Psychrophilic and psychrotrophic fungi: a comprehensive review

Abstract

This article reviews the comparative diversity of psychrophilic and psychrotrophic fungi, their adaptability mechanisms for survival and potential applications in biotechnology and pharmaceuticals. Fungi are able to grow and survive at low temperature and exist widely in polar and non-polar habitats. These cold regions are known for very low temperature, high ultra violet-B radiation, frequent freeze and thaw cycles and low water and nutrient availability. Most of the fungi adapt to such harsh conditions by evolving various strategies in their metabolism and physiology. Psychrophilic and psychrotrophic fungi are of importance in biotechnological and pharmaceutical fields due to their diverse characteristics developed or evolved due to their adaptation and survival in extreme environments, like; production of cold-active enzymes, pharmaceutical or bioactive metabolites and exo-polysaccharides, have potential for bioremediation and can also be used as biofertilizer.

Full text

REVIEW PAPER
Psychrophilic and psychrotrophic fungi: a comprehensive
review
Noor Hassan
.
Muhammad Rafiq
.
Muhammad Hayat
.
Aamer Ali Shah
.
Fariha Hasan
Ó Springer Science+Business Media Dordrecht 2016
Abstract This article reviews the comparative
diversity of psychrophilic and psychrotrophic fungi,
their adaptability mechanisms for survival and poten-
tial applications in biotechnology and pharmaceuti-
cals. Fungi are able to grow and survive at low
temperature and exist widely in polar and non-polar
habitats. These cold regions are known for very low
temperature, high ultra violet-B radiation, frequent
freeze and thaw cycles and low water and nutrient
availability. Most of the fungi adapt to such harsh
conditions by evolving various strategies in their
metabolism and physiology. Psychrophilic and psy-
chrotrophic fungi are of importance in biotechnolog-
ical and p harmaceutical fields due to their diverse
characteristics developed or evolved due to their
adaptation and survival in extreme environments, like;
production of cold-active enzymes, pharmaceutical or
bioactive metabolites and exo-polysaccharides, have
potential for bioremediation and can also be used as
biofertilizer.
Keywords Psychrophilic fungi  Psychrotrophic
fungi  Cold habitats  Diversity  Adaptation 
Applications
1 Background
Approximately, 85 % of Earth is cold with temperatures
ranging below 5 °C, permanently or seasonally (Hos-
hino and Matsumoto 2012; Margesin and Miteva 2011).
Cold habitats range from deep sea to high mountains
and from Antarctica to Arctic region. A large proportion
of cold environment consists of deep sea. Around 71 %
of the biosphere is occupied by oceans and provides
temperature from -1to4°C, the snow covers *35 %
of total terrestrial environment, frozen ground *24 %
of terrestrial environment, sea ice *13 % of the Earth
surface and glaciers *10 % of terrestrial environment,
providing a temperature of about -5 °C, along with
some other low temperature environments comprising
cold soils, lakes, caves and cold deserts (Singh et al.
2006; Margesin and Miteva 2011).
The living entities that have adapted to and live in
cold environments are termed as psychrophiles and
psychrotrophs. Psychrophiles and psychrotrophs are
defined as the organisms that can grow at or near 0 °C
(Ingram 1965; Morit a 1975). More specifically, the
optimum and maximum temperature for the growth
of psychrophiles is B15 and B20 °C, respectively.
Psychrotrophs grow well above 15 °C (Morita 1975;
Gounot 1991; Cavicchioli et al. 2002). ‘‘Obligate
psychrophiles’’ require 15 °C for their optimal growth,
\20 °
C for their maximal growth and 0 °C or lower
for their minimum growth (Turchetti et al. 2008) and
facultative psychrophiles grow well below 0 °C
(Raspor and Zupan 2006).
N. Hassan  M. Rafiq  M. Hayat  A. A. Shah 
F. Hasan (&)
Microbiology Research Laboratory, Department of
Microbiology, Quaid-i-Azam University,
Islamabad 45320, Pakistan
e-mail: farihahasan@yahoo.com
123
Rev Environ Sci Biotechnol
DOI 10.1007/s11157-016-9395-9

According to Deverall (1968), the psychrophilic
fungi have an optimum growth temperature near
10 °C or below and that 10 °C was the minimum
growth temperature requi red for most of the fungi.
Many researchers agree with Morita’s definition of
psychrophiles that psychrophilic fungi grow well at
15 °C or lower, whe reas, psychrotrophic fungi require
temperatures above 20 °C for their maximum growth
(Maheswari 2005; Cavicchioli et al. 2002; Robinson
2001). Bacteria and fungi are reported to remain viable
for at least thousands of years (Shi et al. 1997; Catranis
and Starmer 1991). Microorganisms that can be
recovered from the interior of deep-core samples of
Arctic and Antarctic ice are expected to be millions of
years old (Taylor et al. 1997). Various ancient fungi,
ranging from 10,000 to 140,000 years in age, have
been isolated and documented from Arctic and
Antarctic ice (Abyzov 1993; Christner et al. 2003).
2 Low temperature adapted life forms
The extremely cold environments such as Arctic and
Antarctic areas are dominated by microorganisms e.g.
bacteria, protists and fungi as well as microscopic
animals e.g. nematodes, rotifers, tardigrades, spring-
tails, mites (Hogg et al. 2006; Arenz and Blanchette
2011). The Arctic and Antarctica have been investi-
gated for psychrophiles, belonging to bacteria and
archaea, to some extent, for algae, but less for fungi
(Ma et al. 1999; Gunde-Cimerman et al. 2003; Abyzov
1993). Fungi not only survive but can also grow and
propagate in unusual environments. Diverse fungi
have been documented from different extreme envi-
ronments such as saline liquids (Gunde-Cimerman
et al. 2000), surface of dried rocks (Steflinger 1998),
ocean pits (Lopez-Garcia et al. 2001), dry and hot
deserts (Abdel-Hafez et al. 1989), very low pH
(Lopez-Archilla et al. 2001), as well as in the coldest
polar environments (Tojo and Newsham 2012). Cold
adapted fungal species are considered the most
effective eukaryotic extremophiles and have adapted
such strategies from prokaryotic extremophiles (Petro-
vic et al. 2002).
Many studies have found that primary biomass
production in cold ecosystems is facilitated by fungi
because of their endophytic and lichenic rel ationship
with several primary producers (Rosa et al. 2009;
Gianoli et al. 2004). Their ability to decompose wood
(carboxymethyl cellulose) suggests their role in recy-
cling of the nutrients in cold environments (Duncan
et al. 2006). Several fungi have been isolated from
various historic huts (built with woody materials) in
Antarctica, showing their biodegradation potential
(Blanchette et al. 2010
; Arenz and Blanchette 2009).
Moreover, well-known fungal pathogens such as
Pythium species have also been found in cold habitats
(Uspon et al. 2009; Bridge et al. 2008).
Psychrophilic fungi in cold environments are facing
numerous extreme situations, including coldest tem-
peratures (frequent freeze–thaw cycles), high salt
concentrations, low moisture content, extreme UV and
solar radiation and low nutrient availability. Such
extreme factors may vary from one site to another, but
all fungi must overcome such potential challenges
(McKenzie et al. 2003; Selbmann et al. 2002; Robin-
son 2001). To combat such harsh conditions, fungi
have adapted special features that are still not fully
understood. Although, several cold adaptive mecha-
nisms of psychrophilic fungi have been described, it is
assumed that a combination of strategies including
production of antifreeze proteins, compatible solutes
(glycerol), trehalose, polyols (acyclic sugar alcohols)
and cold-active enzymes, are employed by psy-
chrophiles for their survival (Brown 1978; Lewis
and Smith 1967; Weinstein et al. 2000; Robinson
2001).
3 Fungal diversity in cold habitats
Psychrophilic fungi exist in some of the coldest
environments throughout the world because of their
great efficiency of adaptation to cold environment
(distribution of cold adapted fungi throughout the
world is summarized in Fig. 1; Table 1). The presence
of psychrophilic and psychrotrophic fungi in cold
environments, including; permafrost (Golubev 1998),
cold water (Tosi et al. 2000), glacial ice (Ma et al.
1999), off-shore polar waters (Broady and Weinstein
1998), glaciers, ice sheets and shelves, fre shwater ice,
sea ice, icebergs (Tojo and Newsham 2012), have been
widely studied.
Cryoconite holes on glacier surfaces are the cold
niches of microbial diversity and activity. Multivariate
analysis of terminal-restriction fragment length poly-
morphism (T-RFLP) profiles of rRNA ITS amplicons
detected fungal communities in cryoc onite holes at
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123

