Trends in

Ecology & Evolution

Review

Fungi are key players in extreme ecosystems

Claudia Coleine , 1,*,@ Jason E. Stajich, 2,4,@ and Laura Selbmann 1,3,5,@

Extreme environments on Earth are typically devoid of macro life forms and are Highlights
inhabited predominantly by highly adapted and specialized microorganisms. It has become evident that extreme envi-
The discovery and persistence of these extremophiles provides tools to model ronments are not only inhabited by
archaea and bacteria; fungi are the
how life arose on Earth and inform us on the limits of life. Fungi, in particular,
most versatile phylogenetic lineage in
are among the most extreme-tolerant organisms with highly versatile lifestyles the Tree of Life and can colonize/survive
and stunning ecological and morphological plasticity. Here, we overview the in all types of extreme habitats.
most notable examples of extremophilic and stress-tolerant fungi, highlighting
Fungi often show a greater capacity for
their key roles in the functionality and balance of extreme ecosystems. The re- tolerance to stresses than prokaryotes
markable ability of fungi to tolerate and even thrive in the most extreme environ- and fungal diversity in extreme environ-
ments, which preclude most organisms, have reshaped current concepts ments is higher than previously thought.
regarding the limits of life on Earth.
The discovery of extreme fungi has been
pivotal for major scientific discoveries in
biology and in advancing the field of
biotechnology.
Fungi are conspicuous and important representatives among extreme-resistant
microorganisms A combination of extreme-tolerant fea-
Life evolved on Earth under conditions of high temperature, radiation, and aridity, tougher than the tures and ecological and morphological
plasticity make fungi key organisms in
present day [1]. Ongoing exploration of the biosphere [2,3] is leading to continued discoveries of life
the search for the limits of life on Earth
in environments that were previously considered uninhabitable, redrawing the boundaries where and in the Universe.
life can still persist, considerably stretching our concept of terrestrial habitability (e.g., [4–6]). Hostile
environments encompass over three-quarters of our planet [2] and provide a favorable background
for the creation of a unique type of biodiversity and specific adaptations. Over the past few
decades, a conspicuous number of microorganisms have been found in environments with
temperatures up to +121°C and down to −25°C, or able to survive at pH 0 or 13, or exposed to
damaging radiation or toxic elements, or in saturating salt concentrations [7,8]. These discoveries
have contributed to provide insights into the origins of life on Earth by revealing unexpectedly high
levels of diversity and complexity, tremendously expanding our knowledge of how extremophiles
and extreme-tolerant microorganisms adapt, survive, and function in the extremes [9].

When we think of extremophiles, prokaryotes come first to mind. Eukaryotes, having far more com-
1
Department of Ecological and Biological
Sciences, University of Tuscia, 01100
plex cells, have been reputed to be less efficient against stresses; therefore, effort has been mainly Viterbo, Italy
expended on bacteria or archaea [7,10,11]. It is now becoming evident that eukaryotes, and fungi 2
Department of Microbiology & Plant
in particular, are exceptionally capable of living in extremely inhospitable environments, showing Pathology and Institute of Integrative
Genome Biology, University of
evidence of resistance that is even higher than prokaryotes. Due to their high level of ecological California, Riverside, Riverside, CA
versatility and morphological plasticity [12], fungi represent the most adaptable phylogenetic 92521, USA
3
lineage in the Tree of Life (TOL), as they can dwell in virtually all types of habitats [13], thrive Italian National Antarctic Museum (MNA),
Mycological Section, 16121 Genoa, Italy
under a wide range of parameters, and adopt various lifestyles; they can be, for example, 4
https://lab.stajich.org/
saprotrophs, symbionts, or parasites. Interactions with other life forms have had a role in the evo- 5
https://www.lauraselbmann.com/
lution of some highly extremophilic (see Glossary) or extreme-tolerant lineages that were proven
to derive from lichenized and rock-inhabiting lifestyles [14–16]).
*Correspondence:
coleine@unitus.it (C. Coleine).
Gostinčar and collaborators [17] argued that specific traits displayed in some fungal groups, such @
Twitter: @ClaudiaColeine (C. Coleine),
as asexuality, synthesis of melanin-like pigments, and a flexible morphology ,are pre-adaptations @hyphaltip (J.E. Stajich), and
that promote their endurance and the eventual evolution of extreme tolerance. The capacity to @LauraSelbmann (L. Selbmann).

