., can form extracellular orpiment
(As2S3) and realgar (AsS) nanotubes with diameters from 20
to 100 nm and lengths up to 30 μm. Interestingly, chalcogenide nanotubes behave as metals and semiconductors in
terms of their electrical properties and are photoconductive. This means that they have the potential to be used in
the fabrication of next-generation nanoscale optoelectronic
materials.
MICROBES IN MINERAL EXPLORATION
Microbe-driven metal cycling has been a pervasive
theme throughout the growth of the field of geomicrobiology. The majority of studies have focused either on
precipitation and immobilization of toxic metals or on
mineral redox transformations that release metals into
the environment. However, there also exists significant
interest in prospecting for biologically formed economic
mineral deposits and in understanding how microbes have
influenced the surface processes that control the accumulation and localized precipitation of metals within and
surrounding ore bodies. Thus, geomicrobiology is increasingly being integrated into economic geology and resource
extraction. Frank Reith (University of Adelaide, Australia)
coined the term “exploration geomicrobiology” to refer to
the role played by microbial organisms in cycling rare and
precious metals, particular microbially driven precipitation
of metals at economically viable concentrations.
Microbially mediated mineral dissolution, mineral precipitation, and the concentration of trace elements are core
concepts for predicting the biogeochemical behavior and
localization of Au, Pt, rare earth elements (REEs), and
energy-critical metals. For example, REEs are essential for
the production of photovoltaics, batteries, high-strength
permanent magnets, catalysts, and lighting; yet, economically viable deposits are scarce. In the past decade, there
have been major advances in understanding the mobility
of REEs in surface environments through complexation
with inorganic ligands such as carbonate and phosphate,
as well as by complexation with organic ligands and siderophores (Tang and Johannesson 2003). For example, after
REEs have been solubilized and mobilized from minerals,
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subsequent REE complexation with bacterial surfaces can
lead to secondary enrichment of REEs by immobilization
as phosphate minerals formed by biomineralization (Bau
et al. 2013).
It is critical to defi ne the mechanisms by which microbes
produce the metal enrichments that give rise to economic
mineral deposits. In laboratory studies, elemental platinum
nanoparticles can be generated by the microbial reduction of soluble PtCl40 complexes to produce Pt(II) nanoparticle chains that are stabilized in an organic matrix; these
chains then undergo recrystallization and further reduction to Pt(0) (Lengke et al. 2006). Do such processes
occur in natural systems? Likely yes! A surprising recent
geomicrobiological discovery is the direct involvement of
bacteria—which form biofi lms on secondary gold grains
found in many surface environments—in the formation
of the gold grains themselves. Specifically, Reith et al.
(2009) demonstrated that organisms common in metalrich environments, such as Cupriavidus metallidurans, can
mediate Au biomineralization by reducing soluble, toxic
Au(III) complexes and forming elemental gold as a fi nal
product (FIG. 2). Moreover, in demonstrating that gold is
commonly precipitated biologically, Reith et al. (2009) also
showed that Au(III)-complexes can exert strong controls
on the regulation and expression of a microbe’s genes. This
in turn has spurred significant interest in the molecular
mechanisms involved in metal resistance and Au cycling.
From a resource extraction perspective, there are now great
opportunities to develop “omics” approaches to probe the
genes and metabolites specifically utilized by microorganisms to precipitate precious metals, and to then optimize
their function.
A large conceptual shift in GMG regarding extracellular
electron transport was initiated by Gorby et al. (2006)
who revealed direct electrical connections between single
microbial cells and other organisms, as well as between
cells and solid, electroactive mineral surfaces (such as
Fe(III)-oxides). El-Naggar et al. (2010) used nanofabricated
electrodes and probe atomic force microscopy to quantify
electron-transport rates along nanowires and confi rmed
that the conductivity of these biomaterials was dependent
upon outer-membrane cytochromes (MtrC and OmcA).
These authors also showed that the electron-transfer rates
through nanowires exceeded specific cellular respiration
rates; thus, such nanowires can be effectively used for
microbial metabolism.
So, does the microbial coupling of distant half-reactions
occur in natural environments and give rise to electric
fields that can be detected? The field studies and conceptual models developed by Revil et al. (2010) were groundbreaking: they established that spatially separated redox
reactions could be directly coupled by conductive biological materials interconnected with semiconductor minerals
and that this phenomena is particularly strong in contaminated aquifers.