Kongsfjorden, Svalbard, and were com pared to those
from the soils of adjacent moraine and tundra sites. It
was observed that the communities on glaciers with
contrasting ice-surface hydrology differed remark-
ably. Most of the fungi cultured from cryoconite
sediment were basidiomycetous yeasts or filamentous
Ascomycota (Helotiales/Pleosporales), including
aeroaquatic fungi, such as Articulospora and Vari-
cosporium, indicating their role in cycling of carbon in
cryoconite holes (Edwards et al. 2013).
ItwasreportedbyZumstegetal.(2012)that
fungi shifted from an Ascomycota-dominated com-
munity in young soils to a more Basidiomycota-
dominated c ommunity in old soils. Redundancy
analysis indicated that base saturation, pH, soil C
and N contents and presence of plant material
related to soil age, associated with the microbial
succession along the Damma glacier forefield in
central Switzerland.
Arbuscular mycorrhizal (AM) and dark septate
endophytic (DSE) fungi colonization in two dominant
plant species (Melandrium apetalum and Poa litwi-
nowiana) was observed on the forefront of Zhadang
Glacier in Qinghai–Tibet Plateau, China. It was
observed that AM dominated in M. apetalum and
DSE dominated in P. litwinowiana. A total of five AM
fungal spore morphotypes (Acaulospora capsicula,
Diversispora sp., Glomus constrictum, Glomus ebur-
neum and Glom us sp.) were found in the rhizosphere
soils. Two AM fungal phy lotypes: one Claroideoglo-
mus phylotype from roots and one seaweed, also
thought to be endemic phylotype from spores were
identified (Pan et al. 2013).
3.1 Antarctica
Approximately, 99 % of the Antarctica continent is
covered by ice throughout the year (Fox et al. 1994).
The climate of Antarctica is one of the coolest and
driest on the Earth, however, it contains variable
climatic regions throughout the continent. The Antarc-
tica is grouped into three different regions including
the continental Antarctic, the Sub-Antarctic and the
Maritime Antarctic (Peck et al. 2006). The biodiver-
sity of fungi has been studied in different areas of the
Antarctic continent (Onofri et al. 2005a ; Bridge and
Worland 2004). Biodi versity studies range from the
floristic (Onofri and Tosi 1992; Mercantini et al.
1993), ecophysiologic (Tosi et al. 2002; Onofri et al.
2000), at molecular level (Vishniac and Onofri 2002)
and phylogenetic (Selbmann et al. 2005).
Many mycological studies carried out in Antarc-
tica, comprised different fungi that exist in lakes
(Brunati et al. 2009; Goncalves et al. 2012), soil,
historic woodlands (Fell et al. 2006; Arenz et al. 2006)
as well as live on macroalgae (Loque et al. 2010) and
on plants (Uspon et al. 2009; Rosa et al. 2009). About
0.6 % of fungi (water mold s, Kingdom Chromista)
and 99.4 % true fungi including yeasts (unicellular),
and filamentous fungi (phylum Ascomycota, Basid-
iomycota, Chytridiomycota and Zygomycota) have
been reported from Antarctica (Onofri et al. 2005b).
Fig. 1 Distribution of cold
adapted fungi in different
niches. Distribution of cold
adapted fungi in different
regions of the world. 1
Hindu Kush, Karakoram,
Himalaya (HKKH), 2
European Alps, 3 Iceland, 4
Svalbard, 5 Arctic Ocean, 6
Greenland, 7 Canadian
Arctic Islands, 8 North USA
(Alaska), 9 Western USA
(Utah), 10 North Pacific
Ocean, 11 South America
(a Bolivia, b Patagonia), 12
Antarctica, 13 Indian Ocean,
14 South Pacific Ocean (for
detail refer to Table 1)
Rev Environ Sci Biotechnol
123

Paleobiological and paleoecological studies have
shown that the Antarctic fossil fungal biota was
present in degraded organic material, which proposes
that perhaps they were initially sapr ophytic and acted
as main decomposers (White and Taylor 1988;
Stubblefield and Taylor 1983).
Blanchette et al. (2010) isolated 69 filamentous fungi
from Nimrod Hut, Cape Royds, Antarctica that
included the genera Cadophora,followedbyThielavia
and Geomyces. Thielavia was studied in the Ross Sea
Region (Blanchette et al. 2010), also reported from
lichen on King George Island (Stchigel et al. 2001).
Arenz et al. (2006) studied various filamentous
Ascomycetes (New Harbor), Basidiomycetes (Allan
Hills), Ascomycete yeasts, Geomyces sp. (Mt Fleming)
and Zygomycetes (Lake Fryxell Basin). Duncan et al.
(2006) isolated filamentous fungi from Terra Nova Hut
which were mainly cold active and grow at 4 and 25 °C.
Geomyces pannorum is reported from many locations
of Antarctica (Loque et al. 2010;Rosaetal.2010;
Arenz and Blanchette 2011) which were thought to be
indigenous (Vishniac 1996) and keratinophilic (Mar-
shall 1998). The Geomyces and Cadophora sp. are
widely present in Antarctica (Blanchette et al. 2010),
playing significant role in the decaying and nutrient
recycling (Arenz and Blanchette 2009; Arenz et al.
Table 1 Geographical distribution of cold adapted fungi in the world
No. Region Sampling site References
1 HKKH (non polar) 1. Kumaun, Himalaya Sati et al. (2014)
2. Pangong Lake, Himalaya Anupama et al. (2011)
3. Nainital Kumaun, Himalaya Sati et al. (2009)
2 European Alps 1. Damma glacier, Swiss Alps Brunner et al. (2011)
2. Forni and Sforzellina glacier, Ita. Alps Turchetti et al. (2008)
3. Stubaier glacier, Austria Margesin et al. (2007)
3 Iceland Iceland Richardson (2004)
4 Svalbard Kongsfjorden glaciers Sonjak et al. (2006)
Fujiyoshi et al. (2011)
5 Arctic Ocean 1. Franz Josef Land Bergero et al. (1999)
2. Kongsfjorden glaciers Sonjak et al. (2006)
6 Greenland 1. GISP2 and Dye-3 sites Ma et al. (2000)
7 Canadian Arctic Islands Keewatin, Baffin Island, Ward Hunt Iceland,
Saskatoon Island
Allen et al. (2006)
Ellesmere Island Olsson et al. (2004)
8 North USA Alaska Deslippe et al. (2011)
9 Western USA Utah state Kuddus et al. (2008 )
10 South Pacific ocean Peru Margin and Trench Edgcomb et al. (2010)
11 South America Bolivia Flakus and Kukwa (2012)
Patagonia Garcia et al. (2013)
12 Antarctica 1. Peninsula Laura et al. (2014)
2. Intertidal transects, rocky coastline, Antarctica Laura et al. (2013)
3. King George Island Vivian et al. (2013)
4. Admiralty Bay, King George Rosa et al. (2010 )
5. Livingston Island, West Antarctica Kostadinova et al. (2009)
6. Schirmacher Oasis Singh et al. (2006 )
7. King George Island Stchigel et al. (2003)
13 Indian Ocean Central Indian Basin Singh et al. (2010 , 2012),
Raghukumar et al. (2004),
Damare et al. (2006a, b)
14 South Pacific Ocean region Canterbury (New Zealand) Ciobanu et al. (2014)
Rev Environ Sci Biotechnol
123

