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Annu. Rev. Microbiol. 2009. 63:431–50
The Annual Review of Microbiology is online at
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This article’s doi:
10.1146/annurev.micro.091208.073349
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Atmosphere-Rock Interface:
How Biological Interactions
and Physical Stresses
Modulate a Sophisticated
Microbial Ecosystem
Anna A. Gorbushina1,2,3 and William J. Broughton3
1
Department IV—Materials and Environment, BAM (Federal Institute for Material
Research & Testing), D-12205 Berlin, Germany; email: anna.gorbushina@bam.de
2
Faculties of Biology, Chemistry and Pharmacy & Geosciences, Free University
of Berlin, D-14195 Berlin, Germany
3
LBMPS Sciences III, University of Geneva, 1211 Geneva, Switzerland
Key Words
cyanobacteria, geobiology, microcolonial fungi, rock inhabiting
fungi-phototroph symbioses, soil formation, subaerial biofilms,
weathering
Abstract
Life at the atmosphere-lithosphere boundary is an ancient terrestrial
niche that is sparsely covered by thin subaerial biofilms. The microbial
inhabitants of these biofilms (a) have adapted to all types of terrestrial/
subaerial stresses (e.g., desiccation, extreme temperatures, low nutrient
availability, intense solar radiation), (b) interact with minerals that serve
as both a dwelling and a source of mineral nutrients, and (c) provoke
weathering of rocks and soil formation. Subaerial communities com-
prise heterotrophic and phototrophic microorganisms that support each
other’s lifestyle. Major lineages of eubacteria associated with the early
colonization of land (e.g., Actinobacteria, Cyanobacteria) are present
in these habitats along with eukaryotes such as microscopic green algae
and ascomycetous fungi. The subaerial biofilm inhabitants have adapted
to desiccation, solar radiation, and other environmental challenges by
developing protective, melanized cell walls, assuming microcolonial ar-
chitectures and symbiotic lifestyles. How these changes occurred, their
significance in soil formation, and their potential as markers of climate
change are discussed below.
431
 ANRV387-MI63-21 ARI 6 August 2009 8:30

these inhospitable surfaces (20). Major groups

Contents of microorganisms that are associated with
the colonization of land (Eubacteria including
INTRODUCTION . . . . . . . . . . . . . . . . . . 432
the phyla Actinobacteria, Cyanobacteria, and
WHEREVER YOU LOOK
Firmicutes early in evolution, and fungi for the
YOU WILL FIND A SUBAERIAL
last 0.5 Ga) are present in these habitats. Even
BIOFILM . . . . . . . . . . . . . . . . . . . . . . . . . 432
today, freshly exposed solid surfaces are rapidly
ROCK BIOFILMS: MINIATURE
colonized by subaerial biofilms (SABs) com-
WORLDS BETWEEN THE
posed of both heterotrophic and phototrophic
LITHOSPHERE AND
partners. Interconnected microbial communi-
THE ATMOSPHERE . . . . . . . . . . . . . 434
ties within SABs withstand physical stresses, in-
SUBAERIAL BIOFILMS
teract with the underlying substrate as well as
AND WEATHERING . . . . . . . . . . . . 437
the atmosphere, and support each other. Here
SYSTEMS BIOLOGY: CHANGING
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

we examine the evidence for (a) mechanisms

PERSPECTIVES . . . . . . . . . . . . . . . . . 437
of SAB persistence (i.e., the manifest ways in
FORTRESS-LIKE
which SAB inhabitants meet the biological and
MORPHOLOGIES AND
by University of Zaragoza on 04/01/13. For personal use only.

physical challenges), (b) biological interactions

SUBAERIAL BIOFILM
between heterotrophic and phototrophic in-
PERSISTENCE . . . . . . . . . . . . . . . . . . . 440
habitants of rock biofilms, and (c) reciprocity
Microcolonial Growth Patterns . . . . . 440
between atmosphere, SAB, and rock. We also
MCF Oligotrophy . . . . . . . . . . . . . . . . . 440
discuss ways of dissecting these interactions at
SYMBIOTIC PLAYGROUNDS . . . . . . 441
the molecular level, as well as approaching this
OTHER ASPECTS OF SUBAERIAL
system as a complex entity.
BIOFILM BIOLOGY . . . . . . . . . . . . . 443

WHEREVER YOU LOOK

YOU WILL FIND A SUBAERIAL
INTRODUCTION BIOFILM
Ga: billion years
Atmosphere-rock interfaces are omnipresent Life on rocks occurs everywhere—a thin
Subaerial biofilms
(SABs): largely self-
and occur at all scales—from planetary to mi- network-like microbial film is present on all ob-
sufficient miniature croscopic. Life at the atmosphere-lithosphere jects exposed to the air (Figure 1). The ease
microbial ecosystems boundary is an ancient terrestrial niche. with which SABs can be seen and the way
that develop on Microorganisms in the form of biofilms and they look vary with the microbial composi-
atmosphere-exposed microbial mats, not unlike modern desert or in- tion of the SAB in question, which in turn de-
solid surfaces
tertidal systems, were among the first settlers of pends on climatic conditions, the nature of the

−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 1
Diversity of rock biofilms. (a) The Erechtheum Temple in Athens, Greece, serves as an example of how
long-term subaerial exposure (421 BCE) changes the general appearance of the white marble. Biological
growth and atmospheric deposition cause yellowish patination, while the newer, replacement blocks of
marble (twentieth century, present era) from the same quarry are still white. (b) An outside wall of the New
Pinakothek museum in Munich, Germany (exposed to the atmosphere since 1981), carries well-developed
subaerial biofilms (SABs) comprising green algae, fungi, and lichens. The mild climatic conditions and
constant water supply have stimulated growth in the areas exposed to rain. (c) Under the scorching South
Australian sun, these SABs in Pildappa, Minipa, have developed on a hard Archaean granite surface.
Accumulation of biomass is apparent on the vertical surfaces but, given the extremely unfavorable conditions,
has not resulted in obvious soil formation. (d ) A toxic atmosphere (sulfur vapors from volcanic activity)
presents an additional stress to these SABs growing on a sandstone monument in Rotorua, New Zealand.
The orange color is probably caused by protective pigments (carotenoids) in green algae.

432 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30

substrate, as well as how long the surface has monuments, and building surfaces in all cli-
been exposed to air. Studies have been con- matic zones (13, 21, 25, 34, 41, 60, 75, 81, 84,
ducted on SABs of rocky substrates in hot 85, 101, 103, 106, 114, 120). Multiple exam-
deserts, polar regions, high mountains, ancient ples of geographically distinct SABs are shown