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© 2022 Elsevier Ltd. All rights reserved.
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produce vegetative survival structures or to downregulate metabolic activity to enter into a dor- Glossary
mant state with a high capacity for dehydration and rapid resurrection when water is available Acidophilic fungi: fungi capable of
anew is marked in some extreme-tolerant fungi [18]. growing in highly acidic conditions up
to pH 1.
Acidotolerant fungi: fungi living in
An unexpected degree of fungal species diversity has been discovered in extreme habitats such acidic habitats but also able to grow
as hot and cold deserts, acid mine drainage (AMD), hypersaline environments, and geothermal, under neutral or even alkaline pH.
volcanic, or extremely polluted mining soils (e.g., [19–22]). Endolithic microbial communities:
microorganisms dwelling inside porous
rocks. This spectacular adaptation
Fungi, despite still being neglected, represent an important resource in addressing major global represents the last resort for life under
challenges. They are exceptional degraders, and extreme-loving fungi guarantee C and N flows extreme aridity.
maintaining active biogeochemical cycles, significantly contributing to the balance and function- Extremophilic and extreme-tolerant
fungi: fungi capable of living in
ing of even the harshest ecosystems (e.g., [23]). Transformation of metals and minerals is also a
conditions that would kill other life forms,
key aspect of fungal activity; fungal biomineralization is an important facet of geomycology – including intense cold, heat, pressure,
namely, the roles of fungi in geochemical and geophysical processes [24]. dehydration, acidity/alkalinity, and other
chemical and physical extremes. They
may be categorized as ‘extreme
The time is now ripe to spotlight the extreme talents of free-living fungi and bring them to wider tolerant’ if they can tolerate extreme
scientific attention. While it is beyond our scope to provide an exhaustive review on all extreme- conditions such as oligotrophic, arid,
loving fungi, here we focus on some of the most notable examples, their biology, and their molec- and highly irradiated environments,
ular adaptations. We conclude by summarizing the role of these fungi in ecosystems although they grow optimally under
normal conditions, and as
functioning and highlighting knowledge gaps and areas of opportunity. ‘extremophiles’ if they require the
obligatory extreme conditions for their
Defining an extreme environment in an anthropocentric world survival and proliferation.
Halophilic fungi: fungi requiring high
Our planet contains a plethora of ecosystems that, by anthropocentric criteria, are classified not
salt concentrations (>8.8% NaCl) to
as normally habitable but as ‘extreme’. Extreme environments are characterized by one or more survive in salt environments such as
physicochemical parameters (e.g., temperature, radiation, salinity, pH) that reach values far from hypersaline lakes.
those considered normal and compatible with human life [25–27]. However, diverse and plentiful Halotolerant: fungi capable of
colonizing salt environments (1.2–2.9%
microbial life has been found in every extreme natural ecosystem across the globe and even in
NaCl) such as coastal dunes and saline
some derived from the negative impact of anthropogenic activities, such as AMD and radioactive deserts but that can still grow without
contamination (e.g., [27]; Figure 1). A combination of different stresses may be present at the salt (NaCl).
same time, as in hot springs, which are acidic or alkaline and simultaneously rich in metal content, Osmophiles: fungi that require high
osmotic pressures, such as high sugar
a few hypersaline lakes, which are tremendously alkaline, and the ice-free areas of the Antarctic
concentrations, to survive.
McMurdo Dry Valleys, which are concurrently hyperarid, oligotrophic, and exposed to massive Osmotolerant fungi: fungi that are
incident UV irradiation. Microorganisms able to colonize such environments are classified as adapted to tolerate high osmotic
polyextremophiles or poly-extreme tolerant and are capable of surviving under a wide pressures.
Poly-extreme tolerant: fungi that can
range of stresses; the most prominent examples are typically found in the fungal kingdom. survive under multiple extreme
conditions.
Fungi thrive under a plethora of the harshest environmental conditions Polyextremophiles: fungi that not only
The remarkable tolerance of fungi to water-stress conditions survive but also thrive under multiple
extreme conditions. For instance,
Among the physicochemical parameters that permit or prevent cellular activity, the most critical is polyextremophiles found in desert
water availability. Cells and their macromolecules are reliant on water and the vast majority of regions have to cope with intense UV
organisms function only when water is abundant. The most widely used parameter to measure irradiation and desiccation, high as well
as low temperatures and low availability
water availability is water activity (aw). The ability to tolerate or reproduce under low aw is a
of water and nutrients.
trait of xerophilic and xerotolerant species; osmophiles and osmotolerant species tolerate Psychrophilic: fungi that can grow
water constraints due to high amounts of solutes in the growth medium, while halotolerant spe- at or below 0°C, with optimum
cies and halophiles are able to grow at high salt (NaCl) concentrations. Fungi are the most growth temperatures of ≤15°C and
maximum growth temperatures of
xerophilic and xerotolerant organisms [28]. Most organisms need aw ranging from 0.99 to 0.97
≤20°C.
for active life; some bacteria can tolerate down to 0.9, while Haloarchaea are capable of growing Psychrotolerant: fungi that can grow
in saturated NaCl at aw 0.75 [29]. Notably, life in conditions below those values mostly occur in the close to 0°C, with optimum growth
fungal kingdom, among which the vast majority of species are able to grow on media with aw temperatures of >15°C and maximum
growth temperatures of >20°C.
0.97–0.91 and the true xerotolerant up to aw 0.6. Most xerotolerant fungi are Aspergillus and