2006). In Antarctica, Penicillium species have been
isolated from lakes (Ellis-Evans 1996), soils (Azmi and
Seppelt 1998), historical woodlands (Arenz et al. 2006)
and macroalgal thalli (Loque et al. 2010).
The extreme environment of Antarctica is accom-
panied by stressful conditions (Pugh 1980). Fungal
genera including Aspergillus, Candida, Cryptococcus,
Cylindrocarpon, Glomerella, Golovinomyces, Peni-
cillium and Phoma have been reported from marine
sediments (Singh et al. 2011; Lai et al. 2007; Calvez
et al. 2009). G. pannorum, Thelebolus sp., mainly
Thelebolus microsporus and Mortierella sp. are
reported from Antarctic Peninsula (Goncalves et al.
2012; Arenz and Blanchette 2011). Thelebolus sp. is
widely present in many other sites such as in benthic
mats of Antarctic lakes (Brunati et al. 2009). The genus
Antarctomyces is represented by the type species A.
psychrotrophicus, isolated from Antarctic soil and
seaweed, also thought to be endemic to Antarctic
environment (Arenz et al. 2006; Arenz and Blanchette
2011;Stchigeletal.2001; Loque et al. 2010).
King George Island, South Shetland archipelago,
Antarctica, have an average temperature of 2 °C (min
-20 °C, max 10 °C). Stchigel et al. (2003) reported
two species of Ascomycetes, Thielavia antarct ica and
Apiosordaria antarctica, from King George Island
(Antarctica). Moreover, Azmi and Seppelt (1997)
reported many fungi from soils e.g. Cadophora
malorum
and from moss (Tosi et al. 2002) in the
Windmill Islands, Antarctica. Mycological investiga-
tions in Victoria Land have been carried out by many
authors, who provided lists of fungi present in the
surrounding territories of that area (Broady et al.
1987). Park et al. (2015) studied lichen associated
fungal species from King George Island, Antarctica,
by pyrosequencing of eukaryotic large subunit (LSU)
and revealed that fungal communities belonged to the
Arthoniomycetes, Eurotiomycetes, Lecanoromycetes,
Leotiomycetes, Sordariomycetes (Ascomycota) and
Tremellomycetes and Cystobasidiomycetes (Basid-
iomycota). Litova et al. (2014) isolated Aspergillus,
Penicillium and Alternaria as common genera from
Antarctic soil probes.
McMurdo Dry Valley, one of the m ost unreceptive
environments on Earth is favorable for the growth of
microorganisms which love to grow in ice- free
area including black meristematic fungi, persistent
members of endolithic microbial communities such
as lichen-dominated cryptoendolithic communities
(Nienow and Friedmann 1993; Selbmann et al. 2008).
Black meristematic fungi are known to be tolerant to
extreme environmental conditions. The black fungi
constitute melanized cell walls and m eristematic
development, which support survival and persistence
in hostile environmental conditions (Selbmann et al.
2010). They are commonly isolated from environ-
ments that are almost devoid of other eukaryotic life-
forms, including saltpans (Plemenitas and Gunde-
Cimerman 2005), acidic and polluted sites (Baker
et al. 200 4 ;Isolaetal.2013) and exposed rocks in dry
and extremely hot or c old habitats (Staley et al.
1982). In Antarctica, the black meristematic fungi
have been isolated from Northern and Southern
Victoria Land (Selbmann et al. 2005; 2013).
Pythium belong to oomycete genera and are well-
known fungal pathogens, usually infect small plants
and arthropods in Antarctica (Humber 1989; Bridge
et al. 2008). Pythium species, such as Pythium tenue,
Neozygites sp. etc., have been reported from plants in
vegetated sub-Antarctic islands such as Kerguelen,
Macquarie and South Georgia (Knox and Paterson
1973; Hughes et al. 2003; Bridge and Denton 2007).
Bridge et al. (2008) isolated pathogeni c Pythium
species from Antarctic hair grass Deschampsia
antarctica in Signy Island, South Orkney Islands.
Pathogenic Pythium species have also been reported
from different Antarctic plants (Uspon et al. 2009;
Bridge et al. 2008). The endophytic fungi have also
been investigated in various plants such as D. antarc-
tica and Colobanthus quitensis
(Rosa et al. 2009;
Gianoli et al. 2004). Taxonomically, most endophytic
fungi were Ascomycetes but also belonged to Basid-
iomycota and Zygomycota (Huang et al. 2001). The
endophytic fungal groups can help the plants to face
abiotic (temperature, pH, osmotic pressure) and biotic
stresses (bacteria, fungi, nematodes, and insects)
(Rodriguez et al. 2001).
3.2 Arctic
The cold Arctic region comprises northern fringes of
Ellesmere Island as well as Svalbard, Franz Joseph
Land, Novaya Zemlya and the New Siberian Islands, all
in the region of 80–85°N. The Arctic is divided into five
bioclimatic sub zones (A–E), with A being the coldest
and E the warmest (Ludley and Robinson 2008).
Fungi are found in all aerobic ecosystems, coloniz-
ing a diversity of substrates and performing a wide
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diversity of functions, some of which are not well
understood (Table 2). Yeasts, black yeast-like fungi,
melanized filamentous species as well as representa-
tives of Aspergillus and Penicillium seem to be
dominant among the mycobiota adapted to cold and
saline niches (Cantrell et al. 2001).
Franz Joseph Land is a high-arctic desert or semi
desert archipelago. The average air temperature during
summer, ranges from 0.2 to 1.3 °C, with an average
for the year as 14.1 °C (Bergero et al. 1999). Bergero
et al. (1999) have isolated fungal species of Geomyces,
Phialophora, Phoma, Acremonium, Thelebolus and
Mortierella from Franz Joseph Land. The filamentous
Penicillium species have been inve stigated in three
different polythermal glaciers of Arctic region (Sval-
bard, Norway) (Sonjak et al. 2006). The most
predominant species was Penicillium crustosum.
Thirty-two genera of decomposer basidiomycetes,
having around 100 species, have been collected and
surveyed in Arctic tundra in North America (Lydolph
et al. 2005). The Mycorrhizal fungal communities are
common in arctic environment. They are important for
growth and survival of their host plants as they provide
water and limiting nutrients in exchange for photo-
synthetic carbon (Smith and Read 2002). Some of the
ectomycorrhizal fungal communities have been inves-
tigated in the Arctic–Alpine ecosystems that were
associated with Dryas octopetala or chron osequences
(Cripps and Eddington 2005; Harrington and Mitchell
2002; Jumpponen et al. 2002). The Arbuscular myc-
orrhizal (AM) fungal communities have also been
found in Arctic ecosytems (Allen et al. 2006; Olsson
et al. 2004). Ectomycorrhizal fungi are widely
distributed in arctic and alpine habitats on all conti-
nents. Some widely distributed EMF (Ectomycor-
rhizal fungi) genera include Inocybe, Cortinarius,
Hebeloma, Russula, Thelephora, Tomentella, Ceno-
coccum and Laccaria (Deslippe et al. 2011; Fujiyoshi
et al. 2011).
There are about 2600 morphologically described
macrofungi and at least 150 ectomycorrhizal species
reported from Svalbard, the Russian Arctic and
Iceland (Borgen et al. 2006). EMF have been collected
from two arctic ectomycorrhizal host plants, Salix
Table 2 Fungal species/genera and their distribution in different Artic and Alps regions
No. Distribution sites Fungal genera/species References
1 Franz Joseph Land Geomyces, Phialophora, Phoma, Acremonium,
Thelebolus and Mortierella
Bergero et al. (1999)
2 Colorado Front Range Saccharomyces cerevisiae, Taphrina communis,
Neolecta vitellina, Phialophora gregata,
Fesctuca psuedostems, Hymenoscyphus ericae
and Phialophora finlandia
Schadt et al. (2001)
3 Lyman Glacier Cortinarius decipiens, C. tenebricus, Inocybe
lacera, Laccaria cf. Montana, Suillus cavipes
Jumpponen et al. (2002)
4 Northern Fennoscandia, Arctic Anthracoidea echinospora and Anthracoidea
heterospora
Scholler et al. (2003)
5 Western Beringia, Arctic Acanthophysium, Mortierella, Bensingtonia,
Cryptococcus, Sordaria, Phanerochaete and
Phialocephala
Lydolph et al. (2005)
6 Svalbard, Norway Penicillium crustosum and other penicilium
species
Sonjak et al. (2006)
7 Tyrolean Alps Cenococcum geophilum, Sebacina sp.,
Tomentella sp. and Cortinarius sp.
Muhlmann and Peintner (2008)
8 Cliff ledges, Arctic–Alpine Cenococcum geophilum, Thelephoraceae sp.,
Cortinarius sp., and Sebacinales sp.
Ryberg et al. (2009)
9 Arctic tundra Cortinarius sp. and Russula Deslippe et al. (2011)
10 Austre Broggerbreen, Svalbard Geopora sp. and Cenococcum sp. Fujiyoshi et al. (2011)
11 High Arctic Cryptococcus, Rhizosphaera, Mycopappus,
Melampsora, Mrakia, Tetracladium,
Phaeosphaeria, Venturia, and Leptosphaeria
Zhang and Yao (2015)
Rev Environ Sci Biotechnol
123