a b
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c d

www.annualreviews.org • Life at the Atmosphere-Rock Interface 433

 ANRV387-MI63-21 ARI 6 August 2009 8:30
in Figure 1. In one example, marble blocks
that form part of the Erechtheum Temple in
Athens, Greece, that have been exposed to the
Black yeasts: a group
of imperfect fungi of atmosphere since they were erected are much
ascomycete affinity more yellow than blocks that were replaced dur-
that have dark ing a recent restoration (Figure 1a). This yel-
pigments and blastic lowish patination, which is characteristic of the
conidiogenesis
dry Mediterranean climate, is mainly caused
Microcolonial fungi by subaerial growth of pigmented microcolo-
(MCF): peculiar
nial fungi (MCF) and heterotrophic bacteria
ascomycetes that
inhabit bare rock (27, 48, 71, 112, 116, 117). Atmospheric de-
surfaces and possess a position of discoloring pollutants only plays a
number of specific minor role. Sandstone of the New Pinakothek
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
morphological and museum in Munich, Germany, which has been
physiological
exposed to a more humid, milder climate for
characters (see also
black yeasts) about two decades, still presents distinct, thick
by University of Zaragoza on 04/01/13. For personal use only.
biofilms of green algae, fungi, accompanying
bacteria, and even lichens (Figure 1b). A late
Archaean granite outcrop in South Australia
is one of the most ancient terrestrial subaerial
rock surfaces, and the growth of Tintenstrich
(“ink streak”) biofilms (contemporary and dom-
inated by cyanobacteria and MCF) on its sur-
face is spectacular (Figure 1c). Under these
conditions of intense solar radiation and ex-
treme temperature fluctuations, the biomass of
SAB is much more restricted than in North-
ern Europe, but the principal components of
the subaerial community remain the same—
stress-tolerant phototrophs, heterotrophs, and
lithotrophs. A sandstone monument in Rotorua
(New Zealand) that has been exposed since
1927 to a humid climate and toxic sulfur va-
pors resulting from volcanic activity in the
area has spectacular blooms of red-pigmented
subaerial algae, as well as bacteria and fungi
(Figure 1d ). These examples show that even
though local conditions demand certain varia-
tions, SABs are built using the same basic types
of blocks—autotrophic algae or photosynthetic
bacteria, heterotrophic bacteria, and fungi.
SABs frequently discolor the surfaces on
which they grow. This discoloration may
or may not be obvious to the naked eye
(Figure 1b–d ) and is due to pigments (69, 71)
that are either necessary for primary produc-
tion (chlorophyll of rock-inhabiting prokary-
otic and eukaryotic phototrophs) or provide
434 Gorbushina · Broughton
protection from the environment (carotenoids
of heterotrophic and phototrophic bacteria, as
well as green algae, melanins of actinobacte-
ria, and fungi). Pigments in SAB inhabitants
help protect the cells against UV radiation
especially, but they also guard against desicca-
tion and temperature stresses. Life on rocks ex-
posed to the atmosphere contrasts sharply to
that found under water or in soil, with the main
differences rooted in much harsher and more
variable environmental conditions. The ther-
mal buffering capacity of air is orders of mag-
nitude lower than that of water or soil, and for
this reason temperature fluctuations are a pri-
mary stress factor in SAB communities. Lack of
a radiation shield as well as huge fluctuations in
the availability of water add to the list of envi-
ronmental constraints that restrict survival and
growth of SABs. In arid environments, dew, fog,
and sparse rain are the only sources of humid-
ity, but some rock-inhabiting microorganisms
can directly capture water vapor from the air
(88). Even then, extreme temperatures acceler-
ate water loss through evaporation or freezing.
ROCK BIOFILMS: MINIATURE
WORLDS BETWEEN THE
LITHOSPHERE AND
THE ATMOSPHERE
SABs are sandwiched between the atmosphere
and the mineral substrate. As a result, they inter-
act directly with both. The atmospheric phase is
highly mobile and has changed greatly over the
course of evolution (68). Rocks, on the other
hand, are much more stable surface environ-
ments that harbor low-temperature geochem-
istry as well as major metabolic processes in di-
verse microorganisms.
Life began early in Earth’s history, perhaps
before 3.8 billion years ago (Ga), and achieved
remarkable levels of metabolic sophistica-
tion before the end of the Archaean around
2.5 Ga (26). Life on Earth is dependent on
unbalanced cycles of electron transfers, mostly
involving six elements: carbon, hydrogen,
nitrogen, oxygen, phosphorus, and sulfur.
Metabolic pathways evolved through
 ANRV387-MI63-21 ARI 6 August 2009 8:30
opportunity and selection, forming an interde-
pendent, planetary pool where reductants and
oxidants could flow freely around the world.
Gases, produced by all organisms and geolog-
ical processes, are transported around Earth’s
surface by the atmosphere and oceans (31).
Photosynthesis, the only sustainable source
of biologically generated energy on the planet,
is an ancient terrestrial process (82). Reduced
sulfur compounds were probably the first elec-
tron donors for CO2 fixation (83), but other
low-potential electron donors such as hydro-
gen and Fe2+ were also important fuels for an-
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
cient primary production. Of these, Fe2+ may
well have been the most abundant. Because
Fe2+ has an intermediate redox potential rela-
by University of Zaragoza on 04/01/13. For personal use only.
tive to other electron donors used in photosyn-
thesis, Fe2+ phototrophy may represent a tran-
sitional form of photosynthetic metabolism.
Variation in the DNA sequences of genes in-
volved in Mg-tetrapyrrole synthesis indicates
that most anoxygenic photosynthetic organisms
are ancestral to oxygen-evolving cyanobacte-
ria. In fact, the purple bacterial lineage may
contain the most ancient form of this pigment
biosynthesis pathway (124). As the environment
gradually became more oxidizing, evolutionary
pressures to utilize ever weaker electron donors
grew, resulting in the recruitment of a second
photosystem (PSII) that works in series with
PSI to ensure linear photosynthetic electron
flow. Atmospheric oxygen levels slowly began
to increase around 2.5 Ga (8). PSII utilizes elec-
tron donors weaker than those utilized by PSI
(82). The manganese cofactor of PSII enabled
cells to produce molecular oxygen (O2 ) from
water and thereby oxidize our planet. Indirect
evidence shows that oxygenic photosynthesis
had evolved approximately 3 Ga (16), and geo-
chemical data suggest that between ∼2.3 and
2.2 Ga there was sufficient oxygen in the atmo-
sphere to permit an ozone layer to form (31).
Although many organisms retreated to
anoxic environments (such as deeper layers
of sediments or inner parts of the continen-
tal crust), others evolved to use oxygen as a
high-potential redox couple while concomi-
tantly mitigating its toxicity (94). Over the next
1.5 billion years, the oxidation of the atmo-
sphere and, ultimately oceans, depleted Earth’s
surface of many reductants that were abundant
PS: photosystem
in the first half of our planet’s history. Most
Protective pigments:
of the anaerobic machinery in these organ-
secondary metabolites
isms was corralled by the oxidizing conditions that protect rock-
into relatively small, fragile, hypoxic or anaero- inhabiting MCF
bic reserves (31). Increasing O2 levels are cou- Microbial
pled with metabolic organization more complex hitchhikers:
than that achievable by any anoxic network, and microbes that travel
the adaptation to an oxygen-rich atmosphere across continents by
attaching to mineral
helped drive the development of multicellular
particles serving as
life (94). SAB too made a complete transition to transport vehicles
the aerobic way of life at about this time. The
increased oxygen and therefore ozone (O3 ) lev-
els also had a protective effect in blocking short-
wave solar radiation and thus facilitating growth
at the rock interface.
Initially, SABs were trapped by the increas-
ing oxygen levels. Their anchors were in niches
that could at least partly avoid the toxicity of
O2 and its derivatives (including superoxide
and hydroxyl radicals), while the more exposed
portions could either modify their metabolic
machinery to permit coupling the oxidation of
organic matter to the reduction of O2 to wa-
ter or form symbiotic associations. As multi-
cellular organisms developed, the atmospheric
load of particulate matter and volatiles also
arose, expanding the physical and chemical con-
straints on SAB growth. New opportunities
arose and biofilms within SAB responded by,
for example, producing more protective pig-
ments (e.g., against sulfur vapors, as shown in
Figure 1d ).
Most particles suspended in the atmosphere,
including microbial cells, will eventually fall
out, some on rocks. Changing atmospheric con-
ditions thus drove evolution of SAB in two
ways: The increased O2 levels forced inter-
nal changes in SAB communities, and at the
same time microbes that had evolved elsewhere
fell upon them. Some SAB communities were
seeded with algae and cyanobacteria (both pos-
sess the more efficient PSII) and outcompeted
their predecessors. In similar ways, fungi en-
tered SAB communities along with aerobic
bacteria. As SABs live in poorly buffered
www.annualreviews.org • Life at the Atmosphere-Rock Interface 435
 ANRV387-MI63-21
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ARI 6 August 2009 8:30
environments, the resulting communities are
restricted in both diversity and biomass (43, 72,
119, and references therein).
Atmospheric activity also contributes to the
cosmopolitan nature of SAB. Winds erode sur-
faces to which SAB are attached and carry them
to other niches. In this sense, winds are im-
portant agents of transport and erosion, espe-
cially in arid areas whether hot or cold (53). It
is precisely in these environments that SABs, as
a proportion of total biomass, are particularly
prominent. Small fragments of substrate along
with biofilms are picked up from the surface and
transported across continents and oceans (45).
Each year, tens of millions of metric tons of dust
from African deserts are blown northward and
westward to the Americas and Europe (12, 38,
54, 55, 66). Microbes attach to these fine par-
ticles and hitchhike around the globe (45). Al-
gae, bacteria, lichens, and fungi are distributed
globally in this way.
Given the difficulties of surviving in niches
that are poorly buffered, completely bathed in
air with solar radiation on one surface, but pro-
tected from light on the other, SABs are in-
herently well prepared for the stresses of inter-
continental travel and survival. Multiple lines
of evidence, including the cosmopolitan distri-
bution of rock settlers, support this theoreti-
cal basis: (a) Colonization patterns of freshly
quarried stone vary little around the world
(69, 118), (b) biogeographic and phylogenetic
studies of rock-inhabiting microbes show that
they are similar on different continents (13,
30, 34, 59, 99), and (c) metagenomic compar-
isons reveal few differences between the en-
dolithic microbial communities of Antarctica
and North America (119). Studies of SABs in
different climates will provide insights into how
they have adapted to different niches and how
they have evolved. Because much of the re-
cent progress in biology can be attributed to
the detailed analyses of model systems, devel-
opment of a tractable laboratory SAB system
will make it easier to study how the composi-
tion of the atmosphere, different temperature
regimes, and various substrata help shape SAB
communities.
436 Gorbushina · Broughton
As a result of the physical constraints
discussed above, SAB growth is sporadic in
many environments. Nevertheless, strategically
placed biofilms are always ready to assimilate
particulate matter. In a real sense, airborne
sources of carbohydrates, proteins, and essen-
tial elements control the development of these
nutrient-limited communities. In almost every
instance, energy supplied to SAB communi-
ties is external (from the atmosphere) rather
than internal (from rocks). For example, some
desert endolithic ecosystems receive consid-
erable nitrogen inputs from the atmosphere
in the form of precipitation and dust (81).
Even though these inputs vary significantly,
SAB can compensate for the lack of nitro-
gen by closely associating with diazotrophic
cyanobacteria. Furthermore, many rock set-
tlers catabolize even aromatic hydrocarbons
and other organics from rain or polluted air (78,
92, 100).
Rocks are both substrates and dwellings,
especially when SABs invade internal, pro-
tective niches (e.g., cracks, fissures, flakes).
Rock-inhabiting microorganisms spread over
a complex spatial pattern of mineral grains,
cementing material, pores, and fissures in ways
that are specific to each group of dwellers.
For example, fungal hyphae penetrate the sub-
strate, while algae, bacteria, and yeast-like fungi
cluster to form compact microcolonies (43)
(Figure 2). In long-established SABs [e.g., in
Antarctica, on monuments of the Acropolis
and Angkor Wat (Figure 2), and in deserts],
biofilm communities have crept into deeper
layers of the substrate and offered themselves
an endolithic niche in which the environmental
extremes are better buffered (25, 34, 119). This
ability to penetrate between mineral grains
is guided in part by the search for milder
(better-buffered) conditions that are available
in intergranular spaces and by thigmotropism
(the capacity to grow in contact with surfaces).
On materials that are more resistant to wear,
depressions around colonies are usually less
profound (Figure 2b). Endolithic SABs escape
from the atmosphere-induced terrestrial
stresses (desiccation, radiation, osmotic stress)
 ANRV387-MI63-21 ARI 6 August 2009 8:30
(Figure 2c) and hibernate for long periods.
Small cracks and fissures offer water reservoirs,
where surface tension slows evaporation. De
novo formed minerals and protective pigments
are usually deposited at the air-rock interface
(14, 15, 35, 109, 117). Protective extracellular
polymeric substances (EPSs) in SABs facilitate
this deposition, and in this way additional
protective layers covering the entire biofilm
are formed (43). Similar processes catalyze the
accumulation of airborne particles of diverse
origin and chemistry. Once fixed to the rock
surface and/or SAB matrix in this way, airborne
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
particles may also contribute to color change
in the ancient monuments.
Solid terrestrial surfaces are the stable phase
by University of Zaragoza on 04/01/13. For personal use only.
in complex tripartite interactions between at-
mosphere, lithosphere, and biofilm, but rocks
vary greatly in their geochemistry. All rock
types, from carbonates such as marble to sil-
icates such as quartz, are colonized by SABs.
On some rock surfaces, the presence of SABs
is more obvious because of the color contrast
(Figure 2a). SABs are easily seen on white mar-
ble surfaces, for example (71). The texture and
different crystalline structures within granitic,
sedimentary, and metamorphic rocks affect the
development of SABs. Furthermore, the chem-
ical composition of mineral surfaces (e.g., gran-
ite is composed of feldspars, mica, and quartz
grains) can be diverse and varies with the de-
gree of weathering and the age of coloniza-
tion. Although the first attempts to correlate
mineral composition with the makeup of SAB
communities were made more than fifty years
ago (57), little progress has been made since
then and such studies are still rare (62). In soils,
the structure of bacterial communities corre-
lates with the mineral composition of the sub-
strate (1, 17). When given the choice between
feldspars and quartz, mycorrhizal fungi prefer-
entially colonize the nutrient-rich feldspar (98).
Nevertheless, correlations exist between the
presence of individual nutrients and both bacte-
rial and fungal communities. Microbial settlers
on different mineral grains from weathered
granite preferred certain elements above others
(39, 40).
The fact that SABs form thin networks or
films between the atmosphere and lithosphere
means that the constituent microorganisms are
EPS: extracellular
in close contact with one another. SAB ma- polymeric substance
trices actively participate in interorganism in-
teractions and also facilitate adhesion to, and
chemical interactions with, the underlying rock
surface (43, 67). Organisms and their extracel-
lular substances accelerate leaching of nutri-
ents from the underlying rocks (weathering),
which in turn stimulates growth of SABs in gen-
eral and autotrophic microbes such as algae and
cyanobacteria in particular (102).
SUBAERIAL BIOFILMS
AND WEATHERING
SABs occupy significant portions of terres-
trial rock surfaces (47), actively participating
in weathering and soil formation in numerous
ecosystems. Formation of mineral soils always
involves a rock biofilm stage. The combined ac-
tivity of SAB increases the surface area of rocks,
causing changes to the surface, separation of
grains, as well as accumulation of airborne or-
ganic and mineral compounds (35, 43, 75). Un-
restricted access to air means that SABs are well
placed to mediate all atmosphere-lithosphere
interactions. As a consequence, SABs have con-
siderable influence over geochemical processes
at the atmosphere-lithosphere interface (4).
SYSTEMS BIOLOGY: CHANGING
PERSPECTIVES
The metabolic diversity of today’s SABs re-
flects the accumulated evolutionary response
to the subaerial environment over ∼2.5 Ga
since their ancestors first inhabited our planet
(121). During this time, evolution has formed
rock-inhabiting microbes that capture solar,
atmosphere-derived, and mineral-derived en-
ergy sources. SABs inhabit the upper portion
of the lithosphere, and their communities are
as diverse as the climatic conditions in which
they grow (Figures 1 and 2). Nevertheless, the
inhabitants of each community vary little in
form and function.
www.annualreviews.org • Life at the Atmosphere-Rock Interface 437
 ANRV387-MI63-21 ARI 6 August 2009 8:30