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Penicillium species that accumulate intracellular glycerol as a compatible solute to counteract the Radiosynthesis: the ability of some
fungi to capture and convert ionizing
ambient low aw. Trehalose is another compatible osmolyte that improves stress tolerance in fungi
radiation energy into chemical energy
under various water stress conditions [29] and substitutes for water molecules in cell membranes, analogous to photosynthesis. Melanin is
protecting them from desiccation and freezing damage [30]. proposed as the agent of energy
capture and transduction.
Radiotropism: the ability of several
The growth limit for Eurotium amstelodami (xerophilic, halotolerant) is 0.7 aw and, as border examples, fungal species to harvest usable energy
Xeromyces bisporus (osmophilic) and the yeast Zygosaccharomyces rouxii (osmophilic) show growth from forms of ionizing radiation, such as
limits of aw0.62 and 0.61, respectively (i.e., −70 MPa). awvalues of 0.6 and below cannot sustain any gamma radiation emitted from nuclear
microbial proliferation. Aspergillus penicillioides represents the paramount exception (Box 1), although reactors.
Rock-inhabiting fungi: peculiar fungi
it is not surprising that fungi, both as lichen symbionts and free living, dominate the Antarctic McMurdo that form compact, melanized colonies
Dry Valleys, the coldest and most arid land on Earth and considered to be the closest Martian terres- on bare rock.
trial analog [31]. There, fungi that are also psychrophilic and psychrotolerant form endolithic Thermophilic: an organism that thrives
at relatively high temperatures, between
microbial communities where the rock-inhabiting fungus Friedmanniomyces endolithicus is
41°C and 122°C.
the most widespread and adapted [32], and soil microbial assemblages (e.g., Rhodotorula Water activity (aw): the ratio of the
frigidialcoholis) [33]. By contrast, fungi are not exceptionally skilled in heat resistance compared with water vapor pressure of the sample to
thermophilic prokaryotes and archaea (e.g., [34]). the water vapor pressure of pure water
under the same conditions. It may vary
from 1 (pure water) to theoretically 0
For a long time, hypersaline environments, such as the Dead Sea (aw 0.669), microbial mat eco- (absolute absence of water) and needs
systems, salterns, and saline soils (e.g., salt marshes, deserts, mines), were considered to be to be quantified with an accuracy of at
dominated almost completely by prokaryotes. This assumption was challenged two decades least two decimal places to be
acceptably aligned with sensitivity to
ago when fungi were proven to be highly skilled inhabitants of these habitats (e.g., [35–39]). For
cellular systems.
instance, in the Dead Sea, where most organisms survive in dormant stages and revive only Xerophilic: fungi able to grow up to
when the salinity is temporarily reduced during rare heavy-flooding events, the halophilic fungus aw <0.85, while they do not grow at
Eurotium rubrum is capable of maintaining an active metabolism [40].Many of these fungi higher values (i.e., 0.96–0.97).
Xerotolerant: fungi capable of growing
are also recognized as poly-extreme tolerant, coping simultaneously with multiple stresses (e.g., high at aw 0.85 and can tolerate higher values
salt and ion concentrations, low aw, high UV irradiation, extremes of temperature and pH) [35]. (i.e., >0.85).

Mycobiota inhabiting hypersaline waters mainly comprise meristematic melanized fungi such as
Hortaea werneckii, Phaeotheca triangularis, and Aureobasidium pullulans as well as a number
of Aspergillus and Penicillium species [41]; by contrast, few hyaline yeasts are reported to tolerate
high NaCl concentrations [42]. Some species such as P. triangularis, Wallemia ichthyophaga
(Box 2), and Trimmatostroma salinum are not known outside saline environments, suggesting
that these are their natural ecological niche (e.g., [43]).