arctica and Dryas integrifolia that belong to the major
genera Thelephora, Tomentella, Sebacina, Inocybe,
Cortinarius, Russula, Hebeloma, Laccaria and Cla-
vulina are characteristic of arctic and alpine environ-
ments (Muh lmann and Peintner 2008; Ryberg et al.
2009; Deslippe et al. 2011). Dark septate endophytes
are present in the Arctic and Alpine plant roots but
there is less knowledge about their phylogenetic
antiquities or their effects on host plants (Jumpponen
and Trappe 1998; Schadt et al. 2001). As in Antarctica,
some of the fungal pathogens are also present in Arctic
habitat, for example obligate basidiomycetes plant
pathogens in Arctic ecosystems are Exobasidium
(Nannfeldt 1981; Ing 1998) and rusts (belonging to
Basidiomycetes that consist of a large group of
obligate plant parasites) and smuts (obligate parasitic
fungi of the genus Anthracoidea) (Scholler et al. 2003;
Singh and Palni 2011). Zhang and Yao (2015)
assessed the diversity and dissemination of endophytic
fungal communities in High Arctic using 454 pyrose-
quencing by targeting the ITS region and found that
the Cryptococcus, Rhizosphaera, Mycopappus, Me-
lampsora, Tetracladium, Phaeosphaeria, Mrakia,
Venturia, and Leptosphaeria were predominant fungal
genera.
Cryoconite holes have biogeochemical, ecological
and biotech nological importance. Culturable psy-
chrophilic yeast and filamentous fungi from cry-
oconite holes at Midre Love
´
nbreen glacier have been
studied. The microbes were identified through con-
ventional and DNA sequencing techniques as Cryp-
tococcus gilvescens, Mrakia sp., Rhodotorula sp.,
Phialophora alba and Articulospora tetracladia.
Rhodotorula sp. expre ssed high amylase, while Cryp-
tococcus gilves cens
showed high lipase activity.
Mrakia sp. showed phospha te solubilization between
4 and 15 °C. Filamentous fungi and yeast in the
cryoconite holes drive the process of organic macro-
molecule degradation through secretion of cold-
adapted enzymes, thereby having important role in
nutrient cycling in these sub-glacial environments
(Singh and Singh 2012).
Ribosomal DNA seque nces were amplified from
sub-fossils of the ascolichen Umbilicaria cylindrica
(L.) Delise ex Duby collected at the ablating edges of
Greenland glaciers. Phylogenetic analysis indicated
that they were not closely related to those of the
lichen-forming fungus but rather represented 2
groups of psychrophilic basidiomycetes (orders
Cystofilobasidiales and Sporidiales) and one group
of ascomyc etes (order Leotiales). Sporidiales and the
Leotiales, include fungi previously detected from
grass clothing of the Tyrolean Iceman desiccated and
frozen for over 3000 years and also in 2000 and
4000 year-old ice core samples from northern Green-
land. Cystofilobasidiales were identical to those of the
basidio yeast saprobe Mrakia frigida (DePriest et al.
2000).
3.3 Deep sea
Deep sea is an environment of extreme conditions,
such as high hydros tatic pressure and low nutrient
availability, with an average temperature between -1
and 4 °C in most areas of deep sea or high temperature
([400 °C in hydrothermal vents) and absen ce of
sunlight. Living organisms in deep sea are considered
to be adapted to cold environments. Yeast diversity
commonly found in deep sea is represented by
Rhodosporidium spp., Rhodotorula spp., Candida
spp., Cryptococcus spp., Pichia spp., Sporobolomyces
spp. and Trichosporon spp. As compared to prokary-
otic microorganisms, yeasts in deep-sea environment
remain relatively underexplored, with few studies
carried out on their physiology (Nagano et al. 2013).
The deep-sea is usually defined as the area of ocean
beyond the photic zone (e.g. [200 m depth). Due to
coldness, darkness and stability of the deep-sea
bottom, it was presumed that most of life forms may
be present in a suspended state.
Singh et al. (2010) have isolated filamentous fungi
and yeasts that belong to phylum Ascomycota and
Basidiomycota from sediments of Ce ntral Indian
Basin. Similarly, Aspergillus sp., Fusarium sp.,
Curvularia sp., Penicillium sp. and Cladosporium
sp. have been isolated at 5 °C from deep-sea sediment
core of the Indian Ocean (Raghukumar et al. 2004;
Damare et al. 2006a, b). Singh et al. (2012) also
investigated fungal diversity in two sediment cores
*40 cmb sf (cm below seafloor) at a depth of
*5000 m in the Central Indian Basin, by culture-
dependent as well as culture-independent approaches
and recovered a total of 19 culturable fungi, of which
two showed similarity to Hortaea werneckii and
Aspergillus versicolor. Some of the fungi, such as
Cerrena, Hortaea and Aspergillus sp., were recovered
by culture-depende nt as well as culture-independent
approaches.
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Most of the fungi of deep-sea environments are of
psychrotrophic nature, but in some cases, deep-sea
fungal isolates can also grow well at 30 °C than 5 °C
(Damare and Chandralata 2008; Singh et al. 2010).
Moreover, fungal communities belonging to Ascomy-
cota and Basidiomycota phylum have been reported
from the deep marine subsurface by DNA and RNA-
based clone library analyses (Edgcomb et al. 2011;
Orsi et al. 2013 ; Burgaud et al. 2013). Zhang et al.
(2015) studied the presence of fungal communities in
eight marine sediments of Kongsfjorden (Svalbard,
High Arctic) using 454 pyrosequencing and revealed
the Pichia, Fusarium, Alternaria and Malassezia as
common fungal genera. Zhang et al. (2013) explored
the diversity of fungal communities in different deep-
sea sediment samples of the South China Sea by
culture-dependent methods and isolated Asperg illus,
Cladosporium and Penicillium as dominant genera. In
an another study in the East India Ocean, fungal
diversity of sediments from a depth of 4000 m have
been studied using a mixture of metagenomics and
conventional methods (Zhang et al. 2014). This tactic
stemmed in the salvage of a total of 45 fungal
operational taxonomic units (OTUs) and 20 culturable
fungal phylotypes including fungal genera Aspergillus ,
Alternaria, Cladophialophora, Cladosporium, Euro-
tium, Fusarium, Geomyces , Hypocrea, Leptosphaeria,
Mortierella, Phoma, Rhizoscyphus and Trichoderma.
3.4 The European Alpines
About 200 km long and 800 km wide, European
Alpines extends across eight European Alpine coun-
tries. The highest peaks of Alpine mountain are
approximately 4400–4800 m. The mean temperature
in the valley floors range from -5to4 °C to as high as
8 °C during January, and in July it range between 15
and 24 °C. The variability of climate in European Alps
is influenced by the North with huge Eurasian
terrestrial physique, the Atlantic weather systems
and Mediterranean Sea (Auer et al. 2005; Beniston and
Jungo 2002; Begert et al.
2005).
The microbiological analysis of 78 samples taken
from a bor eal bog in Western Siberia and from a
tundra wetland soil in Alaska showed the presence of
23 yeast species belonging to the genera Bullera,
Candida, Cryptococcus, Debaryomyces, Hansenias-
pora, Metschnikowia, Mrakia, Pichia, Rhodotorula,
Saccharomyces, Sporobolomyces, Torulaspora,and
Trichosporon. Peat samples from the boreal bog were
dominated b y eurytopic anamorphic basidiomycetous
species, such as Rhodotorula mucilaginosa and
Sporob ol om yc e s r o se us , a nd by the ascomycetous
yeasts Candida spp. and Debar yom yces hanseni i.
These samples also contained Candida paludigena
and Schizoblastosporion starkeyi-henricii. The wet-
land Alaskan soil was dominated by one yeast species
(Cryptococcus gilvescens), which is a typical inhab-
itant of tundra soils (Poliakova et al. 2001).
In European Alps, psychrophilic yeasts have been
documented in ice, subgl acial sediments and melted
water from two different Italian alpine glaciers
including C. gilvescens , Aureobasidium pullulans
(about half of the total), Cryptococcus terricolus,
Mrakia gelida, Naganishia globosa, Rhodotorula
glacialis, Rhodotorula psychrophenolica, Rhodotor-
ula bacarum, Rhodotorula creatinivora and Rhodo-
torula larynges (Turchetti et al. 2008). Margesin et al.
(2007) described three new psychrophilic species of
the genus Rhodotorula comprises Rhodotorula psy-
chrophila, R. psychrophenolica and R. glacialis col-
lected from soil of an alpine railway area, from mud in
the thawing zone of a glacier foot and from glacier
cryoconite, respectively. Buzzini et al. (2005) reported
the presence of viable yeast cells in melted waters
running off from glaciers in Italian Alps. Similarly, a
novel species of the genus Acaulospora has also been
reported from numerous mountains in Southern Chile
and Switzerland at 550–1600 and 1850–2050 m,
respectively (Fritz et al. 2011). Acaulospora alpine a
novel arbuscular mycorrhizal fungal species have
been reported from Swiss Alp (Oehl et al. 2006).
Brunner et al. (2011) isolated 45 fungi from sediments
of fine granite of Damma glacier in the central Swiss
Alps. A set of fungal species isolated from fine granitic
sediment of the non-vegetated forefield of the Damma
Glacier showed a high potential to weather powdered
granite material in batch experiments. In particular,
the zygomycete fungi Mucor hiemalis, Mortierella
alpina, Umbelopsis isabellina and the ascomycete
fungus Penicillium chrysogenum dissolved the granite
powder most efficiently. It was shown that high
concentrations of Ca, Fe, Mg and Mn in the solutions
were the result of release of high amounts of organic
acids, mainly citrate, malate and oxalate (Brunner and
Schlumpf 2014). Muggia et al. (2015) isolated 248
lichen-associated fungi that belong to the Chaetothyri-
omycetes and Dothideomycetes, while a slight section
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represents Sordariomycetes and Leotiomycetes, from
the Koralpe mountain range in the south eastern rim of
the Austrian Alps. A total of 347 endophytic fungi
were isolated from alpine plants, Rhodiola crenulata,
Rhodiola angusta and Rhodiola sachalinensis, repre-
senting at least 57 genera in 20 orders of four phyla,
namely, Ascomycota (88.89 %), Basidiomycota
(2.78 %), Zygomycota (1.11 %), and Glomeromycota
(0.56 %), which displayed high copiousness and
diversity (Cui et al. 2015). Coleine et al. (2015)
studied the presence of fungi in Alpine Tarfala Valley
and the data showed that the mainstream of fungi
isolated belonged to the Ascomycota and Cryptococ-
cus gilvescens and Pezoloma ericae were the most
frequently isolated species.
3.5 Glaciers of Hindu Kush–Karakoram–
Himalayas (HKKH)
Hindu Kush–Karakoram–Himalayas hosts more than
20,000 glaciers, of which 5000 are in the Karakor am
range (Inman 2010) and more than 12,000 are in the
Himalayas that cover about 60,000 km area (Kaab
et al. 2012). The HKKH glaciers have not been
properly investigated earlier for presence of psy-
chrophilic and psychrotrophic fungi and very few
studies have been carried out. Five species of aquatic
hyphomycetes belonging to the genus Lemonniera and
aquatic hyphomycete, Tetracladium nainitalense a
root endophyte has been isolated from Kumaun
Himalaya, India (Sati et al. 2009, 2014; Sati and
Belwal 2005). Anupama et al. (2011) reported the
psychrophilic and halotolerant Thelebolus mi-
crosporus from the Pangong Lake, Himalayan region.
Singh and Palni (2011) have collected 35 species
belonging to 7 families of rust fungi from herbaceous
and shrubby hosts in central Himalayan region.
Moreover, 25 psychrophilic yeasts have been identi-
fied from Roopkund Lake soil of Himalayas, India
(Shivaji et al. 2008). Wang et al. (2015) studied
glaciers on the Qinghai–Tibet Plateau for the presence
of cold-adapted fungi and isolated 1428 fungi, of
which 150 were identified and Phoma sclerotio ides
and Pseudogymnoascus pannorum were the most
dominant species and Helotiales (Leotiomycetes,
Ascomycota) was the most commonly encountered
group and also described six new species; P. antarc-
tica, P. lutea, P. olivacea, T. ellipsoideum, T. globo-
sum and T. psychrophilum.
Recently, few studies about the diversity of fungi in
Hindu Kush and Karakoram mountain ranges of
Pakistan have been conducted. A total of 77 fungal
isolates were isolated from Batura, Passu and Siachen
glaciers, representing 24 fungal genera, one class and
one order (Hassan 2015). Most of the fungi from these
glaciers belong to genus Penicill ium
, Cladosporium,
Mrakia, Geomyces, Leotiomycetes, Thelebolus, Tri-
choderma, Pueraria, Pseudogymnoascus, Beauveria,
Pseudeurotium, Fontanospora, Cordyceps, Cado-
phora, Periconia, Cryptococcus, Trametes, Mortier-
ella, Scopulariopsis, Candida, Antrodia,
Sporobolomyces, Phoma, Eupenicillium, while one
fungal species to order Pleosporales and class Doth-
ideomycetes each. Antrodia juniperina is isolated for
the first time from any polar or non-po lar habitats. In
another study, Nadeem (2014) isolated 57 fungal
strains from Tirich Mir glacier, Pakistan, with Al-
ternaria, as predominant genus.
4 Adaptability in cold environment
Psychrophilic fungi in cold habitats of polar and non-
polar regions are subject to extreme low temperature
and various other stress conditions including high
repeated freeze and thaw cycles (Ruisi et al. 2006), UV
radiation (mainly UV-B), reduced moisture, increased
salinity, low nutrient availability and desiccation.
These potential challenges and stress conditions vary
considerably from one environment to the other, and
fungi must counter it for their survival. Coldness is a
relative name (Smith 1993), which is defined as
freezing temperature with a limit of -70 °C, beyond
which life process stops (Robinson 2001). Such low
temperature and regular freeze thaw cycles are also
provided by Polar terrestrial regions (Montiel 2000).
Low temperature influence fungal cells by increasing
water viscosity, denaturing of proteins, slowing of
chemical reactions and decreasing of membrane
stability (Crowe et al. 1992; Russell 1990). Water
unavailability and salinity are common in Antarctic
island due to extreme dryness. Antarctica has almost
70 % of the world’s fresh water which is entirely
covered in ice. High winds enhance evaporation that
leads to drought and the key source of humidity is
fleeting water melted due to solar heating during the
austral summer. Due to increased evaporation, salt
concentrations in the soil, shallow ponds and rocks are
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frequently elevated (Nishiyama 1977), that produce
similar consequence of osmotic disparity as caused by
freezing (Gunde-Cimerman et al. 2003). UV-B is a
solar spectrum’s component that causes wide range of
harmful effects (Kerr and McElroy 1993) on the
environment due to which the whole productivity of
ecosystems may be affected. The consequences of
UV-B radiation (280–315 nm) have been observed on
fungal growth (Gunasekera et al. 1997; Newsham
et al. 1997). The significant detrimental effects of UV-
B have also been observed on several Antarctic
terrestrial fungi including G. pannorum, Phoma
herbarum, Mortierella parvispora, Pythium and Ver-
ticillium species (Hughes et al. 2003).
4.1 Adaptation characteristics
To thrive under extreme conditions, fungi have
adapted special mechanisms and features (Fig. 2).
However, all the mechanisms in psychrophilic fungi
are not completely known that allows them to survive
at low temperature (Weinstein et al. 2000; Smith 1993;
Snider et al. 2000; Russell 1990). To grow at low
temperature, it is necessary that all the cell components
of psychrophilic fungi must function properly (Russell
1990). Several tools of cold tolerance have been
documented in fungi, as mentioned earlier.
4.1.1 Plasma membrane fluidity maintenance
The first line of defense is the cell membrane that faces
the change coming from external environment. It is,
therefore, important to be stable and function properly.
Cell membrane consists of phospholipid bilayer and
proteins organized in various coinciding domains with
unlike fluidity features (Strancar et al. 2000; Simons
and Toomre 2000). Hence, a minute change can
considerably disturb membrane functions (Hazel and
Williams 1990). It is well established that the Antarc-
tic and other cold inhabitant microorganisms alter
membrane lipid conformation as a strategy of cold-
tolerance (Russell 1990). Extreme low temper ature
causes freezing and dehydration, damages cells by
changing the cell membrane lipids from liquefied
crystalline to gel phase and leads to disruption of
membrane function (Crowe et al. 1987). This
Pigments
Membrane fluidity by cis and branched PUFA *
Trehalose production
Antifreeze protein
Compatible solute (Mannitol, glycerol)
Extracellular Polysaccharide
Mycosporin
Melanin
Other cold shock proteins (CSP)
Nucleus
Mitochondria
Cell Membrane
Cell Wall
External glacial environmen
t
Fungal fruiting body
Genetic level adaptation
Fig. 2 A typical structure of psychrophilic and psychrotrophic fungi and their adaptability mechanisms in low temperature
environments, *Polyunsaturated fatty acids
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123