Recent work by Risgaard-Petersen et al. (2012) and Pfeffer
et al. (2012) revealed that sulfide in marine sediments
could be microbially oxidized when pulses of oxygen are
introduced centimeters above. One novel pathway for the
long-distance electron transport involves the activity of
“cable-bacteria,” which are fi lamentous deltaproteobacteria (e.g. Desulfobulbacea) that can form centimeter-scale
conductors. When electron transfer between spatially
separated anodes and cathodes occurs through electrical
conductors, steep gradients in pH, as well as sulfate,
calcium and iron, are the result. This drives ion migration across suboxic zones and induces changes in mineral
solubility (Risgaard-Petersen et al. 2012). If such “cables”
are disrupted or cut, they lose their property to transmit
electrical currents (Pfeffer et al. 2012) (FIG. 3).
False-colored gold that is inferred to have formed
by microbial reduction and precipitation of Au(III)complexes from solution. IMAGE CREDIT: FRANK R EITH, (CSIRO)
FIGURE 2
“BIOGEOBATTERIES” AND LONG-DISTANCE
ELECTRON TRANSPORT
In the past decade, a massive expansion in the known
pathways for microbial extracellular electron transport
has revealed how biogeochemical processes can be directly
coupled across the entire scale of the system studied.
While the spatial domain for electron transfer was once
defined only at the nanometer scale, today one can directly
observe centimeter-scale long-distance electron transfer.
This means that redox gradients and “biogeobatteries” may
develop over scales of meters … possibly even kilometers!
The core concept of “biogeobatteries” is that anodic
reactions are spatially separated from cathodic reactions.
An example would be the oxidation of sulfide (or organic
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matter or oils) in sediments and shallow aquifers being
linked to the consumption of oxidants, such as oxygen
or nitrate, that are distant from the sulfide. For this to be
possible, electron transfer and ion exchange must occur
over long length scales to balance the coupled reactions.
Several mechanisms for such extracellular electron transfer
have been identified, some of which require microbially
generated electroactive materials (“electron shuttles”) or
extracellular conductive proteinaceous appendages (pili,
membrane components, or “nanowires”). Large, multimeter-scale biogeobattery systems may commonly exist
where biomaterials and conductive minerals are coupled
together to enable long-distance electron transfer (Revil
et al. 2010).
Extracellular electron-transport processes also have technological applications—such as biological remediation, the
design of microbial fuel cells, and sensor development—
and implications for microbial community function across
redox gradients. There are also intensive efforts being made
to test when and where biogeobatteries are established in
natural systems. The self-potential anomalies detected by
Revil et al. (2010) were shown to be >100mV. Being able to
use geophysical methods to detect gradients in chemical
potential is a major technological advance for detecting
subsurface biogeochemical activity. Similarly, there is
intensive investigation into the microbially produced
materials that can serve as electrical conductors, into the
conditions that give rise to their expression, and into the
rates of electron transfer that can be sustained.
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A
HIGHLIGHT BOX:
LONG-DISTANCE E-TRANSFER
“Bacterial Nanowire” Extracellular
appendages that are 10s of nm wide
and at least 100× longer; electrically
conductive across their width and
length.
“Electron Shuttle” Compounds
that can be reduced and re-oxidized,
and thereby transfer electrons
between bacteria and extracellular
oxidants or reductants, including
solid minerals. Note: “phenazines”
discussed in the text can be an
electron shuttle; other common
examples include humic substances.
“Cable Bacteria” Filamentous
bacteria shown to be physically and
electrically connected over mm and
cm length scales; the first known
example is the sulfide-oxidizer
Desulfobulbacea.
“Biogeobattery” A system where
oxidizing and reducing zones are
connected through conductive
minerals and/or organisms and their
appendages or extracellular shuttles.
B
It is exciting to consider the environments that might harbor biogeobatteries or the microbial communities
that are electrically connected for
both energ y conservation and
signaling. The recently discovered
“cable-bacteria” are unlikely to be
the only organisms that are capable
of self-organizing in order to mediate
long-distance electron transfer in a
continuous fashion. It is possible that
such long-distance electron transport pathways might be important
for inducing subsurface, or hardrock, biogeochemical activity by
providing a pathway for electron flow
from reduced minerals (anodes) to
groundwaters that experience pulses
of oxidants (cathodes). Establishing
ionic and electrical gradients could
directly drive bedrock weathering via
the localized production of protons,
steep pH gradients, and incipient
hydration, alteration, and oxidation.