Fungi have evolved numerous morphological and osmotic adaptations, such as meristematic
growth, extracellular polysaccharide substance (EPS) production, glycerol loss prevention,
pigmentation (melanins in the cell wall), and changes in membrane composition and fluidity, to
survive extremely saline conditions [36] (Figure 2, Key figure).

A high proportion of acidic amino acid residues was found in the genomes of several halophilic
species, supporting the theory of convergent evolution under extreme hypersaline stress. Metal-
ion transporters such as zinc/iron permease and a heavy-metal-transporting ATPase are upregu-
lated at high salinity in E. rubrum. Moreover, the mitogen-activated protein kinase (MAPK) pathway,
involved in germ tube elongation, branching, and hyphal fusion, is stimulated by conditions of low
aw in many xerotolerant fungal species [44]. Notably, fungi can modulate their membrane and cell
wall structure to counteract chaotropic and kosmotropic activity caused by solutes [45]; the
chaophilic X. bisporus, for instance, maintains low membrane unsaturation indices [46].

Adaptations can differ among these halophiles, suggesting the potential independent evolution of
the ion-homeostasis mechanisms of these fungi. For instance, transcriptomic and genomic

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Figure 1. Notable examples of extreme environments present around the Earth and beyond. Different environments where extremophilic and extreme-tolerant
microorganisms can be found and their approximate location (squares), adapted by Merino et al. [7]. In the right lower panel, squares indicate the McMurdo Dry Valleys and
Polar Plateau of Antarctica that are considered analogs of extraterrestrial environments as the Red Planet and icy moons (circles), respectively.

Box 1. A fungus beyond the limits of drought tolerability

Aspergillus penicillioides, first isolated from moldy sugar cane, cured fish, and desiccated chili [89], is a common mold with
a worldwide distribution from temperate to tropical climates. Being a true halophile, it is present in diverse saline and
hypersaline econiches such as the Dead Sea and solar salterns [44,90]. A. penicillioides is not only halophilic but also
xerophilic and osmophilic, withstanding low aw and high sugar along with high NaCl concentrations. It also grows close
to 0°C and can function anaerobically, and it is sometimes implicated in disseminated diseases such as aspergillosis
and keratomycosis [90,91].

Under saline conditions, xerophilic fungi accumulate molar concentrations of intracellular glycerol as compatible solutes to
counteract the ambient low aw [92]. Germination at very low aw can be significantly enhanced in spores that have accumu-
lated glycerol and by supplementing germination media with molar concentrations of glycerol [93]. These practices could
induce A. penicillioides, physiologically growing at aw0.68, which is inhibitory to most fungi, to germinate down to 0.585,
outside the currently accepted thermodynamic window for life. Understanding the water relations of microbial xerophiles
has important implications for increasing the productivity of soils in drylands, reducing human exposure to mycotoxins in
buildings or in dry and salt-preserved foods, in preventing food spoilage, and in protecting books and museum specimens.
There are also hints for planetary protection and the possibility of life on dry planets such as Mars. Spacecraft are frequently
contaminated with airborne propagules; Aspergillus sp. spores are among the most abundant and their accidental
transport to other planetary bodies poses a concrete contamination risk. Therefore, it is important to precisely define
the capabilities of these potential micronauts. Moreover, glycerol, copiously produced as a biophysical and physiological
stress protectant, can mitigate chaotropicity-mediated stresses caused by MgCl2 and other salts, potentially facilitating the
colonization of Martian brines.

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Box 2. The most halophilic fungus, Wallemia ichthyophaga

Although xerotolerance is rare in the Basidiomycota, the genus Wallemia comprises obligate halophilic yeast-like fungi that
are common inhabitants of concentrated seawater and air and food preserved with low aw. W. ichthyophaga [94], which is
phylogenetically and morphologically distinct from other species of the genus, is able to grow at extremely low aw. It is also
remarkably adapted to highly salt-concentrated conditions with an optimum between 2.6- and 3.4-M NaCl. In addition,
this fungus is able to grow in saturated KCl and MgSO4 solutions and even at around 2-M MgCl2 [95]. Such narrow
ecological versatility is common for specialized archaeal and bacterial halophiles, but the skills of this species are an excep-
tion in Eukarya; this fungus thus represents the most halophilic eukaryote described to date. The ecology and global
distribution of W. ichthyophaga remains unclear due to its only sporadic isolation from nature, which may be a conse-
quence of its extreme specialization and halophilic behavior as it is strictly limited to extremely saline habitats [17]. Interest-
ingly, the genome sequencing of this fungus uncovered an unusually compact genome (<10 Mbp) with a low number of
predicted protein-coding genes (<5000), while the average genome size in Basidiomycota is 50 Mbp and an average
genome contains more than 15 000 genes [96]. The ability to survive osmotic stress requires several adaptations.
W. ichthyophaga withstands high salt concentrations by increasing the intracellular concentration of polyols, using high-
affinity K+ transporters, and increasing the thickness of its cell wall by a factor of three [95]. In a recent population genomic
study [96], a mating-type locus was identified, providing evidence of the existence of (sexual) recombination in this fungus,
and supported the hypothesis that it can form a single recombining population even between different habitats and over
large geographical distances.