SABs have been studied for almost five their expeditions (23, 61, 89). Yet our views of
hundred years. Naturalists including Paracel- SABs have changed with time. At first, SAB in-
sus, von Humboldt, and Darwin described the habitants were treated as single groups and not
growth of thin films on mineral outcrops during as interacting microorganisms. It was widely

a b
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
by University of Zaragoza on 04/01/13. For personal use only.

5 mm 2 µm

c d

100 µm 1 mm

e f

300 µm 30 µm

438 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30

believed that colonization was driven either by
oxygenic photosynthesis or by chemolithoau-
totrophy. Lithotrophic bacteria (e.g., thiobacilli
or nitrifying bacteria), which derive energy
from inorganic compounds, were repeatedly
described as energy providers for life on the
rocks (10, 57, 63, 74, 80, 105). At the same time,
phototrophs such as algae (including lichens)
and cyanobacteria were thought to dominate
rock-inhabiting communities (3, 64, 104). In
fact, these were rational expectations of olig-
otrophic communities living at the atmosphere-
rock interface where atmospheric CO2 and
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
requirements of the heterotrophic inhabitants
are low and can be provided by airborne
particulates and volatiles (78, 82, 99) and
metabolites of phototrophic organisms (11,
44), as well as by the excreta and remains of
biofilm-associated animals (51). Frequently,
however, specialized heterotrophic fungi
and heterotrophic bacteria are the primary
colonizers of SABs, especially when airborne
organic sources are abundant (19, 114, 118) or
when the main requirement for survival is high
tolerance to environmental stresses (106).
Culture-independent methods suggest that

energy from either solar radiation or inorganic algae and bacteria (including actinobacteria and
compounds were the only feasible inputs. Yet cyanobacteria), as well as micromycetes, are
many phototrophs and lithotrophs need more the primary colonizers of newly exposed ter-
by University of Zaragoza on 04/01/13. For personal use only.

protection from solar radiation and/or the
atmosphere to flourish, and for this reason
they are rarely pioneers or the only settlers in
SAB communities.
We now know that the situation is much
more complex. Beijerinck’s laws “everything
is everywhere” but “the environment selects”
(93) have a long geobiological tradition (2,
32). SAB communities also contain diverse
and important heterotrophic components (43).
Fungi, often called ecological opportunists (37,
115), dominate and, along with heterotrophic
bacteria, were reported in early observations
on weathered rocks (3, 57, 86). Since growth is
often restricted on solid surfaces, the nutrient
restrial surfaces (42, 76, 84, 103, 119). After-
ward, secondary inhabitants including lichens,
mosses, and climbing plants, as well as small
animals that feed on the biofilms or propa-
gate on and in rock crevices, settle in SAB
communities. Biomass production accelerates
with each new arrival until an equilibrium
is attained in which the inputs of energy
match the community’s demands. Three-
dimensional structures result (Figure 2). Un-
derstanding SAB development requires that
knowledge of all components—aerobic het-
erotrophs, lithotrophs, oxygenic phototrophs,
and even heterotrophic phagotrophs—be con-
sidered (35, 43).

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure 2
Enlarged views of subaerial rock biofilms. (a) Fungal and lichen growth on a marble surface exposed to the
atmosphere for 100 years. As this vertical marble tombstone in the Australian desert is dated, it was possible to
determine the exact age of the subaerial rock biofilms. (b) Single fungal microcolonies on a quartzite surface
from the Atacama Desert (desert pebbles in the vicinity of La Silla, Chile). Macroscopic fungi are dominant,
but accompanying organisms such as bacteria are always present. (c) Cross-section through a marble block
from the Philopappos Monument in Athens, Greece, from which Sarcinomyces petricola strain A95 was isolated.
The upper (epilithic) part of the colony is to the left, while the endolithic structures anchor the colonies to the
grains. Note the spaces around the endolithic colonies—marble as calcium carbonate is easily leached by even
weak acids such as carbonic acid. (d ) Microcolonies on a granite surface from Pildappa, South Australia (see
also Figure 1c), belong to a complex community including microcolonial fungi and cyanobacteria. Though
morphologically similar, these organisms demonstrate a convergent evolution caused by growth under
demanding conditions. (e, f ) Biofilms on sandstone from Angkor Wat (Cambodia) grow in a humid and warm
climate. Under these mild conditions, thicker, more luxuriant biofilms accumulate considerable biomass.
Filamentous cyanobacteria are spectacular under these conditions. ( f ) Magnified view of (e) showing
contacts between organisms and the rock surface with traces of biogenic etching typical of SAB formation.