To better identify the extent of extracellular electron-transfer processes
in natural systems, we will need to
cultivate microbes that use minerals
and electrodes as electron donors
and acceptors. In turn, there are
great opportunities to discover previously unknown microorganisms and
reveal their mechanisms for element
cycling. Are there any reasons not
to expect such cell-to-cell and cellto-mineral electron transfer interactions in other biomes, including
the human body? In many ways,
the recent observations of intercellular electron transport should also
become integrated into comprehensive models of biofilm formation and
function.
Long-distance electron transfer can be mediated by
several different microbial pathways: bacterial
nanowires, electron shuttles, cable bacteria, and biogeobatteries.
ILLUSTRATIONS REPRODUCED WITH PERMISSION (COPYRIGHT © THOM G RAVES) FROM
EL-NAGGAR AND FINKEL (2013), "L IVE WIRES." THE SCIENTIST. HTTP ://WWW.
THE -SCIENTIST.COM /?ARTICLES .VIEW /ARTICLE N O /35299/TITLE /L IVE -WIRES / (A)
FIGURE 3
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Chains of bacteria encapsulated in “cables” oxidize hydrogen
sulfide in buried marine sediments and transmit the electrons to
oxygen dissolved in the upper sediments and porewaters. (B)
Individual bacteria can also transfer electrons to mineral surfaces
through chains of cytochromes embedded into conductive extracellular materials, or through diffusible extracellular electron carriers.
426
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GMG APPLIED
TO THE HUMAN BODY
The human body is a microbial biome ripe for investigation
by GMG approaches. Microorganisms inhabit the surface of
the human body and also intensively colonize numerous
environments within the human body, such as the mouth,
lungs, and gastrointestinal tract. Each of these microenvironments is difficult to characterize but each has unique
local chemical conditions (e.g. pH, pO2, metabolites, redox
homeostasis) that shape microbial community composition, function, metabolic status, and cell-to-cell interactions. These complexities suggest that GMG investigations
will become increasingly integrated into the health sciences
as efforts grow to understand the microbial role in normal
human physiology, to determine why systems go awry due
to changes in microbiota, and to understand how microbiological activity can change the materials in our body.
Although this is a vast topic, two examples provide great
illustrations of the interconnections between GMG and the
health sciences. First, scientists need a better understanding
of calcium phosphate formation. Geomicrobiologists
propose that bacteria are responsible for the accumulation
of large phosphorus deposits (phosphorites) in geological
systems (e.g. Cosmidis et al. 2013). These sedimentary
deposits were formed at specific geological periods and
represent a major sink in the global geochemical cycle of
phosphorus. Similarly, medical scientists have studied the
mechanisms of calcium phosphate formation by bacteria
(McLean et al. 1989). Some calculi, such as some kidney
or prostate stones or dental calculus, are indeed of microbial origin (Omelon et al. 2013). Infectious kidney stones,
which are composed of Ca-oxalates and Ca-phosphates,
have been shown to be associated with bacterial species
such as Escherichia coli, Klebsiella pneumonia, or Proteus
mirabilis. Ureolysis, which can induce pH increases, is
a metabolism that triggers Ca-phosphate precipitation
in kidneys; additional processes in the kidney, such as
phosphatase activity or proteins-involved in mineral nucleation, may also be important in precipitating Ca phosphate.
Interestingly, the same questions arise for the formation of
phosphorites: are there some microbial species that preferentially induce calcium phosphate formation? Are there
specific metabolic pathways and proteins with particular
nucleating properties that are involved?
A second topic where GMG and the health sciences overlap
is the critical role that Fe plays in sustaining growth and
microbial function in numerous environmental systems,
as well as in the human body. A focal area is the lung
environment of chronic cystic fibrosis patients, where
opportunistic pathogens, such as Pseudomonas aeruginosa,
establish biofi lms that are renowned for being highly
resistant to antimicrobial agents. Several studies from the
health sciences and GMG field have collectively found
that Fe-cycling pathways may be critical for P. aeruginosa
to function across diverse physiological and intrabody
environmental states, such as low-oxygen and low-iron
availability (e.g. Cornelis and Dingemans 2013). In particular, mechanistic studies, which focused on microbial
utilization and cycling of Fe from numerous pools in the
body (such as transferrin, heme, and ferritin) revealed two
overarching pathways of Fe acquisition. First, siderophoremediated complexation of Fe(III). Second, “secondary
metabolite” interactions with Fe, where molecules that
function as electron shuttles, such as phenazines, can
reduce Fe(III)-bearing cellular components to bioavailable
Fe2+ (aq) (Cornelis and Dingemans 2013).