transition can be handled by an increase in fatty acids’
unsaturation. Various strains isolated from Antarctic
region including Cadophora fastigiata, Mortierella
alpine and Mortierella antarctica, produce arachi-
donic and linoleic acid, when grown at low temper-
ature and the change of fatty acid in cell membrane in
reaction to cold temperature has even been scrutinized
in Geomyces vinaceus and G. pannorum and in other
Antarctic strains (Maggi et al. 1991; Finotti et al.
1993). In a similar study, the presence of fatty
acids ‘stearidonic acids’ were also reported, in another
fungi Mortierella elongate only, formerly described in
psychrotrophic zygomycete, however the ergosterol
were not detected (Weinstein et al. 2000). The
increased membrane fluidity has been reported in
psychrotolerant yeast Rhodosporidium diobovatum
(Turk et al. 2011), indicating the role of unsaturation
of fatty acids in maintaining integrity and functionality
of plasma membrane at low temperature.
4.1.2 Compatible solute–polyols
Fungi produce various compatible solutes to overcome
the increased dehydration and osmotic stress due to
low temperature (Pascual et al. 2002). Glycerol is
supposed to be the utmost important compatible solute
(Brown 1978). Sugars, such as mannitol provides
cryoprotective ability during freeze or desiccation
(Feofilova et al. 1994). These solutes sustain the
function and integrity of cell membrane to stabilize it.
They can stabilize plasma membrane by sustaining
their functi on and integrity and complete dehydration
(Crowe et al. 1984, 1986). Grant (2004) observed an
increase in the concentration of mannitol and glycerol
to sustain the turgor pressure against heat mediated
decrease in the external water potential i (Grant 2004).
Mannitol might have role in cryoprotection (Wein-
stein et al. 1997), and is thought to be dynamic in water
stress protection (Lewis and Smith 1967). Polyols are
thought to act as buffering agents (Jennings 1984). The
potential cryoprotectant role of polyols in fungi is
revealed by comparing Humicola marvinii with H.
fuscoatra (Weinstein et al. 1997). Polyols (acyclic
sugar alcohols) are the principal soluble carbohydrates
in fungi (Lewis and Smith 1967). Polyol’s main
function in fungi is in osmoregulation and coenzyme
regulation (Jennings 1984 ) as well as protection
against damage due to freezing by lowering the
freezing point of intracellular fluid.
4.1.3 Trehalose
Trehalose is a disaccharide widely found in both
reproductive and vegetative stages in f ungi (Theve-
lein 1984
). Trehalose plays a key role in enh ancing
the resistance in fungi to environmental stress condi-
tion s, like freezin g, desiccation, dehydration and
extreme temperature (Lewis et al. 1995;D’Amore
et al. 1991). It has been documented that concentra-
tion of trehalose increases, when fungi is subjected to
low tempera ture and such changes have been seen in
excised alpine mycorrhizal roots (Niederer et al.
1992), H. marvinii, a psychrophile, (Weinstein et al.
2000)andHebeloma species of the arctic and
temperate regions (Tibbett et al. 1988a). Weinstein
et al. (2000) documented the increase of cryoprotec-
tive carb ohydrates at low temperature in H. marvinii,
such as ext racellular glycerol and intracellular tre-
halose, while in Mortierella elongate, only intracel-
lular trehalose, in field soils of maritime Antarctica. It
has also been documented that thermophilic fungus
Myceliophthora thermophila (growth optimum at
42 °C) has also s hown an increase in trehalose and
mann itol content and a de crease in inositol content
when ex posed to low temperature stress (growth at
26 °C), suggesting a role for trehalose and mannitol in
the fungal response to low temperature (Feofilova
et al. 1994). Trehalose has been found to be the most
effective cryoprotectant during desiccation or freez-
ing and help in main taining membrane integrity and
function (Crowe et al. 1986).
4.1.4 Cold-active enzymes
The fungi and other microbial proliferation at
extremely low temperature is extensively supported
by cold-adapted enzymes as they provide high flex-
ibility and active site complementarity for substrate,
ensuing an increased specific activity at low energy
cost (Weinstein et al. 2000; Kuddus et al. 2011). Such
flexibility is accomplished by combining structural
features including, increased surface residue charge,
decreased ionic and electrostatic interactions and
deterioration in core hydrophobicity (Weinstein et al.
2000). The tractability also comprise substitution of
proline by glycines in surface loops, decreased in
lysine–arginine ratio, low subunit and inter domain
interaction and reduced aromatic interaction (Gerday
2000; Gianese et al. 2001).
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Several Antarctic fungal species produce cold
dynamic enzymes (Fenice et al. 1998) that may
highlight the struggle of the fungi to flourish at low
temperatures. Although, some Antarctic fungal spe-
cies have wide enzymatic capabilities that intensify
probability of persistence under hostile conditions
(Fenice et al. 1997). Fungal strains isolated from
Antarctic soil has been documented to have an
enzymatic activity at low temperature e.g. psy-
chrophilic fungal species, H. marvinii, H. fuscoatra
and H. marvinii, responsi ble for production of extra-
cellular protease and inorganic phosphate solubiliza-
tion in solid media at 15 °C, have also been
documented from Antarctic soil (Weinstein et al.
1997). Similarly, Fenice et al. (1997) reported differ-
ent fungal strains including mitosporic fungi, yeast
like fungi, Ascomycetes and sterile mycelial strai ns to
produce various extracellular enzymes like DNase,
protease, phosphatase, amylase glucose oxidase,
lipases and polygalacturonase. The strains were iso-
lated from diverse locations of Victoria Land (Antarc-
tic continent). The ectomycorrhizal fungal strains
belonging to genus Hebeloma have been screened for
proteolytic and phosphatase activity (Tibbett et al.
1988a, b).
Enzymes can als o act as a virulence factor in
animals as well as in plants. One of such enzyme in
plants is keratinase. Out of 72 positive samples
(67.3 %), a total of seven genera with eleven species
Chrysosporium keratinophilum (3.7 %), Chrysospo-
rium tropicum (5.6 %), Chrysosporium state of
Ctenomyces serratus (11.2 %), G. pannorum
(2.8 %), Malbranchea sp. (0.9 %), Microsporum
gypseum complex (20.6 %), Microsporum nanum
(1.9 %), Microsporum van-breuseghemii (0.9 %),
Trichophyton ajelloi (15 %), Trichophyton terrestre
(2.8 %) and Uncinocarpus reesii (1.9 %) were iso-
lated from soil at glacier banks of Gulmarg, Khilan-
marg, Sonamarg and Tangmarg of Kashmir valley,
and were able to utilize keratin, and are keratinophilic
fungi and dermatophytes (Deshmukh 2002).
4.1.5 Antifreeze proteins
Production of Antifreeze protein (AFP) is one of the
key strategies of prokaryotes and poikilothermic
eukaryotes to persevere in low temperature environ-
ment (Duman and Olsen 1993 ). Antifreeze proteins
adsorb to ice surface and avoid its growth and to attach
to ice nucleators (Knight et al. 1993: Sicheri and Yang
1995). AFPs when bind to ice, lowers the freezing
temperature of a solution, melting point remains same.
This phenomenon is known as thermal hystere sis
(Urrutia et al. 1992). The thermal hysteresis ranges
from 2 to 6 °C in insects, in fish from 1 to 1.5 °C and in
plants from 0.1 to 0.5 °C (Urrutia et al. 1992), in fungi
it ranges from 0.3 to 0.35 °
C in fungi (Snider et al.
2000) and 0.1 to 0.35 °C in bacteria (Duman and Olsen
1993). AFPs alter the ice crystal pattern, i.e. it changes
the ice crystals from hexagonal to pyramid (Scotter
et al. 2006). Antifreeze proteins’ adsorption to ice
crystals can lead to inhibition of recrystallization
(Knight et al. 1984, 1988). Antifreeze proteins have
been studied in fungi (snow molds) that are pathogenic
to dormant plants under snow covers (Hoshino 2005;
Hoshino et al. 2003; Snider et al. 2000). Snow molds
consist of two key fungal taxa, Basidiomycetes and
Ascomycetes and one pseudofungal taxon of oomy-
cetes. However, among all three taxa, the AFPs have
only been identified in Coprinus psychromorbidus
belonging to basidiomycetes (Hoshino et al. 2003).
The Ascomycetes isolat ed from Antarctica have been
studied in detail among which seven strains were able
to produce and modify ice crystal nature, although they
were not recognized as Antifreeze proteins (Hoshino
2005). Xiao et al. (2010) recognized and purified a
novel fungal antifreeze protein from Antarctic asco-
mycetes Antarctomyces psychrot rophicus.
4.1.6 Mycosporines
Mycosporines are renowned small secondary metabo -
lites, which were initially revealed in spores of various
terrestrial fungi and sporulating mycelia (Young and
Patterson 1982; Bernillon et al. 1984). Mycosporine
compound, like mycospor ine glutaminol was found in
Trichothecium roseum belo nging to Deuteromycetes
(Favre-Bonvin et al. 1987). The oxo-carbonyl chro-
mophores are present in these compounds (absorbing
radiation of UVB at 310 nm), are restricted to
fungi that are found in terrestrial habitats (Shick and
Dunlap 2002). In Basidiomycetous yeasts like Rho-
dotorula minuta and Rhodotorula slooffiae, the
Mycosporine glutaminol glucoside (absorb UV at
310 nm) was studied for the first time (Sommaruga
et al. 2004). Similarly, a non-melanized and predatory
Antarctic fungus Arthrobotrys ferox, which feed on
springtail, was capable of producing carotenoids and
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123