analyses of the species W. ichthyophaga demonstrated unusual traits of salt tolerance mecha-
nisms; compared with the high-salt-tolerant species H. werneckii, this fungus shows a lack of
most cation transporters and its main strategy of tolerance appears to be the prevention of ion
entry [47]. H. werneckii, instead, apparently excludes this cation, while its exceptional adaptability
to osmotically stressful conditions was related to whole-genome-duplication events [48].

Low pH is the realm of acid-loving fungi

A neutral pH allows most biological processes (e.g., human blood pH must be between 6.8 and
7.8 to support life), but nature is replete with organisms that thrive in extremely alkaline or acidic
conditions. Acidic environments on Earth are of both natural and anthropogenic origin, including
geothermal and volcanic areas, acidic lakes, acid rock drainage (ARD), and AMD (e.g., [49,50])
and are commonly characterized by elevated levels of toxic metals and sulfate and high tempera-
tures. Acidic habitats harbor highly diversified microbial communities in which acidophilic and
acidotolerant fungi represent an important component [51]. Strikingly, while a few acidophilic
fungi can still grow at pH 0 – the equivalent of car battery acid – others are also capable of optimal
growth at neutral and even alkaline pH (e.g., [52,53]).

These fungi have developed a wide spectrum of adaptation strategies to cope with acidic con-
ditions even more efficiently than their prokaryotic counterparts, such as the intracellular pH
regulatory system to keep the cytoplasmic pH near neutral (e.g., [54,55]) (Figure 2). The
major factor that contributes to intracellular pH is membrane impermeability, which controls
the proton influx inside the cell. Key players in fungal pH control are the vacuolar-type ATPase
(V-ATPase) and the P-type proton pump Pma1 acting in concert with a large array of other
transporters [56]. For instance, the Acidiella bohemica genome encodes the potassium uptake
permease (KUP) system, cation transporters, H+-transporting ATPases, and several
symporters to prevent the inflow of protons and to pump excess protons out of the cell [57].
Moreover, fungi deploy certain proton transport and pH control mechanisms not shared with
other eukaryotes; these regulators of cellular pH may therefore be accounted as potential
antifungal targets. There is also evidence that acidophilic fungi are highly resistant to heavy
metals and that can efficiently sequester a plethora of these elements [58]. Data obtained
with a Penicillium sp. isolate, for instance, suggested that the mechanism of specific copper
sequestering (33% at 100-mM Cu2+) depends on active cell growth, involving metal transport and
the formation of cellular inclusions.

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Key figure
Notable examples of extremophilic and extreme-tolerant fungi

Trends in Ecology & Evolution

(See figure legend at the bottom of the next page.)

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Box 3. Acidomyces acidophilus and its ability to survive in extremely acidic environments
Meristematic and melanized fungi have been found to be the predominant group in extremely acidic environments. This
group includes A. acidophilus, an anamorphic fungus belonging to the Capnodiales (class Dothideomycetes). This species
was first isolated by Starkey and Waksman [97] in the extremely acidic, sulfate-containing waters of industrial plants;
subsequently, more strains of this species were retrieved and identified successfully from various extreme environments,
acidic soils, and AMD biofilm [60]. The fungus grows optimally at pH values between 3 and 5, but is also capable of grow-
ing well at pH 1 [13] by maintaining the intracellular cytoplasm at a near-neutral pH. A. acidophilus was not only able to
tolerate extremely low pH, but it has also developed tolerance towards high concentrations of toxic metals and metalloids
such as Al, As, Cu, Fe, or U [60] and the ability to use 4-hydroxybenzene (4HB) and protocatechuic acid (PCA) under acidic
conditions. Recent proteomic and transcriptomic analyses of A. acidophilus have revealed a wide range of metal trans-
porters specific to iron, copper, zinc, magnesium, calcium, and nickel [61]. Despite the remarkable ability of this fungus
to survive in extremely adverse environments, A. acidophilus remains a poorly researched organism, and further work is
required to fully explore and maximize its potential in bioremediation and other biotechnological applications such as the
cleaning of contaminated soils or water and in the field of biocatalysis. Finally, with the advancement of omics tools, genetics,
and proteomics, the discovery of novel pharmaceutical extremozymes and biologically active compounds produced by
A. acidophilus under low-pH conditions could have important applications in applied scientific areas such as ecotoxicology.