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To better understand the roles of iron-cycling in the human
body, and because Fe availability is critical for P. aeruginosa biofi lm formation, numerous studies have explored
the interaction of high-affi nity Fe ligands, such as the
siderophores, with transferrin and heme (e.g. Banin et al.
2006). Recently, Dehner et al. (2013) also demonstrated
that P. aeruginosa can induce the dissolution of ferrihydrite
contained within ferritin, which allows this microbe to
acquire intracellular Fe through the activity of pyoverdin
and proteases. Separately, several recent works have also
shown how Fe can be acquired through siderophoreindependent pathways via the activity of microbially
produced reductants. For example, the phenazines that
regulate redox homeostasis can permit electron shuttling
and reduce the Fe(III) that is contained in proteins to Fe2+,
which is critical for maintaining Fe bioavailability (Wang
et al. 2011).
The growing body of literature on Fe-cycling in the lung
environment underscores how it will become critical to
disrupt biofi lms by targeting the availability of intracellular and extracellular Fe3+ and Fe2+ during chronic infection (Cornelis and Dingemans 2013). In turn, the insights
gleaned from such medical microbiology studies will
continue to shape our emerging views of how redox-active
small molecules may function in environmental biofilms in
terms of signaling agents, as well as how electron-shuttles
affect cellular redox homeostasis or Fe(III)-speciation.
MICROBIAL PRESERVATION
AND PALEOGEOBIOLOGY
With the realization that the rock record contains evidence
of microbial fossils from at least 3.5 Ga, the geobiology
community has made tremendous strides in understanding
early Earth history. In contrast to macroorganisms from the
Phanerozoic Era, fossil microorganisms leave different types
of physical and chemical signatures. These include characteristic sedimentary rocks (e.g. stromatolites), micrometer-sized chemical (e.g. isotopic) signatures in minerals,
minerals with specific shapes or sizes or pseudomorphs,
and fossil remnants of the microbial cells themselves.
Remarkably, it has been shown that very fi ne biological
details can be fossilized, even down to the subcellular level
(e.g. Li et al. 2013).
For geobiologists, the challenge consists in sampling rocks
from diverse ages and geological settings, obtaining the
least altered samples, and only then using analytical tools
that will provide data from the hand-scale down to the
nanometer-scale. However, the connection between geomicrobiology and paleontology goes beyond this search for
fossil microbes in the geological record. While there is a
dramatic bias towards the preservation of biomineralized
tissue, soft tissues, such as feathers, muscles, eyes or gills,
can be exquisitely preserved as well. This occurs in so-called
Konservatt-Lagerstätten, which are sedimentary deposits
containing exceptionally preserved fossils, including the
soft parts. Among the most emblematic Lagerstätten is the
Cambrian Burgess Shale of Yoho National Park, British
Columbia (Canada). These shales document the early
diversification of animals (the so-called “Cambrian explosion”). Another classic Lagerstätten is the Upper Jurassic
Solnhofen limestone of Germany, where preservation of
feathers helped to identify the fi rst discovered specimen of
Archaeopteryx. It was microbes that facilitated the preservation of the feathers in the fi rst place.
Microbial fossils are often associated with fossils of macroorganisms and, therefore, the microbiota often interpreted as facilitators of fossilization. This may come as
something of a surprise because one typically thinks of
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D ECEMBER 2015
microorganisms as destroyers of potential fossils because of
their tendencies to remineralize “dead meat.” Observations
from these settings have spawned an ongoing debate about
how microorganisms may facilitate fossilization of macroorganisms and have inspired experimental studies into the
fossilization process (Iniesto et al. 2013). First, microorganisms can colonize a dead body, feed on its tissues so
that the microbial cells eventually form a 3-D biofi lm,
and pseudomorph the original structures of the macroorganism. Alternatively, the formation of a microbial biofilm
at the surface of a dead macroorganism may also protect its
tissues from decay by blocking any downward diffusion of
oxidants. Finally, microorganisms can favor biomineralization, inducing the formation of a mineral layer enclosing
and protecting tissues from further degradation (FIG. 4).
