Published by
the International
Society of
Protistologists
The Journal of
Eukaryotic Microbiology
Journal of Eukaryotic Microbiology ISSN 1066-5234
SYMPOSIUM ARTICLE
Ciliates in Extreme Environments
Xiaozhong Hu
Laboratory of Protozoology, Institute of Evolution and Marine Biodiversity & College of Fisheries, Ocean University of China, Qingdao 266003,
China
Keywords
Aquatic environment; ciliated protozoan;
extremophiles; free-living; heterotroph;
terrestrial habitat.
Correspondence
X. Hu, Laboratory of Protozoology, Institute
of Evolution and Marine Biodiversity, Ocean
University of China, Qingdao 266003, China
Telephone number: +86 532 8203 1610;
FAX number: +86 532 8203 1610;
e-mail: [email protected]
Received: 23 January 2014; revised 26
March 2014; accepted March 27, 2014.
ABSTRACT
As eukaryotic microbial life, ciliated protozoan may be found actively growing
in some extreme condition where there is a sufficient energy source to sustain
it because they are exceedingly adaptable and not notably less adaptable than
the prokaryotes. However, a crucial problem in the study of ciliates in extreme
environments is the lack of reliable cultivation techniques. To our knowledge,
only a tiny fraction of ciliates can be cultured in the laboratory, even for a very
limited period, which can partly explain the paucity of our understanding about
ciliates diversity in various extremes although the interest in the biodiversity of
extremophiles increased significantly during the past three decades. This minireview aims to compile the knowledge of several groups of free-living ciliates
that can be microscopically observed in extreme environmental samples,
although most habitats have not been sufficiently well explored for sound
generalizations.
doi:10.1111/jeu.12120
THE English word “extreme” comes from the Latin word
“extremus,” the superlative of “exter” (being on the outside). “Extremes” include physical extremes (for example,
temperature, radiation or pressure) and geochemical
extremes (for example, desiccation, salinity, pH, oxygen
species, or redox potential) (Rothschild and Mancinelli
2001). However, there is no consensus on the definition
of an extreme environment. The term is commonly used
for any setting that exhibits life conditions detrimental or
fatal to higher organisms with respect to its physicochemical properties. Thus, extreme environments differ in one
or more aspects from those which humans consider as
“normal,” moderate conditions with circumneutral pH,
temperatures between 5 and 50 °C, pressures around
0.1 MPA (1 atm), and adequate concentrations of nutrient
and saline. Simply speaking, extreme environments are
places where “normal” life forms find it hard to survive.
This doesn’t mean that there isn’t any life in extreme environments. Certain creatures can live and grow in extreme
environments.
Some extreme environments that we may know about
are deserts, mountain peaks, caves, and frozen places like
the Arctic and Antarctic. Some environments are very hot
or very cold, extremely dry, or both. Other extreme environments are filled with acids, are blasted with radiation,
are under high pressure, or are tough places for most
living things in various other ways. They can be: without
410
oxygen, alkaline, acidic, extremely hot, extremely cold, hypersaline, without water, under pressure, radiation, etc.
(Horikoshi and Grant 1998; Rothschild and Mancinelli
2001). Some environments are extreme in more than one
way. Most deserts are both hot and dry. The Dry Valleys
in Antarctic are very cold and dry (Roberts et al. 2004).
Some hot springs are acidic. Deep-sea hydrothermal vents
don’t receive any sunlight, spew out hot water filled with
harsh chemicals, and are weighed down by the crushing
pressure of the deep oceans (Kouris et al. 2007).
An organism that thrives in an extreme environment is
an extremophile. Some extremophiles are able to overcome two more extreme conditions and, we call them
“polyextremophiles”, which are very diverse (Rothschild
and Mancinelli 2001). Most terms used to describe extremophiles are generally straightforward. They are a combination of the suffix -phile, meaning “lover of,” and a
prefix specific to their environment.