Although data on fungal communities in acidic environments remain fragmentary, it is now evident
that the mycobiota of highly acidic substrates differ from those of less-acidic habitats. A large
number of mostly melanized specialists are taxonomically placed in the Teratosphaeriaceae
family (Capnodiales, Dothideomycetes). Among these, the remarkable example of Acidomyces
acidophilus, often successfully retrieved from various acidic environments as the sulfuric ore
AMD in Richmond (USA), is capable of growing at pH 0.5 [59–61] (Box 3). Another black fungus,
Exophiala sideris (Chaetothyriales, Eurotiomycetes), was isolated from an ancient gold arsenic
mine polluted with alkylbenzenes in Złoty Stok, Poland [52]. Hyaline fungi belonging to
Leotiomycetes and Sordariomycetes have been also frequently found in acidic environments
(e.g., from drainage waters of the Iberian Pyrite Belt) as well as the yeasts Rhodotorula spp.
(e.g., R. mucilaginosa, R. toruloides) and Cryptococcus spp. (C. acidotolerans, C. ibericus, and
C. metallitolerans) [62].

Fungi are attracted by radiation

Although life emerged on our planet at a time when there was much higher background radiation
[63], radiation is still a hazard on Earth. In particular, among major types of radiation, ionizing
radiation, depending on the type and length of exposure, damages DNA directly or indirectly
through the production of reactive oxygen species (ROS) [64].

Until recently, the bacterium Deinococcus radiodurans was largely considered the champion at
withstanding ionizing radiation (gamma radiation up to 20 kGy); however, some fungi are by far
the most resistant [65]. On 25 April 1986, one of the most devastating nuclear accidents occurred
when reactor 4 of the Chernobyl nuclear power plant exploded and high levels of radioactivity
released into the surrounding area raised radiation levels up to five orders of magnitude above
normal levels. Over the following 18 years, over 2000 fungal isolates were retrieved from
there and the so-called cooling-pool water of nuclear reactors [66,67]. Melanized fungal
species (i.e., Cladosporium spp.), which responded to ionizing radiation with directional growth
(i.e., radiotropism), were predominant [68]. Moreover, some filamentous and yeast fungal
species isolated from Chernobyl have also been detected on board the International Space

Figure 2. The figure shows examples of the most talented extremophilic and extreme-tolerant fungal species (squares), indicates the maximum resistance for each
species (gray rectangles; * indicates the optimal growth condition), and summarizes with major functional processes and prevailing adaptation strategies (light-blue
rectangles) in specific stressful environments. Abbreviations: EPS, extracellular polymeric substance; GATA-type TFs, GATA-type transcription factors that are
important for radiation sensitivity, including SRE1, BZP2, GAT5, GAT6, and HCM1; K, potassium; MAPK, mitogen-activated protein kinase; Na, sodium; P-type
ATPases, a large protein family that pumps ions and lipids across cellular membranes; Transm, transmembrane; Unsatur., unsaturated.

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Box 4. Cryomyces antarcticus, an extremely radioresistant cryptoendolithic black fungus

The rock-inhabiting black fungus C. antarcticus was first isolated from sandstone collected in the Antarctic Dry Valleys.
This coldest hyperarid desert is considered one of the best terrestrial analogs of Mars; there, microbes’ last chance for
survival is to find refuge inside the porous rocks forming the so-called microbial cryptoendolithic communities [98]. The
ability of C. antarcticus to withstand stresses has been widely demonstrated in more than 10 years of space and ground
experiments and it is now recognized as one of the best eukaryotic test organisms for astrobiological research. This fungus
survived and maintained its DNA integrity and ultrastructural stability, and its metabolic activity recovered after 18 months’
exposure to space and Mars-like conditions in low Earth orbit in experiments conducted by the European Space Agency
[65–99]. C. antarcticus also survived exposure to high doses of space-relevant gamma (6°Co; up to 117.07 kGy) – almost
30 000 times the tolerance of human cells and 5000 times that of Escherichia coli [65]. It also demonstrated the ability to
survive, despite a strong reduction in growth, even after 50 cycles of heating (+20°C) and cooling (−20°C) over 2 weeks,
ranges compatible with freeze-and-thaw cycles in space. Besides, despite its psychrophilic behavior, unexpectedly
C. antarcticus proved to survive at temperatures up to 90°C, an important skill in the light of space flights. In one of the first
experiments, it was proved to survive increasing UV-B (280–360 nm) irradiation doses corresponding to over five to eight
times the Antarctic terrestrial UV-B irradiance [99]. To date, melanins aside, the basic mechanisms of such impressive
radiation resistance remain unknown. Further studies are needed to untangle the unique regulatory network that provide
this fungus with this capacity to survive under the harshest conditions and to inform us on the limits of life on Earth.