mycosporins that act as protecting agents against UV
(Arcangeli et al. 1997; Arcangeli and Cannistraro
2000). In our knowledge, mycosporines have not been
investigated in fungi from polar and non-polar origin,
but the vast presence of mycosporines in other fungi
use them to protect themselves from UV radiation, has
clearly show n that these metabolites can exist in such
fungi but it needs further exploration.
4.1.7 Melanin
Melanin is a distinctive and multifunctional pigment
present in all biological kingdoms (Eisenman and
Casadevall 2012; Gomez and Nosanchuk 2003). In
fungi it provides protection against various environ-
mental stresses like desiccation, ionizing radiation,
oxidizing agent and UV light (Gorbushina 2003;
Butler and Day 1998). It also plays a part in fungal
pathogenesis. Several strains of Antarctic fungal taxa
like having melanized strains that resist UV radiation
including Alternaria alternat, Stachybotrys chartarum
and Ulocladium consortiale (Domsch et al. 1980).
Hughes et al. (2003) observed P. herbarum, isolated
from Antarctica, was able to produce a brow n
pigment, probably melanin, within 24 h of disclosure
to high radiation of UV-B. Similarly, many other
investigators also reported the melanin in fungi (Kogej
et al. 2004), which perhaps gives the idea that melanin
is helping them to face the extreme conditions.
4.1.8 Fungal adaptation to high pressure
High pressure disturbs or inhibits the microbial activit y
such as growth, respiration and specific biochemical
processes (Abe 2006). Effect of lethal pressures on
yeast cells were studied by several groups (Iwahashi
et al. 2003). Iwahashi et al. (2003) studied DNA
microarrays of S. cerevisiae and analysed expression
levels of *6000 genes. The genome-wide expression
profiles suggested that high pressure (180 MPa at 4 °C
for 2 min) caused damage to cellular organelles as
same as damage caused by detergents, oils, freezing
and thawing (Raghukumar et al. 2010). It has been
observed that the effects of pressure that cause growth
inhibition in S. cerevisiae were different from those
caused by lethal pressures (Abe 2004).
Pressure-inducible genes, to help in pressure
acclimatization, have been studied in marine bacteria
(Bartlett 1991). In case of bacteria, the pressure effects
on DNA replication, growth (El-Hajj et al. 2009), gene
expression, membranes, membrane proteins, DNA
structure and function, cell division, protein and
enzyme functions have been studied in detail while
in case of fungi the studies have not been carried out
except their detection in the deep-sea sediments and
capability to grow under high pressure and yield
extracellular enzymes active under raised hydrostatic
pressure (Raghukumar and Damare 2008). In conclu-
sion, none of the principle mechanism of adaptability
has yet been explored. It needs to be further investi-
gated to find out the factors involved in adaption of
fungi in deep sea environment.
5 Applications
5.1 Cold active enzymes
Psychrophilic fungi are capable of providing a large
number of biotechnological and pharmaceutical
applications (Fig. 3
). Psychrophilic fungi are capable
of synthesizing secondary metabolites t hat are very
unique to cold ecosystems (Margesin et al. 2008).
They are an important source of cold-adapted
enzymes which are economically important, as they
work actively at low and moderate temperatures
(Georlette et al. 2003). Fungi from cold habitats have
the ability to be used as biofertilizers and production
of pigments of medicinal value (Singh et al. 2011,
2014)(Table3).
The psychrophilic enzyme that is active at low and
moderate temperature provides probable cost-effec-
tive benefits (Cavicchioli et al. 2002). For instance, it
works in low temperat ure set-up in winter season,
provides high yields, increases stereospecificity,
decreases undesirable reactions and saves significant
energy in large scale process, which requires the
heating of reactors. The thermophilic and mesophilic
fungi have been investigated extensively for the
production of extracellular enzymes (Sahai and
Manocha 1993; Hankin and Anagnostakis 1975),
however psychr ophilic fungi are yet to be investigated
in detail.
Cold active enzymes, polygalacturonases and alka-
line proteases have been characterized from deep-sea
yeast and fungi, respectively (Abe et al. 2006; Damare
et al. 2006a, b). Alkaline, cold-tolerant proteases have
been isolated from deep-sea fungi in the Central Indian
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Basin. Many of these grew and produced alkaline
proteases at 5 and 30 °C and 1 bar pressure.
Aspergillus ustus (NIOCC #20) produced the highest
amounts of the enzyme. The fungus produced alkaline,
cold-tolerant protease when grown at 30 °C and 1 bar
pressure. The enzyme was active at combinations of 5,
30 and 50 °C with 300 bar pressure (Damare et al.
2006a, b). The presence of psychrophilic yeasts in
supra- and sub-glacial sediments, ice and meltwater
collected from two glaciers of the Italian Alps (Forni
and Sforzellina—Ortles-Cevedale group) was inves-
tigated. A significant proportion of isolated yeasts
exhibited one or more extracellular enzymatic activ-
ities (starch-degrading, lipolytic, esterolytic, prote-
olytic and pectinolytic activity) at 4 °C (Turchetti
et al. 2008).
Nutrient cycling
Low temperature fungi
Health
Exopolysaccharides
Environment
Bioremediation
Bio fertilizers
Molecular biology
Detergent
Food, baking,
cheese, wine
Industry
Antibiotics
Oil recovery
Pigments/lipids
Anti-tumor activity
Hydrocarbons and
fuel degradation
Pharmaceutical
Cosmetic
Leather
Pulp bleach
Desizing denim jeans
Animal feed
Immunosuppressive
Fig. 3 Schematic
representation of
psychrophilic and
psychrophilic fungal
metabolites applications in
different fields
Rev Environ Sci Biotechnol
123