www.annualreviews.org • Life at the Atmosphere-Rock Interface 439

 ANRV387-MI63-21 ARI 6 August 2009 8:30

FORTRESS-LIKE colonial growth both on the rock surface and in

MORPHOLOGIES AND culture (52, 106). Even in extremely arid con-
Chaetothyriales and
SUBAERIAL BIOFILM ditions like varnished surfaces in hot deserts
Verrucariales: two PERSISTENCE where lichens and other SAB inhabitants have
closely related surrendered to the environment, melanized
Rock surfaces are unique terrestrial habitats
ascomycete orders fungal microcolonies still grow directly on the
that challenge their settlers to the extreme.
from the class rock surface (106) (Figure 2b).
Eurotiomycetes Widely varying temperatures and water sup-
plies, along with intrusive solar radiation and
restricted nutrient availability, have biased se- MCF Oligotrophy
lection toward survival. These nonspecific,
The ability to rely exclusively on sparse, air-
diverse stresses shape a universal response
borne, low-molecular-weight nutrients (olig-
sometimes referred to as poikilo-tolerance
otrophism) contributes to the amazing survival
( poikilos, “diverse,” “irregular,” or “variable”).
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

capabilities of MCF. Yet in culture MCF grow

A highly specialized but diverse group of
well on complex media and in this sense are
melanized, poikilo-tolerant MCF (106) are
not typical oligotrophs. The evolution of MCF
among the most persistent settlers of bare rocks.
by University of Zaragoza on 04/01/13. For personal use only.

into a heavily protected poikilo-tolerant mi-

These rock-inhabiting ascomycetes are micro-
crocolonial form followed a convergent pat-
scopic, relatively inconspicuous (Figure 2b,c),
tern. The free-living rock-inhabiting lifestyle
and have been frequently overlooked (59). First
evolved in two classes of ascomycetes—the
discovered in extreme rock environments of hot
Dothideomycetes and the Eurotiomycetes (99,
deserts (70, 106) and in Antarctica (33), these
108, 109). Gueidan et al. (59) used multigene
nonlichenized fungi were later shown to persis-
analyses to study the phylogenetic relation-
tently colonize rock surfaces under more tem-
ships of eurotiomycetous ascomycetes isolated
perate climates (113, 123). Largely owing to the
from a variety of substrates at different geo-
absence of competition and to their poikilo-
graphical locations. Free-living rock-dwellers
tolerance, MCF thrive in semiarid and arid
are spread among the early, diverging lineages
habitats (87, 99, 107).
of two fungal orders with strikingly differ-
A high proportion of fungal biomass is
ent lifestyles: Chaetothyriales and Verrucari-
melanized in the natural environment (35), and
ales (both Eurotiomycetes). Verrucariales are
melanized fungi play a key role in establish-
mostly lichen-forming fungi (58), while the
ment and development of SABs. Melanization
Chaetothyriales are best known as opportunis-
(Figure 2b,c) protects MCF from solar radia-
tic pathogens of vertebrates (24, 122). Gueidan
tion and also against extreme temperatures and
et al. (59) suggest that the completely lichenized
desiccation. Other protective UV-absorbing
Verrucariales probably evolved from free-living
pigments with high antioxidant potential,
MCF on rock surfaces. A variety of rock-
such as carotenoids and mycosporines, are
inhabiting MCF are also present in the early-
also present in this peculiar ecological group
diverging lineages of pathogenic Chaetothyri-
(46, 52).
ales, which use melanization and microcolonial
growth patterns as stress-tolerance mechanisms
Microcolonial Growth Patterns (59).
The production of internal asexual spores Rock-dwelling SABs played an important
and their typical isodiametric (meristematic) role in the evolution of terrestrial life. A major
growth form minimizes the surface/volume ra- role for terrestrial bacteria in metabolic evolu-
tio (and thus desiccation losses) of cells and tion has been proposed (7), suggesting that the
colonies (123) and confers the ability to sur- terrestrial lifestyle on rocks and in soils possi-
vive extreme drought (46). These ascomycetes bly drove the evolution of many metabolic pro-
maintain protective pigmentation and micro- cesses. Life on rocks preceded the development

440 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30
of soil ecosystems and probably dates to
∼2.5 Ga (121). Because one eubacterial clade
(6, 7) has diverged from the other clades dur-
ing the colonization of land, it is possible
that the evolution of Terrabacteria (including
actinobacteria and cyanobacteria) occurred in
terrestrial environments similar to those found
containing SABs.
Similarly, the atmosphere-rock interface
drove important aspects of ascomycete evo-
lution. Most likely, the common ancestor of
both lichenized Verrucariales and pathogenic
Chaetothyriales was nonlichenized and dwelled
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
on rocks (59). As with present-day rock-
inhabiting fungi, this ancestor was proba-
bly microcolonial and melanized, characters
by University of Zaragoza on 04/01/13. For personal use only.
that ward off general stresses (e.g., desicca-
tion, temperature, pH, radiation). If growth at
the atmosphere-rock interface was ancestral to
such diverse lifestyles as lichen symbioses and
pathogenicity, it supports our hypothesis that
primordial terrestrial habitats played an impor-
tant role in the evolution of life. This hypoth-
esis is supported by the idea that fungi played
a leading role in the evolution of terrestrial life
(9). In other words, the multiple and varying
stresses inherent to atmosphere-rock interfaces
have shaped the morphological and physiolog-
ical evolution of ascomycetes and have enabled
their descendants to colonize various substrates
and lead different lifestyles that range from par-
asitism to symbiosis.
Different SAB-dwelling species and taxa
are similar or identical in appearance, with
simplified morphology and reduced size both
in situ (106) and in vitro (110). MCF are
protected by restricted radial expansion and
recolonization of old cells by new ones inside a
semiclosed fortress where accumulated storage
compounds may be reused by a new genera-
tion of cells (52). Similar thermodynamically
advantageous and protected colony forms are
observed in rock-inhabiting actinobacteria
(Geodermatophilus; 29), cyanobacteria (Chroococ-
cidiopsis, Gloeocapsa; 13, 49), and green algae
(sarcinoid colonies of Apatococcus, Desmococcus,
Pleurococcus, Protococcus; 73, 97) (Figure 2d ).
These morphological similarities have led to
the erroneous description of some MCF as
cyanobacteria (22).
Indeed, a typical rock-inhabiting microor-
ganism survives as vegetative cells or tissue-
like structures for long periods without wasting
energy on spore formation, production of
propagules, or other means of escaping vari-
able environmental conditions. SAB survival
strategies encompass the creation of protective
microenvironments at the individual organism
level (43) (see Microcolonial Growth Patterns,
above). Furthermore, in their search for more
protective and perhaps nutrient-rich environ-
ments, SABs bore into and fracture rocks (25,
28, 111). Substrates are more effectively colo-
nized this way, and the growth between gran-
ules of rocks eventually leads to the separation
of grains and weathering.
Crusts offer SABs protection from the en-
vironment and are formed by (a) the accumu-
lation and agglutination of airborne particles
to the biofilm matrix, (b) deposition of minerals
that coat the biofilm (14, 15, 35), and (c) pigment
production by the biofilm (50). An example of
a poorly structured but nevertheless protective
crust of this type, growing on the upper surface
of marble and neighboring an epilithic colony,
is shown in Figure 2c. Finally, close and coordi-
nated juxtaposition of different SAB inhabitants
leads to protection of the community.
SYMBIOTIC PLAYGROUNDS
Inhabitants of SAB communities are in close
contact with one another. Heterotrophs,
lithotrophs, and phototrophs grow in thin films
that develop into associations that resemble
symbioses. Indeed, life within a SAB commu-
nity resembles a symbiotic playground. Vital
biofilm connections at the atmosphere-rock in-
terface are stimulated by the massive physi-
cal and nutritional stresses that all members
have to bear. In such an ecosystem, antibiosis
is counterproductive and rare (34). A simple
way to solve the evolutionary necessity of hav-
ing to adapt to terrestrial stresses or nutrient
deficiencies is to form symbiotic associations
between photosynthetic and heterotrophic
www.annualreviews.org • Life at the Atmosphere-Rock Interface 441
 ANRV387-MI63-21 ARI 6 August 2009 8:30

organisms. As mentioned above, a possi-
ble ancestor of lichenized ascomycetes (order
Verrucariales) probably dwelled on rock sur-
faces and was nonlichenized (59). Free-living
rock-inhabiting MCF easily grow with green
algae (44) and cyanobacteria (A.A. Gorbushina,
F. Cavat, J. Favet, R. Kort, C. Reisner,
Z. Saci & W.J. Broughton, manuscript in
preparation) (Figure 3). The capacity for en-
dolithic growth makes rock-inhabiting MCF
(28, 111) attractive partners to less-protected
phototrophs that enter the endolithic niche.
The remarkable survival abilities of SABs
are boosted by contacts and metabolic in-
teractions between rock-inhabiting fungi and
phototrophs.

a b
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
by University of Zaragoza on 04/01/13. For personal use only.

c d

10 µm 10 µm

Figure 3
A laboratory model of a subaerial rock biofilm. (a) Flasks with liquid cultures of Nostoc punctiforme (left) and
Sarcinomyces petricola (right). (b) Mixed fungal/cyanobacterial biofilms contain both partners growing on
membrane filters placed on top of media without carbon and nitrogen sources. (c) Confocal laser-scanning
microscope image of a calcofluor white stained cross-section of this biofilm demonstrates that the two
components form complex spatial patterns (red, autofluorescence of chlorophyll; blue, calcofluor white
stained fungal cells). The filter is below. (d ) The same biofilm seen from above. In contact with the fungus,
N. punctiforme changes to aseriate growth pattern.