Station (ISS) (e.g., [69,70]); the ISS-isolated species are of paramount significance for investi-
gating how microgravity and irradiation affect them compared with their ground counterparts.
The most notable example of radioresistant fungi is the rock-inhabiting Cryomyces antarcticus
(Box 4), but other fungal species are remarkably resistant. For instance, the dimorphic genus
Aureobasidium survived up to 10 000 Gy [71]; by contrast, the lethal whole-body dose for a
human is approximately 5 Gy, making us >1500-times more susceptible than fungi. Another
high-radiation environment where fungi have adapted is orbiting spacecraft with enhanced
irradiation, microgravity, and temperature extremes [72].

Fungi have evolved various survival strategies to cope with ionizing radiation differently from all
other inhabitants of the Earth. In recent work, the authors found that genes involved in the oxida-
tive stress response and DNA damage repair were upregulated in response to gamma radiation
in the yeast Cryptococcus neoformans [73]. Radioresistance is mainly due to melanins, unique
multifunctional and multiprotective pigments found in all lineages of the TOL; a 20–30-nm-thick
layer provides an efficient barrier by lowering the relative biological efficacy (RBE) of densely ion-
izing radiation [74,75]. Ionizing radiation may also induce growth in these highly pigmented fungi, a
phenomenon called radiosynthesis [76]. Irradiated melanized fungi, in contrast to their
hyaline counterparts, are able to convert electromagnetic energy into chemical energy to sustain
biological processes and survive ionizing radiation levels lethal to most (up to 30 000 times higher
than the lethal dose to humans) [77]. Melanins, bolstered by other protective molecules (e.g., carot-
enoids, trehalose, EPSs) contribute to the extraordinary resistance of fungi, protecting them from
not only radiation, but also dryness and salinity [73] (Figure 2). It is not by chance that melanized
fungi are the most frequently recovered under multiple stressing conditions.

Fungi are essential for the functioning of extreme ecosystems

Depending on the biome, fungi represent an average of 55–89% of microbial biomass [78,79];
thus, their activities can have large-scale consequences for global biogeochemical cycles. Fungi
play irreplaceable roles in the functioning of natural ecosystems; they are the main decomposer
of organic material to obtain energy, supplying members of the other biological compartments
with nutrients (e.g., carbon, nitrogen, phosphorus) that are typically not abundant in extreme envi-
ronments. The suites of traits determining how fungi respond to extremes also may determine how
these organisms contribute to ecosystem dynamics.

For instance, traits allowing fungi to maintain activity under unusually extreme conditions include
1,3-glucan and melanin production, leading to the deposition of fungus-derived carbon and