Zucconi et al. (1996) isolated psychrotolerant G.
pannorum that hydrolyze starch and produce lipase,
urease, extracellular chitinase, that are active at lower
than 25 °C. Fenice et al. (1997) reported enzyme
production by screening various strains of fungi,
isolated from various locations of Victoria (continen-
tal Antarctica ), including polygalacturonase, pecti-
nase, amylase, cellulose, chitinase, cellulases,
phosphatase, glucose oxidase, urease, protease, lipase,
RNase, DNase. Takasawa et al. (1997) isolated
polygalacturonase from Sclerotinia borealis psy-
chrophilic fungi. Various other fungal strains includ-
ing G. pannorum have been documented from
Antarctica that produce keratinases (Marshall 1998).
Similarly, the Cadophora, Penicillium, Geomyces and
Cladosporium species were documented for produc-
tion of extracellular endo-1, 4-b-glucanases at 15 and
4 °C (Duncan et al. 2006). Gawas-Sakhalkar et al.
Table 3 Fungal species with various cold-active enzymes production and their applications in different fields
Enzymes Temperature
(°C)
Fungal species Applications References
a-amylases 4–20 Thelebolus microsporus,
Rhodotorula glacialis and
Rhodotorula
psychrophenolica
1. Starch conversion
2. Detergent industry
3. Fuel alcohol production
4. Processed-food industry such as baking,
brewing, preparation of digestive aids,
production of cakes, fruit juices and starch
syrups
5. Pulp and paper industry
Turchetti et al.
(2008), Singh
et al. (2014)
Cellulases 4 Cladosporium oxysporum
and Geomyces sp.
1. Detergent industry
2. Fuel alcohol production
3. Textile industry
4. Bioremediation
Duncan et al.
(2006)
Glucose oxidases 20–25 Geomyces pannorum and
Verticillium lecanii
1. Food technology
2. Bioanalysis
Fenice et al.
(1997)
Lipases 20–25 Aspergillus versicolor,
Alternaria sp.,
Cladosporium
cladosporioides and
Phoma sp.
1. Production of fatty acids
2. Detergent industry
Fenice et al.
(1997)
Phosphatases 10–30 Aspergillus niger and P.
citrinum
1. Biofertilization Singh et al.
(2011),
Gawas-
Sakhalkar et al.
(2012)
Polygalacturonases 0–60 Sclerotinia borealis,
Cryptococcus liquefaciens,
and Aspergillus japonicus
1. Food industry
2. Pectin hydrolysis
Takasawa et al.
(1997), Abe
et al. (2006)
Proteases 2–50 Aspergillus ustus,
Cryptococcus gilvescens,
Mrakia gelida and
Rhodotorula laryngis
1. Detergent industry
2. Textile industry
Damare et al.
(2006a, b),
Turchetti et al.
(2008)
Xylanases 4–20 Criptococcus albidus 1. Bioconversion of lignocellulosic
materials
2. Higher-value products, such as fuel and
other Chemicals
3. Production of oligosaccharides
Amoresano et al.
(2000)
Rev Environ Sci Biotechnol
123

(2012) analyzed fungal isolates from Arctic soils for
the production of phospha tase enzyme, among all the
isolates a Penicillium citrinum strain PG162 (a cold-
tolerant fungus) was documented as best producer of
intracellular acid phosphatase. Hassan (2015)
screened 77 fungal strains, isolated from Batura,
Passu and Siachen glaciers, Pakistan, were found to
produce six extracellular enzymes including amylase,
cellulase, deoxyribonuclease, lipase, phosphata se and
protease. Fungal isolat es were good in producing
lipase and cellulose. Sporobolomyces ruberrimus was
able to produce 5 enzymes except phosphatase. For
instance, glucose oxidase has a significant application
in food technology and bioanalysis is produced by
species belonging to Aspergillus, Penicillium, Pleu-
rotus, Alaromyces and Phanerochaete. However, only
three strains like Aspergillus niger, P. chrysogenum
and Penicillium amagasakiense are responsible for
industrial scale production (Crueger and Crueger
1990).
For reduction of viscosity and clarification of fruit
juices at low temperature, cold active pectinases can
be used. Mukherjee and Singh (2011) documented that
the a-amylase activity were maximum at 20 °C,
signifying its use in food industry, in fabric treating
and as a detergent additive, baking industry, pulp
bleach, desi zing denim jeans. Moreover, they can be
used in industrial ‘peeling’ of leather, detergents, food
industry, dough fermentation, cheese ripening, baking
industry, wine industry, animal feed and molecular
biology (Mayordomo et al. 2000).
5.2 Pharmaceutical products
The fungi from temperate and tropical habitats, have
been reported for pharmaceutical products production
(Schulz et al. 2002), although the metabolites isolated
from psychrophilic and psychrotrophic fungi are quite
rare. However, to some extent, this aspect of the
psychrophilic fungi has been investigated by many
researchers. Fungi have been found thriving in the
Pacific Ocean floor, where the nutrient availability is
low and the sediments are more than 100 million years
old. This finding leads to the idea that life is present
everywhere and at unusual places and it also creates an
opportunity for pharmaceutical companies which are
looking for new and more efficient antibiotics to
counter the increasing problem of emergence of drug-
resistant bacteria.
From point of view of pharmaceutical products,
the Penicil lium species are of a great interest. The
Penicillium species such as Penicillium lanosum and
Penicillium soppi i found in permanently cold soils,
can efficiently produce valuable secondary metabo-
lites e.g. griseofulvin and cycloaspeptide A (both are
antibiotic compounds with antimicrobial activity)
(Frisvad et al. 2006). Penicillium antarcticum,a
psychrotolerant to mesophilic and halotolerent spe-
cies (McRae and Seppelt 1999), can produce pat ulin
and asper entins. Several othe r species including
Penicillium ribium , Penicillium rivulorum and Peni-
cillium algidum
can produce other secondary
metabolites. For instance, P. ribium areableto
produce a cyclic nitropeptide psychrophilin A as well
as cycloaspepti de A and D (Frisvad et al. 2006:
Dalsgaard e t al. 2004a), whi le P. rivulorum ca n
effectively produce communesin G and H and
psychrophilin B and C (Dalsgaard et al. 2004b,
2005a). Similarly, P. algidum are capable of produc-
ing psychrophilin D and cycloaspeptide A and D
(Dalsgaard et al. 2005b). Interestingly, these cyclic
peptides are mostly produced by fungi harbor in low
temperature habitat. The cyclic peptides have been
found with varied biological activities, such as
antibacterial activity, immunosuppressive activity,
and anti-tumor activity (Joo 2012).
Brunati et al. (2009) revealed the antimicrobial
activity of filamentous fungi belonging to fifteen
diverse genera. Among 160 fungal strains, 47 fungi
exhibit activity against Staphylococcus aureus, E. coli,
Cryptococcus neoformans and Candida albicans,
although, the activity against filamentous fungi and
Enterobacteria was low. The skyrin and rugulosin
isolated from the Antarctic P. chrysogenum are very
fascinating and currently these are explored for
insecticidal and medical applications (Sumarah et al.
2005).
An antifungal protein, AfAFPR 9, was isolated from
the Aspergillus fumigatus R9, isolated from the South
Atlantic sediment sample that possessed antifungal
activity against plant pathogenic Fusarium oxyspo-
rum, Alternaria longipes, Colletotrichum gloeospori-
oides, Paecilomyces variotii and Trichoderma viride
(Rao et al. 2015). In an another study, a novel
antifungal protein (Pc-Ar ctin) was purified from P.
chrysogenum A096 isolated from an Arctic sediment
that exhibited antifungal activity against P. variotii, A.
longipes and T. viride (Chen et al. 2013).
Rev Environ Sci Biotechnol
123