442 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30

OTHER ASPECTS OF SUBAERIAL the experimental framework has to include

BIOFILM BIOLOGY (a) all known physical influences on the sub-
aerial environment, (b) different substrates in
Naturalistic studies first helped elucidate the
various stages of exposure to the atmosphere,
complexity of SAB development and how they
(c) permutations of possible atmospheric con-
spread around the globe (34, 70, 106). Later,
ditions, and (d ) likely members of the biofilm
the introduction of molecular biological tech-
consortium. Yet by reducing a complex SAB
niques showed that the complexity extends to
ecosystem to the tractable minimum, abiotic
the genetics of SAB inhabitants (39, 40, 73, 76,
and biotic interactions can be investigated
119). Wider application of molecular genetic
quantitatively. Reduction of model systems
techniques will hopefully reveal how similar (or
to the bare minimum has been successfully
different) SAB communities are in various geo-
applied to the study of symbioses between
graphical locations on different substrates. New
legumes and Rhizobium (65) as well as arbuscu-
members of SAB consortia will undoubtedly be
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

lar mycorrhizae and legumes (90). By analogy,

identified, and this information will help an-
we have reduced a SAB community to just two
swer the questions about the spread, growth,
components, a heterotrophic fungus and an
and survival of SABs on a global scale.
by University of Zaragoza on 04/01/13. For personal use only.

autotrophic cyanobacterium. We are using this

SABs are attractive objects of study in mi-
much-simplified system to study the effects
crobial ecology, geobiology, and applied re-
of atmosphere and substrate on SAB devel-
search, including materials science (biodeteri-
opment (Figure 3). We chose a well-studied
oration) and exobiology. Yet as we have seen
marble-derived isolate [strain A95 (46)] of
above, there is a need to move from descrip-
the microcolonial fungus Sarcinomyces petricola
tive, naturalistic, predictive studies to more
(Chaetothyriales) as the heterotroph (59; C.
quantitative ones. Understanding how these
Gueidan & A.A. Gorbushina, manuscript
unique assemblages of microorganisms con-
in preparation). Because cyanobacteria can
tribute to climate change, weathering, and soil
both photosynthesize and fix atmospheric
formation is important to many disciplines in-
nitrogen, they are important components
cluding agronomy, geochemistry, microbiol-
of rock biofilms. In addition, three features
ogy, soil science, and symbiosis research (5).
of cyanobacteria make them irreplaceable
A conceptual model of the SAB-atmosphere-
candidates in models of rock colonization:
lithosphere interface is necessary before we can
(a) perfect adaptation to desiccation (91) and
fully understand the global biogeochemistry
solar radiation (13, 36); (b) abundant production
of element fluxes (18). Simple models will
of capsular and easily released EPSs (96); and
not explain the holistic properties of a given
(c) their ability to enter into symbiosis with
system (95), but because there are many
fungi, bacteria and plants (56, 77, 79). Nostoc
microbe/climate/substrate combinations, de-
punctiforme strain ATCC 29133 ( = PCC
tailed, molecular analyses are only possible on
73102) is capable of carbon and nitrogen
greatly simplified systems.
fixation, is genetically well characterized, is
Even if a global commonality of SAB inhab-
completely sequenced, and has been widely
itants exists, the mere fact that a well-developed
used in symbiosis research (77). It was chosen
SAB community may include algae, cyanobac-
as the autotrophic and diazotrophic partner of
teria, heterotrophic bacteria, lichens, and
A95 for these reasons.
fungi means that the combinations of different
Detailed microscopic examination shows
microbes in separate SAB communities can be
that N. punctiforme and S. petricola grow well
vast, much too vast in fact to be modeled under
together, forming three-dimensional struc-
laboratory conditions. Fortunately, alternative
tures (Figure 3). Our preliminary observations
ways of studying SAB ecosystems exist. To accu-
indicate that the model biofilm strongly
rately reflect the development of a SAB system,

www.annualreviews.org • Life at the Atmosphere-Rock Interface 443

 ANRV387-MI63-21 ARI 6 August 2009 8:30

interacts with different substrates, nutrients,
environmental parameters, and physical
stresses. Quantification of growth and the
concomitant changes in the proportions and
localization of the biofilm components will
shed light on SAB contributions to weathering
of mineral components and degradation
of materials. This simplicity and genetic
tractability will permit detailed dissection of
how a heterotroph and phototroph/diazotroph
interact with one another to build SABs.
Model systems like these will allow additional
elements (of the biofilm, the mineral surface, or
the atmosphere) to be added and will provide
an instrument for the genetic dissection of SAB
development.

SUMMARY POINTS
1. SABs are cosmopolitan collections of microbial communities that occupy significant por-
tions of exposed terrestrial surfaces. SAB participants (comprising phototrophic algae and
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

cyanobacteria, heterotrophic fungi and bacteria, as well as lithotrophic microorganisms)

have contrasting growth requirements and development strategies.
2. SABs are subject to complex tripartite interactions between the atmosphere, the litho-
by University of Zaragoza on 04/01/13. For personal use only.

sphere, and biofilms. Genetic diversity of rock biofilms is reduced and is shaped by both
the atmosphere and the mineral substrate. Although the diversity of each individual mem-
ber of a SAB community is restricted, there are so many players (e.g., algae, ascomycetes,
actinobacteria, cyanobacteria, and lichens) that combinations of organisms in SABs can
be enormous.
3. Specially adapted, heterotrophic organisms are important members of SAB ecosystems.
Ascomycetous melanized MCF are particularly stress tolerant, easily penetrate the rock
substrate, and cooperate in an almost symbiotic way with phototrophic consortium mem-
bers.
4. SAB participants have shed all superfluous capacities to concentrate on survival. Micro-
colonial fungi are but one such example—the metabolic costs of sexual reproduction
versus the advantages of adaptability are too high to pay. All rock-inhabiting organisms
adapt the most thermodynamically efficient colony architecture and possess characteristic
unique and universal survival strategies.
5. The atmosphere-rock interface plays a key role in the evolution of developmental strate-
gies in fungi: The ancestor of both lichenized and pathogenic ascomycetes was most
likely a nonlichenized poikilo-tolerant rock-dweller.
6. With time, SABs cover the surface of rocks, but growth follows crevices/pores and re-
mains patchy. SABs actively participate in weathering and soil formation. Rock biofilm
communities absorb gases, organic matter, particulate matter, nitrogenous substances,
pollutants, and water from the atmosphere, therefore contributing to SAB growth and
weathering of the underlying substrate.
7. The volatile, atmospheric phase seeds newly exposed rock surfaces with organisms orig-
inating from SAB communities removed by wind erosion.
8. Since we are faced with a plethora of possibilities, it is almost impossible to study in-
dividual abiological or biological contributions to SAB development and a simplified
laboratory model is the only way to quantify the interactions. SAB ecosystems are an
attractive subject of research in geobiology, microbiology, and applied material sciences.

444 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30

DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS
This work was supported by a Feodor-Lynen Scholarship of the Alexander von Humboldt
Foundation to AAG, as well as by grants from the Swiss National Science Foundation (no.
3100AO 116858/1, IZK0A0-119407, and 3100AO-122513/1). DFG grant KON 1416/2007 GO
897/9-1 made a sampling trip to Australia and New Zealand possible. This trip was facilitated by
the generosity of Max Broughton and Clive Pankhurst. Yin Yin Aung, Christoph Bauer, Jerome
Bosset, Arlette Cattaneo, Fanny Cavat, Dora Gerber, Jocelyne Favet, Michel Goldschmidt-
Clermont, Mike Parkan, and Zakarie Saci of the University of Geneva kindly helped with various
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

aspects of this review. We thank Dagmar Weinreich-Brunner (Oldenburg University) for her help
with compiling the figures, as well as Renate Kort for Figures 1a and 2e,f .
by University of Zaragoza on 04/01/13. For personal use only.