524 Trends in Ecology & Evolution, June 2022, Vol. 37, No. 6
Trends in Ecology & Evolution

contributing up to 50% of organic C [80,81]. The importance of the ecological role of Outstanding questions
xerophilic fungi is increasing over time in a warming and drying world, where drylands are The stunning adaptability of
expected to expand to up to 56% of Earth’s surface by the end of the century [82]. They microorganisms to thrive in extreme
environmental niches informs on the
play a key role acting as pioneers catalyzing ecosystem development at low water availability
limits and origin of life on Earth and
and driving saprotrophic processes in arid soils and exposed natural rock surfaces in drylands beyond. Discoveries on the vast
worldwide. distribution of microbial diversity
continue to raise the fundamental
question of what are the
Halotolerant and halophilic fungi as well play a paramount role in maintaining the ecological func-
physicochemical boundaries for life?
tions in global saline environments as, for example, a source of bioavailable hydrogen and thus
supporting the growth of hydrogen-consuming prokaryotes [83]. Targeted studies in this field So far, most studies in extreme
may revolutionize agriculture by appropriately using salt resistance genes and gene networks in environments have focused on
bacteria and archaea. Eukaryotes,
crops enabling them to grow in desert and saline environments on a drying and warming planet.
and fungi in particular, remain almost
Another important ecological aspect of halophilic fungi is the close relationship with their completely unexplored. What is the
xerophilic nature. For instance, many fungal species (e.g., Debaryomyces hansenii) were initially survival potential of extreme-tolerant
detected in hypersaline environments only and were successively found in other low-aw and extremophilic fungi? What are
the molecular mechanisms allowing
environments such aspolythermal Arctic glaciers [84]. them to thrive, adapt, and survive in
extreme environments?
In acidic environments, instead, fungi play a pivotal role as main contributors in the formation of
Fungal cells are surprisingly similar to
structured biofilms, which are the site of metal and mineral precipitation and provide a substrate
human cells, not only because both
for other, less-tolerant microbial populations [51]. Obligate acidophilic fungi – together with are eukaryotes but also from a
archaea, bacteria, and protozoa – are adept scavengers and rely on carbon originating as metabolic, genetic, and evolutionary
leakage or lysis products from chemolithotrophic acidophiles [51,85]. point of view; the study of extreme
fungi may inform on radioprotective
protocols for humans subjected to
Ultimately, radiotrophic fungi have the ability not only to act as a radiation shield to protect other anomalous irradiation. What are the
life forms but also to mineralize radionuclides and spatially redistribute materials in the environ- mechanisms protecting eukaryotic
ment, thus altering their potential availability to other microbial populations [86–88]. cells from radiation? To what extent
may fungal melanins protect cells
from radiation?
Concluding remarks and future perspectives
The presence and, in some cases, even dominance of fungi in diverse extreme environments of Extreme adaptation pushes fungi to
Earth is becoming more evident over time. Although numerous studies in the past decades produce novel biomolecules; studies
on these organisms provide useful
have considerably raised awareness of their stunning capacity to tolerate, persist, and reproduce products for various biotechnological
under conditions incompatible with life, many aspects remain largely unexplored. For instance, applications. Where can we search
halophilic fungi play an important role in ecological sustainability through bioremediation of herbi- for new extreme fungi producing new
biomolecules to exploit?
cides, pesticides, and heavy metals in extreme conditions by the production of extracellular
extreme enzymes. Fundamental knowledge of these fungi has also important biotechnological All of this knowledge will be important
implications such as for the prevention of spoilage of dry or salty preserved foods. The remarkable to understand the risk level to
tolerance of acidophilic fungi may open research opportunities for biotechnological processes humans during space exploration
(i.e., contamination of the ISS, pro-
(e.g., applicability to biometallurgical processing in mining activity) and in exploration for planetary
duction of mycotoxins, shifting to
and astrobiological studies in the search for life on acidic and hot planets such as our sister planet, opportunism). How might extreme
Venus. However, the resistance mechanisms of fungi against radiation remain not fully under- conditions and the space environ-
stood; melanins are pivotal protecting agents and even high-energy-harvesting pigments, but ment affect the physiological features
of fungi and the mycobiome, including
cannot alone explain the ability to withstand the highest doses of gamma rays and of heavy-ion cell metabolism, proliferation rate,
irradiation. The propensity of fungal hyphae to adsorb radionuclides may provide an alternative cell division, cell motility, and biofilm
means to effect the radionuclide cleanup of industrial effluent and inform us on bioremediation production?
programs for polluted environments. Moreover, as future space missions will require effective
materials for protection against various forms of radiation, the capacity of melanins to absorb
or screen multiple types of ionizing radiation makes those biomolecules strong candidates for
biomaterials for radioprotection. Melanins may also be used as cost-effective and sensitive
biological detectors of nuclear accidents or to protect individuals undergoing irradiation for
medical treatments or exposed to nuclear accidents.

Trends in Ecology & Evolution, June 2022, Vol. 37, No. 6 525
 Trends in Ecology & Evolution

In this perspective, an integrated approach untangling extreme-tolerant fungi, investigating the

enormous implications across multiple disciplines and the new breakthrough opportunities (see
Outstanding questions), will further advance our knowledge on the ecology and evolution of
extreme environments on Earth.

Acknowledgments
We apologize to all our colleagues working on fungi from extreme environments whose work could not be cited due to space
restraints and due to the requirement to cite recent articles primarily. C.C. and L.S. thank the Italian National Program for
Antarctic Research (PNRA) for continued support. C.C. is a recipient of a PNRA postdoctoral fellowship. J.E.S. is a CIFAR
fellow in the Fungal Kingdom: Threats and Opportunities program.

Declaration of interests
No interests are declared.

Author contributions
C.C. and L.S. developed the original idea and wrote the first draft of the review; J.E.S. contributed to the revisions of the
manuscript that resulted in the final submitted version.

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