Newly isolated fungal species, from Batura, Passu
and Siachen glaciers, Pakistan, were checked for their
antimicrobial activity against multi-drug resistant
(MDR) clinically isolated bact erial and fungal strains
such as E. coli (MDR), Klebsiella pneum onia (MDR),
S. aureus (MDR), Staphylococcus sp., Enterococcus
sp. (Vancomycin resistant Enterococcus), C. albicans
and A. niger, respectively. The fungal strains showed
good antimicrobial activity against Gram positive
bacteria as compared to Gram negative bacterial and
fungal strains (Hassan 2015).
5.3 Bioremediation potentials
It has been thought that psychrophilic microorganisms
might remediate the waste water and polluted soils in
winter season when the endogenous microbial
degradative capability is reduced by low temperature.
Although, not enough work has been done on the
bioremediation potentials of the psychrophilic fungi
but it is the need of the time that this aspect of cold-
tolerant fungi should be considered for much better
exploration. However, Hughes et al. (2007) have
studied the Antarctic fungi comprising genera Tricho-
derma, Phoma, Penicillium, Trichoder ma, Mortier-
ella and Mollisia for hydrocarbons and fuel
degradation. It was also observed that Mortierella
species might be capable of using dodecane as sole
carbon source. This work indicates the future use of
Antarctic fungi for hydrocarbon degradation. Accord-
ing to Adams et al. (2006) fungi are important as
decomposers in Antarctic environment. Yergeau et al.
(2007) have described the genes responsible for
decomposition through microarray survey of the
Antarctic Peninsula and recommended that fungi are
the prevailing decomposers in the Antarctica.
5.4 Pigment/lipid production
Pigment/lipids produced by cold-tolerant fungi, are
usually used to tolerate and face the harsh temperature.
Many of the investigators have reported lipids like
polyunsaturated trigl ycerides and fatty acids from
fungi that thrive at low temperature mostly (psychro-
tolerant and psychrophilic) in increased quantity
(Weinstein et al. 2000; Weete and Gandhi 1999:
Istokovics et al. 1998). Singh et al. (2014) reported a
fungal strain, Thelebolus microsporus, as a cold
tolerant fungus, which can be used for fatty acid and
pigment production. Pigment was confirmed as
carotenoid through complete analysis. The commer-
cial application of such pigments/lipids is very vast.
For instance the linolenic acid is used for enhancement
of food for individuals suffering from diabetic
neuropathy, eczema and cardiovascular diseases
(Singh et al. 2014). Similarly, linoleic acid a key
aromatic compound is precursor of 1-octen-3-ol, has
been reported in most fungi including T. microsporus
(Singh et al. 2011, 2014).
5.5 Exopolysaccharide (EPS) production
The Antarctic strain P. herbar um Westend CCFEE
5080 was examined and investigated for the produc-
tion of exopolysaccharide (EPS) (Selbmann et al.
2002). The molecular structure of the EPS was
characterized as a b 1–3, 1–6 glucan of 7.4 9 10
6
Dalton. Commonly, the production of EPS by fungi
signifies as a response to harsh environmental condi-
tion i.e. it was found that embedded mycelium showed
higher ability to grow than the unembedded one after
exposing it to repeated freeze and thaw cycles
(Selbmann et al. 2002). It has been documented that
the meristematic black fungi from Antarctica produce
EPS externally to the hyphae or adjacent to conidia,
similar to Friedmann iomyces endolithicus (Selbmann
et al. 2005). Different microbes can produc e EPS
which is independent of seasonal variations and EPS
recovery and purification is relatively easy (Suther-
land 1994). Due to their possible bioactive role
(Cheung 1996) and rheological behavior (Sutherland
1994), EPS are of great applicability in cosmetic and
pharmaceutical industries, food technology and oil
recovery (Hisamatsu et al. 1997; Blaicher and Mackin
1995).
5.6 Bio-fertilization capabilities
Phosphorus is a significant nutrient that plays vital role
in crop plant yields and developm ent. In nature,
phosphorus is present in both organic and inorganic
forms. The insoluble inorganic phosphate present in
soil is not significant to plants until converted to
soluble form. The inorganic phosphorus converted to
organic form due to solubilization can be used by
plants upon mineralization. Numerous microorgan-
isms are responsible for the conversion of insoluble
phosphates to soluble form via chelation and exchange
Rev Environ Sci Biotechnol
123

of reaction and acidification (Reyes et al. 2002;
Narsian and Patel 2000). A number of bacteria,
Actinomycetes and mesophilic fungi that are respon-
sible for phosphate solubilization have been docu-
mented from High Arctic glacier, Kanchanaburi
(Thailand) (Nenwani et al. 2010; Stibal et al. 2009;
Nopparat et al. 2007). Fungi produce organic acid for
phosphorus solubilization and have more solubiliza-
tion efficiency than bacteria (Nenwani et al. 2010).
Researchers have tried to encapsulate fungi that are
responsible for solubiliz ation of phosphate that have
an agricultural and industrial importance (Vassileva
et al. 1998). Various microfungal gener a including
Aspergillus, Penicillium and Fusarium are identified
that produce phosphatase (Yoshida and Tamiya 1971;
Nozawa et al. 1998; Vassileva et al. 1998; Haas et al.
1991). Similarly, species of Ectomycorrhizal Hebe-
loma (cold- tolerant fungi) has also been revealed to
produce cold active acid phosphatases (Tibbett et al.
1998). The cold tolerant phosphate solubilizing fungi
has been reported in Arctic soils for the first time by
Singh et al. (2011).
6 Conclusions
Psychrophilic and psychrotrophic fungi grow well at
low temperature. They have been extensively inves-
tigated in Antarctica and Arctic environments but less
significantly in non-polar habitats. Various studies
have shown that fungi are psychrotrophic in polar and
non-polar habitats. They are naturally exposed and
subjected to several extreme conditions of very low
temperature, high UV-B radiations, frequent freeze
and thaw cycles, low water and nutrient availability.
The life of fungi is impossible without an active
ecological niche constituting proper nutrient cycling
among autotrophic and heterotrophic entities. Cold
habitats are one of the most extreme environments for
survival. The presence of fungus in cod habitats is
quite interesting. The possibility of its pres ence on
glaciers can be hypothesized as, ‘to overcome the
extreme low temperature environment, fungi adopted
all the necessary equipment needed for survival at
such an extreme condition’. Under such circum-
stances, a most important question arises that from
where they obtain their food? It can be explained by
the fact that on the alpine glaciers, the main sources for
nutrition are plants, bacteria, archaea and viruses, and
their metabolites produced and released as a result of
their intera ctive ecological cycles. Another point to
consider in case of valley glaciers or mountain glaciers
is that during summers there is vegetation on the
mountain slopes or tops above the glacier valleys and
these plan ts erode with wind and rain and flow down
where they are embedded in the glacier body. The
microorganisms utilize this plant material as carbon
and energy source. Similarly, the rain drains the
surface soil of the mountain containing different
metals and trace elements d own to the glacier, which
is then used up by fungus and chemolithotrophs in
their normal biochemical pathways. The most impor-
tant possibility is the interactive ecology of fungi,
bacteria, archaea and viruses, which creates an envi-
ronment, helping in the growth of some microorgan-
isms (inclu ding fungi). The viruses as well, in their
lytic cycles produce nutrients, for the heterotrophic
microorganisms (fungi) by killing other microbes
(bacteria etc .). The fungi adapted themselves to harsh
conditions of low nutrient and low temperature
through various mechanisms. Although, all the phys-
iological and ecological adaptive mechanisms still
need more exploration but such adaptability mecha-
nisms include alterations in membrane lipid or fatty
acid configuration, an increase production of cold-
active enzymes, compatible solutes, trehalose and
synthesis of melanin and mycosporine. It is a fact that
psychrophilic and psychrotrophic fungi have greater
potential of applications in various biotechnological
and pharmaceutical fields. They can provide the
production of cold-active enzymes, pharmaceutical
metabolites, EPS and having a good potential of
bioremediation and biofertilization capabilities.
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