LITERATURE CITED
1. Aristovskaya TV. 1980. Mikrobiologija processov pochvoobrazovanija. Leningrad: Nauka. 187 pp.
2. Baas Becking LGM. 1934. Geobiologie of inleiding tot de milieukunde. Diligentia Wetensch. Ser. 18/19; van
Stockum’s Gravenhange: The Hague, 263 pp.
3. Bachmann E. 1916. Ein kalklösender Pilz. Ber. Bot. Ges. 34:528–39
4. Banfield JF, Barker WW, Welch SA, Taunton A. 1999. Biological impact on mineral dissolution: appli-
cation of the lichen model to understanding mineral weathering in the rhizosphere. Proc. Natl. Acad. Sci.
USA 96:3403–11
5. Banfield JF, Tyson GW, Allen EI, Whitaker RJ. 2005. The search for a molecular-level understanding
of the processes that underpin the Earth’s biogeochemical cycles. Rev. Mineral. Geochem. 59:109–55
6. Battistuzzi FU, Feijao A, Hedges SB. 2004. A genomic timescale of prokaryote evolution: insights into
the origin of methanogenesis, phototrophy and the colonisation of land. BMC Evol. Biol. 4:44
7. Battistuzzi FU, Hedges SB. 2009. A major clade of prokaryotes with ancient adaptations to life on land.
Mol. Biol Evol. 26:335–43
8. Bekker A, Holland HD, Wang PL, Rumble D III, Stein HJ, et al. 2004. Dating the rise of atmospheric
oxygen. Nature 427:117–20
9. Blackwell M. 2000. Terrestrial life—fungal from the start? Science 289:1884–85
10. Bock E, Sand W. 1993. The microbiology of masonry biodeterioration. J. Appl. Bacteriol. 74:503–14
11. Braams J. 1992. Ecological studies on the fungal microflora inhabiting historic sandstone monuments. PhD thesis.
Oldenburg Univ. 128 pp.
12. Brown JKM, Hovmoller MS. 2002. Epidemiology—aerial dispersal of pathogens on the global and
continental scales and its impact on plant disease. Science 297:537–41
13. Büdel B. 1999. Ecology and diversity of rock-inhabiting cyanobacterial in tropical regions. Eur. J. Phycol.
34:361–70
14. Burford EP, Fomina M, Gadd GM. 2003. Fungal involvement in bioweathering and biotransformation
of rocks and minerals. Mineral. Mag. 67:1127–55
15. Burford EP, Hillier S, Gadd GM. 2006. Biomineralization of fungal hyphae with calcite (CaCO3 ) and
calcium oxalate mono- and dihydrate in carboniferous limestone microcosms. Geomicrobiol. J. 23:599–611
16. Canfield DE. 2005. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev.
Earth Plant. Sci. 33:1–36
17. Carson JK, Rooney D, Gleeson DB, Clipson N. 2007. Altering the mineral composition of soil causes a
shift in microbial community structure. FEMS Microbiol. Ecol. 61:414–23
18. Chertov OG, Gorbushina AA, Deventer B. 2004. A model for microcolonial fungi growth on rock
surfaces. Ecol. Model. 177(3–4):415–26

www.annualreviews.org • Life at the Atmosphere-Rock Interface 445

 ANRV387-MI63-21 ARI 6 August 2009 8:30

19. Ciferri O. 1999. Microbial degradation of paintings. Appl. Environ. Microbiol. 65:879–85
20. Costerton JW, Stoodley P. 2003. Microbial biofilms: protective niches in ancient and modern micro-
biology. Fossil and Recent Biofilms: A Natural History of Life on Earth, ed. WE Krumbein, DM Paterson,
GA Zavarzin, pp. 15–21. Dordrecht: Kluwer
21. Crispim CA, Gaylarde CC. 2005. Cyanobacteria and biodeterioration of cultural heritage: a review.
Microb. Ecol. 49:1–9
22. Danin A, Gerson R, Marton K, Garty J. 1982. Patterns of limestone and dolomite weathering by lichens
and blue-green algae and their paleoclimatic significance. Palaeogeogr. Palaeoclimatol. Palaeoecol. 37:221–33
23. Darwin CH. 1890. Naturalist’s Voyage Around The World. London: John Murray. 500 pp.
24. de Hoog GS. 1993. Evolution of black yeasts: possible adaptation to the human host. Antonie van Leeuwen-
hoek 63:105–9
25. de los Rios A, Wierzchos J, Sancho LG, Ascaso C. 2004. Exploring the physiological state of continental
Antarctic endolithic microorganisms by microscopy. FEMS Microbiol. Ecol. 50:143–52
26. Des Marais DJ. 2001. On the origins of photosynthesis. Science 291:436–37
27. Diakumaku E, Gorbushina AA, Krumbein WE, Panina L, Soukharjeski S. 1995. Black fungi in marble
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

and limestones—an aesthetical, chemical and physical problem for the conservation of monuments.
Sci. Tota Environ. 167:295–304
28. Dornieden T, Gorbushina AA, Krumbein WE. 1997. Änderungen der physikalischen Eigenschaften von
by University of Zaragoza on 04/01/13. For personal use only.

Marmor durch Pilzbewuchs. Int. J. Restor. Build. Monum. 3:441–56

29. Eppard M, Krumbein WE, Koch C, Rhiel E, Staley JT, Stackebrandt E. 1996. Morphological, physi-
ological, and molecular characterization of actinomycetes isolated from dry soil, rocks, and monument
surfaces. Arch. Microbiol. 166:12–22
30. Fajardo-Cavazos P, Nicholson W. 2006. Bacillus endospores isolated from granite: close molecular rela-
tionships to globally distributed Bacillus spp. from endolithic and extreme environments. Appl. Environ.
Microbiol. 72:2856–63
31. Falkowski PG. 2006. Tracing oxygen’s imprint on Earth’s metabolic evolution. Science 311:1724–25
32. Falkowski PG, Fenchel T, Delong EF. 2008. The microbial engines that drive Earth’s biogeochemical
cycles. Science 320:1034–39
33. Friedmann EI. 1982. Endolithic microorganisms in the Antarctic cold desert. Science 215:1045–53
34. Friedmann EI, Ocampo-Friedmann R. 1984. Endolithic microorganisms in extremely dry environments:
analysis of a lithobiontic microbial habitat. In Current Perspectives in Microbial Ecology, ed. MJ Klug,
CA Reddy. pp. 177–85. Washington, DC: ASM
35. Gadd GM. 2008. Bacterial and fungal geomicrobiology: a problem with communities? Geobiology 6:278–
84
36. Garcia-Pichel F, Castenholz RW. 1993. Occurrence of UV-absorbing, mycosporine-like compounds
among cyanobacterial isolates and an estimate of their screening capacity. Appl. Environ. Microbiol. 59:163–
69
37. Gargas A, DePriest PT, Grube M, Tehler A. 1995. Multiple origins of lichen symbioses in fungi suggested
by SSU rDNA phylogeny. Science 268:1492–95
38. Giles J. 2005. The dustiest place on Earth. Nature 434:816–19
39. Gleeson DB, Clipson N, Melville K, Gadd GM, McDermott FP. 2005. Characterisation of fungal
community structure on a weathered pegmatite granite. Microb. Ecol. 50:360–68
40. Gleeson DB, Kennedy NM, Clipson N, Melville K, Gadd GM, McDermott FP. 2006. Characterization
of bacterial community structure on a weathered pegmatitic granite. Microb. Ecol. 51:526–34
41. Golubic S, Friedmann EI, Schneider J. 1981. The lithobiontic ecological niche, with special reference
to microorganisms. J. Sediment. Petrol. 51:475–78
42. Gonzalez JM, Saint-Jimenez C. 2005. Application of molecular nucleic-acid based techniques for the
study of microbial communities in monuments and artwork. Int. Microbiol. 8:189–94
43. Gorbushina AA. 2007. Life on the rocks. Environ. Microbiol. 9:1613–31
44. Gorbushina AA, Beck A, Schulte A. 2005. Microcolonial rock inhabiting fungi and lichen photobionts:
evidence for mutualistic interactions. Mycol. Res. 109:1288–96
45. Gorbushina AA, Kort R, Schulte A, Lazarus D, Schnetger B, et al. 2007. Life in Darwin’s dust: inter-
continental transport and survival of microbes in the nineteenth century. Environ. Microbiol. 9:2911–22

446 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30

46. Gorbushina AA, Kotlova ER, Sherstnjova OA. 2008. Cellular responses of microcolonial rock fungi to
long-term desiccation and subsequent rehydration. Stud. Mycol. 60:91–97
47. Gorbushina AA, Krumbein WE. 2004. Role of organisms in wear down of rocks and minerals. In
Microorganisms in Soils: Roles in Genetics and Functions, ed. F Buscot, A Varma, pp. 59–84. Berlin: Springer
48. Gorbushina AA, Krumbein WE, Hamman CH, Panina L, Soukharjevski S, Wollenzien U. 1993. Role
of black fungi in color-change and biodeterioration of antique marbles. Geomicrobiol. J. 11:205–21
49. Gorbushina AA, Krumbein WE, Palinska KA. 1999. Poikilotroph growth patterns in rock inhabiting
cyanobacteria. In The Phototrophic Prokaryotes, ed. GA Peschek, W Löffelhardt, G Schmetterer, pp. 657–
64. New York: Kluwer Academic/Plenum
50. Gorbushina AA, Krumbein WE, Volkmann M. 2002. Rock surfaces as life indicators: new ways to
demonstrate life and traces of former life. Astrobiology 2:203–13
51. Gorbushina AA, Petersen K. 2000. Distribution of microorganisms on ancient wall paintings as related
to associated faunal elements. Int. Biodeterior. Biodegrad. 46:277–84
52. Gorbushina AA, Whitehead K, Dornieden T, Niesse A, Schulte A, Hedges J. 2003. Black fungal colonies
as units of survival: hyphal mycosporines synthesized by rock dwelling microcolonial fungi. Can. J. Bot.
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

81:131–38
53. Goudie AS. 2008. The history and nature of wind erosion in deserts. Annu. Rev. Earth Planet. Sci. 36:97–
119
by University of Zaragoza on 04/01/13. For personal use only.