Overall, a fossilizing animal can be seen as an interesting
geomicrobiological system (FIG. 4). The ultimate objective of GMG researchers is to describe the biogeochemical
processes that are occurring in such a system and why these
processes can result in partial or total loss of the original
organic matter that comprise the tissues of the animal.
Depending on the existing metabolic capabilities in the
microbial ecosystems, some molecules may or may not be
degraded. The microbial community that colonizes a dead
body is usually very diverse, phylogenetically and metabolically. Some microorganisms may favor degradation of the
biological structures, i.e. act as destroyers. Others may
preserve the structures and induce mineral precipitation.
But changes in environmental conditions and interspecies
interactions also impact on degradation and preservation
(Raff et al. 2014). There is, thus, a critical need to integrate
biogeochemical complexity at the micrometer-scale, to
understand microbial ecological interactions, and to fi nd
out how these systems are forced by external environmental changes. All this offers a tremendous and exciting
challenge for geomicrobiologists.
A remarkably wide diversity of mineral phases—apatite,
clay minerals, calcite, and silica—are associated with
exceptionally preserved fossils, as are anoxic conditions.
Yet, microbially catalyzed decay can also happen under
anoxic conditions, given that oxidants other than O2
may be present (Gaines et al. 2012). Oxygen fugacity was
not the major parameter controlling fossil preservation.
Instead, pH buffering of the environment may play an
even more important role. If a local environment does not
exchange much chemically (i.e. it becomes a closed system)
then pH variations and/or accumulation of elements may
favor mineral precipitation and, hence, the preservation
of biological structures (Briggs 2003).
A
B
D
F
H
I
C
E
G
Fossilization of macroorganisms by microbial mats.
Exceptionally preserved Early Cretaceous fossils from
Las Hoyas (near Cuenca, Spain) can be compared with laboratory
fossilization experiments (Iniesto et al. 2013). (A) Section of a fish
(Paracheirodon innesi) colonized by a microbial mat after 8 months
in the laboratory, representing entombment. (B) Magnetic
resonance image illustrating a slowdown in the decay of the fish’s
internal organs, including eye, muscles, and intestinal tract.
(C) Photograph showing a perfectly articulated fossil fish from Las
Hoyas; the fossilized equivalent of 4B. (D) Scanning electron microscope (SEM) image showing the surface of a fl y (Musca domestica)
as moulded by a microbial mat after 5.5 years in the laboratory.
(E) Photograph showing a fossil insect from Las Hoyas with imprints
FIGURE 4
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J
of the wings; the fossil equivalent of 4D. (F) SEM image showing
the pseudomorphism (replacement) of the eye of a fish by microbial
cells after 2 years of colonization in the laboratory. (G) Photograph
of a fish from Las Hoyas with an eye purportedly replaced by fossil
microbial cells; the fossil equivalent of 4F. (H) and (I) SEM image
and associated elemental map showing the bioprecipitation of a
Si-rich phase at the surface of a fish fossilized in the laboratory.
(J) Photograph of a fossil fish (Pelecanimimus) from Las Hoyas. The
fish throat (indicated by arrow) has been preserved due to the
lithification of a microbial mat; the fossil equivalent of 4H. Scale
bars are 0.5 cm for A, B, C, E, G and J; 100 μm for H and I; 10 μm
for D and F. A LL IMAGES BY M IGUEL INIESTO (U NIVERSITY OF MADRID).
428
D ECEMBER 2015
CONCLUDING REMARKS
The emerging conceptual frameworks that have derived
from GMG research on microbial diversity, activity, and
function, have revealed new interconnections between
microorganisms, Earth materials, and environmental
microenvironments. Microbial controls on the pervasive
fluxes of electrons and ions between biochemical systems,
minerals, and (bio)materials are emerging as focal areas
within geomicrobiology. New insights into large-scale
pathways of electron transfer and biomineralization are
leading to new models for how biogeochemical cycles
function and can be interlinked. We anticipate that GMG
approaches will become increasingly used in resource exploration and materials synthesis. Similarly, the convergence
between the processes observed in environmental systems
and the human microbiome are rapidly altering our understanding of how complex living systems function. Lastly,
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ACKNOWLEDGMENTS
The authors would like to thank Greg Druschel and Trish
Dove for their editorial contributions. We also gratefully
acknowledge support from the MATISSE Cluster of Excellence
(ANR-11-IDEX-0004-02); the NASA Astrobiology Institute
Cooperative Agreement NNA15BB02A (Templeton); and the
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