54. Griffin DW, Kellogg CA, Garrison VH, Shinn EA. 2002. The global transport of dust. Am. Sci. 90:228–
35
55. Griffin DW, Kubilay N, Kocak M, Gray MA, Borden TC, Shinn EA. 2007. Airborne desert dust and
aeromicrobiology over the Turkish Mediterranean coastline. Atmospher. Environ. 41:4050–62
56. Grilli Caiola M. 1992. Cyanobacteria in symbioses with bryophytes and tracheophytes. In Algae and
Symbiosis: Plants, Animals, Fungi, Viruses, Interactions Explored, ed. W Reisser, pp. 231–53. Bristol, UK:
Biopress
57. Gromov BV. 1957. Microflora of rock substrates and primitive soils from northern areas of the USSR.
Mikrobiologiya 26:52–59
58. Gueidan C, Roux C, Lutzoni F. 2007. Using a multigene analysis to assess generic delineation and
character evolution in Verrucariaceae (Verrucariales, Ascomycota). Mycol. Res. 111:1147–70
59. Gueidan C, Ruibal Villasenor C, de Hoog GS, Gorbushina AA, Untereiner WA, Lutzoni F. 2008. An
extremotolerant rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud. Mycol.
60:111–19
60. Hoppert M, Flies C, Pohl W, Gunzl B, Schneider J. 2004. Colonisation strategies of lithobiontic mi-
croorganisms on carbonate rocks. Environ. Geol. 46:421–28
61. Humboldt von A. 1808. Tableaux de la nature, ou considerations sur la deserts, sur la physiognomie des vegetaux,
et sur la cataractes des l’Orenoque. Paris. 240 pp.
62. Hutchens E, McDermott FP, Clipson N. 2008. Bacteria, fungi and archaea on silicate minerals—a case
for selective colonization. Geochim. Cosmochim. Acta 72:A404
63. Isacenko B. 1936. Sur la corrosion du béton. Dokl. Akad. Nauk SSSR 2:288–89
64. Jaag O. 1945. Untersuchungen über die Vegetation und Biologie der Algen des nackten Gesteins in den Alpen,
im Jura und im schweizerischen Mittelland. Bern, Switz.: Büchler
65. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC. 2007. How rhizobial symbionts invade
plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619–33
66. Kellogg CA, Griffin DW. 2006. Aerobiology and the global transport of desert dust. Trends Ecol. Evol.
21:638–44
67. Kemmling A, Kamper M, Flies C, Schieweck C, Hoppert M. 2004. Biofilms and extracellular matrices
on geomaterials. Environ. Geol. 46:429–35
68. Knoll AH. 2003. Life on a Young Planet: The First Three Billion Years of Evolution on Earth. Princeton,
NJ: Princeton Univ. Press
69. Krumbein WE. 1969. Über den Einfluss der Mikroflora auf die exogene Dynamik (Verwitterung und
Krustenbildung). Geol. Rundsch. 58:333–63
70. Krumbein WE, 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

www.annualreviews.org • Life at the Atmosphere-Rock Interface 447

 ANRV387-MI63-21 ARI 6 August 2009 8:30

71. Krumbein WE, Petersen K, Schellnhuber HJ. 1989. On the geomicrobiology of yellow, orange, red,
brown and black films and crusts developing on several different types of stone and objects of art. In
Proc. Symp. on the Oxalate Films: Origin and Significance in the Conservation of Works of Art, Milano, ed.
G Alessandrini, pp. 337–47
72. Kuhlman KR, Venkat P, La Duc MT, Kuhlman GM, McKay CP. 2008. Evidence of a microbial com-
munity associated with rock varnish at Yungay, Atacama Desert, Chile. J. Geophys. Res. Biogeosci. 113:G4
doi:10.1029/2007JG000677
73. Lopez-Bautista JM, Rindi F, Casamata D. 2007. The systematics of subaerial algae. In Algae and Cyanobac-
terial in Extreme Environments, ed. J Seckbach, 11:599–617. Amsterdam: Springer
74. Lyalikova NN, Petushkova YP. 1991. Role of microorganisms in the weathering of minerals in building
stone of historical buildings. Geomicrobiology J. 9:91–101
75. McNamara CJ, Mitchell R. 2005. Microbial deterioration of historic stone. Front. Ecol. Environ. 3:445–51
76. McNamara CJ, Perry TD, Bearce KA, Hernandez-Duque G, Mitchell R. 2006. Epilithic and endolithic
bacterial communities in limestone from a Maya archaeological site. Microb. Ecol. 51:51–64
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

77. Meeks JC. 1998. Symbiosis between nitrogen-fixing cyanobacteria and plants. BioScience 48:266–76
78. Mitchell R, Gu JD. 2000. Changes in the biofilm microflora of limestone caused by atmospheric pollu-
tants. Int. Biodeterior. Biodegradation 46:299–303
by University of Zaragoza on 04/01/13. For personal use only.

79. Mollenhauer D, Mollenhauer R, Kluge M. 1996. Studies on initiation and development of the part-
ner association in Geosiphon pyriforme (Kütz.) v. Wettstein, a unique endosymbiotic system of a fungus
(Glomales) and the cyanobacterium Nostoc punctiforme (Kütz.) Hariot. Protoplasma 193:3–9
80. Müntz A. 1890. Sur la decomposition des roches et la formation de la terre arable. C.R. Acad. Sci.
110:1370–72
81. Nienow JA, Friedman EI. 1993. Terrestrial lithophytic (rock) communities. In Antarctic Microbiology, ed.
EI Friedmann, pp. 342–412. New York: Wiley-Liss
82. Olson JM, Blankenship RE. 2004. Thinking about the evolution of photosynthesis. Photosynth. Res.
80:373–86
83. Olson JM, Pierson BK. 1986. Photosynthesis 3.5 thousand million years ago. Photosynthesis Res. 9:251–59
84. Omelon CR. 2008. Endolithic microbial communities in polar desert habitats. Geomicrobiol. J. 25:404–14
85. Ortega-Morales O, Guezennec J, Hernandez-Duque G, Gaylarde CC, Gaylarde PM. 2000. Phototrophic
biofilms on ancient Mayan buildings in Yucatan, Mexico. Curr. Microbiol. 40:81–85
86. Paine SG, Lingood FV, Schimmer F, Thrupp TC. 1933. The relation of micro-organisms to the decay
of building stones. Philos. Trans. R. Soc. B 222:97–127
87. Palmer FE, Staley JT, Ryan B. 1990. Ecophysiology of microcolonial fungi and lichens on rocks in
Northeastern Oregon. New Phytol. 116:613–20
88. Palmer RJ, Friedmann EI. 1990. Water relations and photosynthesis in the cryptoendolithic microbial
habitat of hot and cold deserts. Microb. Ecol. 19:111–18
89. Paracelsus. 1567. Philosophia magna, tractus aliquot, Cöln
90. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol.
6:763–75
91. Potts M. 1999. Mechanisms of desiccation tolerance in cyanobacteria. Eur. J. Phycol. 34:319–28
92. Prenafeta-Boldu FX, Summerbell R, de Hoog GS. 2006. Fungi growing on aromatic hydrocarbons:
biotechnology’s unexpected encounter with biohazard? FEMS Microbiol. Rev. 30:109–30
93. Quispel A. 1998. Lourens G. M. Baas Becking (1895–1963), inspirator for many (micro)biologists. Int.
Microbiol. 1:69–72
94. Raymond J, Segrè D. 2006. The effect of oxygen on biochemical networks and the evolution of complex
life. Science 311:1764–67
95. Relman DA. 2008. “Til death do us part”: coming to terms with symbiotic relationships. Nat. Rev.
Microbiol. 6:721–24
96. Richert L, Golubic S, Guédès RL, Ratiskol J, Payri C, Guezennec J. 2005. Characterization of ex-
opolysaccharides produced by cyanobacteria isolated from Polynesian microbial mats. Curr. Microbiol.
51:379–84

448 Gorbushina · Broughton

 ANRV387-MI63-21 ARI 6 August 2009 8:30

97. Rindi F. 2007. Diversity, distribution and ecology of green algae and cyanobacterial in urban habi-
tats. In Algae and Cyanobacteria in Extreme Environments, ed. J Seckbach, 11:619–38. Amsterdam: The
Netherlands
98. Rosling A, Lindahl BD, Finlay RD. 2004. Carbon allocation to ectomycorrhizal roots and mycelium
colonising different mineral substrates. New Phytol. 162:795–802
99. Ruibal CV. 2004. Isolation and characterization of melanized, slow-growing fungi from semiarid rock surfaces
of central Spain and Mallorca. PhD dissertation. Univ. Autónoma Madrid/Merck, Sharp & Dohme
100. Saiz-Jimenez C. 1997. Biodeterioration vs biodegradation: the role of microorganisms in the removal of
pollutants deposited on historic buildings. Int. Biodeterior. Biodegrad. 40:225–32
101. Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S. 2005. Fungi at the edge of life:
cryptoendolithic black fungi from Antarctic desert. Stud. Mycol. 51:1–32
102. Siebert J, Hirsch P, Hoffmann B, Gliesche CG, Peissl K, Jendrach M. 1996. Cryptoendolithic mi-
croorganisms from Antarctic sandstone of Linnaeus terrace (Asgard range): diversity, properties and
interactions. Biodiv. Conserv. 5:1337–63
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org

103. Sigler WV, Bachofen R, Zeyer J. 2003. Molecular characterisation of endolithic cyanobacterial inhabiting
exposed dolomite in central Switzerland. Environ. Microbiol. 5:618–27
104. Sollas WJ. 1880. On the action of a lichen on a limestone. Rep. Br. Assoc. Adv. Sci. 586 pp.
105. Somova NG, Dobrovolskaya TG, Zenova GM, Ivanovskii RN. 1997. Microbial growth on the masonry
by University of Zaragoza on 04/01/13. For personal use only.

surface: synecological analysis. Microbiology 67:569–74

106. Staley JT, Palmer F, Adams JB. 1982. Microcolonial fungi: common inhabitants on desert rocks? Science
215:1093–95
107. Sterflinger K. 1998. Temperature and NaCl-tolerance of rock-inhabiting meristematic fungi. Antonie
van Leeuwenhoek 74:271–81
108. Sterflinger K, De Baere R, de Hoog GS, De Watcher R, Krumbein WE, Haase G. 1997. Coniosporium
perforans and C. apollinis, two new rock-inhabiting fungi isolated from marble in the Sanctuary of Delos
(Cyclades, Greece). Antonie van Leeuwenhoek 72:349–63
109. Sterflinger K, de Hoog GS, Haase G. 1999. Phylogeny and ecology of meristematic ascomycetes. Stud.
Mycol. 43:5–22
110. Sterflinger K, Krumbein WE. 1995. Multiple stress factors affecting growth of rock-inhabiting black
fungi. Bot. Acta 108:490–96
111. Sterflinger K, Krumbein WE. 1997. Dematiaceous fungi as a major agent for biopitting on Mediterranean
marbles and limestones. Geomicrobiol. J. 14:219–22
112. Sterflinger K, Krumbein WE, Lellau T, Rullkötter J. 1999. Microbially mediated orange patination of
rock surfaces. Anc. Biomol. 3:51–65
113. Sterflinger K, Prillinger H. 2001. Molecular taxonomy and biodiversity of rock fungal communities in
an urban environment (Vienna, Austria). Antonie van Leeuwenhoek 80:275–86
114. Suihko ML, Alakomi HL, Gorbushina AA, Fortune I, Marquardt J, Saarela M. 2007. Characterization of
aerobic bacterial and fungal microbiota on surfaces of historic Scottish monument. Syst. Appl. Microbiol.
30:494–508
115. Thompson JN. 1994. The Co-evolutionary Process. Chicago: Univ. Chicago Press
116. Urzı̀ C, Krumbein WE, Warscheid TH. 1992. On the question of biogenic color changes of Mediteranean
monuments. Conserv. Monum. Mediterr. Basin. In Proc. 2nd Int. Symp., Genève, ed. D Decrouez,
J Chamay, F Zezza, pp. 397–420. Mus. Hist. Nat., Genève
117. Urzı̀ C, Realini M. 1998. Colour changes of Noto’s calcareous sandstone as related to its colonisation by
microorganisms. Int. Biodeterior. Biodegrad. 42:45–54
118. Viles HA, Gorbushina AA. 2003. Soiling and microbial colonisation on urban roadside limestone: a three
year study in Oxford, England. Build. Environ. 38:1217–24
119. Walker JJ, Pace NR. 2007. Endolithic microbial ecosystems. Annu. Rev. Microbiol. 61:331–47
120. Warscheid T, Braams J. 2000. Biodeterioration of stone: a review. Int. Biodeterior. Biodegrad. 46:343–
68
121. Watanabe Y, Martini JE, Ohmoto H. 2000. Geochemical evidence for terrestrial ecosystems 2.7 billion
years ago. Nature 408:574–78

www.annualreviews.org • Life at the Atmosphere-Rock Interface 449

 ANRV387-MI63-21 ARI 6 August 2009 8:30

122. Winka K, Eriksson OE, Bång Å. 1998. Molecular evidence for recognizing the Chaetothyriales. Mycologia
90:822–30
123. Wollenzien U, de Hoog GS, Krumbein WE, Urzı̀ C. 1995. On the isolation of microcolonial fungi
occurring on and in marble and other calcareous rocks. Sci. Total Environ. 167:287–94
124. Xiong J, Bauer CE. 2002. Complex evolution of photosynthesis. Annu. Rev. Plant Biol. 53:503–21
Annu. Rev. Microbiol. 2009.63:431-450. Downloaded from www.annualreviews.org
by University of Zaragoza on 04/01/13. For personal use only.

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Annual Review of
Microbiology

Contents Volume 63, 2009

Frontispiece
Lars G. Ljungdahl p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p xii
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A Life with Acetogens, Thermophiles, and Cellulolytic Anaerobes

Lars G. Ljungdahl p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
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Regulation of Translation Initiation by RNA Binding Proteins

Paul Babitzke, Carol S. Baker, and Tony Romeo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p27
Chemotaxis-Like Regulatory Systems: Unique Roles
in Diverse Bacteria
John R. Kirby p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p45
Aminoacyl-tRNA Synthesis and Translational Quality Control
Jiqiang Ling, Noah Reynolds, and Michael Ibba p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p61
Resurrected Pandemic Influenza Viruses
Terrence M. Tumpey and Jessica A. Belser p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p79
Interspecies Chemical Communication in Bacterial Development
Paul D. Straight and Roberto Kolter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p99
Lipid Signaling in Pathogenic Fungi
Ryan Rhome and Maurizio Del Poeta p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 119
Biological Insights from Structures of Two-Component Proteins
Rong Gao and Ann M. Stock p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 133
Role of GTPases in Bacterial Ribosome Assembly
Robert A. Britton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 155
Gene Transfer and Diversification of Microbial Eukaryotes
Jan O. Andersson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177
Malaria Parasite Development in the Mosquito and Infection
of the Mammalian Host
Ahmed S.I. Aly, Ashley M. Vaughan, and Stefan H.I. Kappe p p p p p p p p p p p p p p p p p p p p p p p p p p p p 195
How Sweet it is! Cell Wall Biogenesis and Polysaccharide Capsule
Formation in Cryptococcus neoformans
Tamara Lea Doering p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 223

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Mitochondrial Evolution and Functions in Malaria Parasites

Akhil B. Vaidya and Michael W. Mather p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 249
Probiotic and Gut Lactobacilli and Bifidobacteria: Molecular
Approaches to Study Diversity and Activity
Michiel Kleerebezem and Elaine E. Vaughan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 269
Global Emergence of Batrachochytrium dendrobatidis and Amphibian
Chytridiomycosis in Space, Time, and Host
Matthew C. Fisher, Trenton W.J. Garner, and Susan F. Walker p p p p p p p p p p p p p p p p p p p p p p p p p 291
Anaerobic Oxidation of Methane: Progress with an Unknown Process
Katrin Knittel and Antje Boetius p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 311
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The Trypanosoma brucei Flagellum: Moving Parasites

in New Directions
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Katherine S. Ralston, Zakayi P. Kabututu, Jason H. Melehani,

Michael Oberholzer, and Kent L. Hill p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 335
Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions
Paola Bonfante and Iulia-Andra Anca p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 363
Evolutionary Roles of Upstream Open Reading Frames in Mediating
Gene Regulation in Fungi
Heather M. Hood, Daniel E. Neafsey, James Galagan, and Matthew S. Sachs p p p p p p p p p 385
Single-Cell Ecophysiology of Microbes as Revealed by Raman
Microspectroscopy or Secondary Ion Mass Spectrometry Imaging
Michael Wagner p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 411
Microbiology of the Atmosphere-Rock Interface: How Biological
Interactions and Physical Stresses Modulate a Sophisticated
Microbial Ecosystem
Anna A. Gorbushina and William J. Broughton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 431
What Sets Bacillus anthracis Apart from Other Bacillus Species?
Anne-Brit Kolst, Nicolas J. Tourasse, and Ole Andreas Økstad p p p p p p p p p p p p p p p p p p p p p p p p p p p 451
The Expanding World of Methylotrophic Metabolism
Ludmila Chistoserdova, Marina G. Kalyuzhnaya, and Mary E. Lidstrom p p p p p p p p p p p p p p 477
Genomics, Genetics, and Cell Biology of Magnetosome Formation
Christian Jogler and Dirk Schüler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 501
Predatory Lifestyle of Bdellovibrio bacteriovorus
Renee Elizabeth Sockett p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 523
Plant-Growth-Promoting Rhizobacteria
Ben Lugtenberg and Faina Kamilova p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 541

vi Contents
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Photorhabdus and a Host of Hosts

Nick R. Waterfield, Todd Ciche, and David Clarke p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 557
Management of Oxidative Stress in Bacillus
Peter Zuber p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 575
Sociobiology of the Myxobacteria
Gregory J. Velicer and Michiel Vos p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 599

Index

Cumulative Index of Contributing Authors, Volumes 59–63 p p p p p p p p p p p p p p p p p p p p p p p p p p p 625

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Errata
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An online log of corrections to Annual Review of Microbiology articles may be found at

http://micro.annualreviews.org/

Contents vii