In the past three decades, we have seen that interest in
the biodiversity of microorganisms living in “extreme environments” has increased significantly. There are several
reasons for this: some fundamental (e.g., we think that
these environments were far more widespread during the
early life of our planet and that organisms isolated from
these sites are representative of archaic life forms), and
some more applied (e.g., the increasing use of extremophiles as living organisms or as sources of enzymes and
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2014, 61, 410–418
Ciliates
Hu
other cell products in a variety of industrial and biotechnological operations).
DISCOVERY OF CILIATES IN EXTREME
ENVIRONMENTS
Eukaryotic ciliated protozoan may be found actively growing in some extreme condition where there is a sufficient
energy source to sustain it (Lynn 2008; Roberts 1999).
This contribution presents a brief review on free-living ciliate morphotypes from several representative extreme
conditions.
Anaerobes
Anaerobe can grow in the absence of oxygen. Anaerobic
ciliates have been found in most natural anoxic environments, including marine (Fenchel et al. 1977; Hayward
et al. 2003; Xu et al. 2013) and freshwater (Finlay 1982)
sediments, the anoxic hypolimnia of lakes (Bark 1981;
Esteban et al. 1993a; Finlay et al. 1991), deep basins of
esturaries (Fenchel et al. 1990, 1995), bathyal anoxic sediments (Beaudoin et al. 2012), oxygen-depleted marine
water-column habitats (Orsi et al. 2012a,b), and domestic
landfill (Finlay and Fenchel 1991).
As far as we know, free-living anaerobic ciliates belong
to only a few taxonomic groups, especially the Metopidae
(Armorphorida, formerly Heterotrichida), the Trimyemidae,
Plagiopylidae, Sonderiidae (Plagiopylida, formerly Trichostomatida), and species of the order Odontostomatida
(Beaudoin et al. 2012; Esteban et al. 1993b; Fenchel and
Finlay 1991; Fenchel et al. 1995; Xu et al. 2013). These
anaerobes are not phylogenetically related, implying that
the process allowing their existence was not difficult, and
they have strong morphological ties to their aerobic relatives, implying that the process was recent.
For example, Metopus is the largest anaerobic genus
including more than 80 nominal species from various habitats (Bernhard et al. 2000; Esteban et al. 1995; Foissner
and Agatha 1999; Foissner et al. 1992). Its members are
characterized by torsion of the anterior part of the cell,
and a frontal lobe that protrudes above the AZM. The
anterior twisting often gives Metopus a characteristic Sshape. Likewise, all ciliates belonging to the genus Trimyema are anaerobic (Augustin et al. 1987; Cho et al. 2008;
Finlay et al. 1993; Lynn 2008; Nerad et al. 1995; Serrano
et al. 1988).
Free-living aerobic ciliates are totally reliant on mitochondrial respiration for energy generation, whereas in anaerobic ciliates the role of the mitochondrion has been
replaced by the hydrogenosome (Brul and Stumm 1994;
Embley et al. 1992, 1995; Esteban et al. 1993b; Fenchel
and Finlay 1992; Finlay et al. 1991). In the cells of the latter, methanogens are situated close to or even surrounding hydrogenosomes, which form a consortium (Fenchel
and Finlay 1991, 1992; Finlay et al. 1991). This kind of
consortium is either stable or unstable (Esteban et al.
1993b; Finlay et al. 1993; Wagener et al. 1990). Anaerobic
ciliates also demonstrate various metabolic pathways, for
example, nitrate respiration under anoxia has been
recorded for freshwater species of Loxodes (Finlay 1985).
Very recently, efforts have been made to visualize and
describe the cellular morphologies of novel ciliate clades,
and their functional roles within ecosystems in Deep
Hypersaline Anoxic Basins (DHABs, Orsi et al. 2012a,b).
Thermophiles
A thermophile is defined as an organism with optimal
growth at temperatures 40 °C or higher. Hyperthermophiles can grow well at temperatures 80 °C or higher.
True thermophilicity and hyperthemophilicity are quite
common in Archea and somewhat common in Eubacteria.
In contrast, the maximum temperature tolerated by
eukaryotes extends only slightly into the range of thermophilicity, and there are no reports of growth at above
80 °C for any ciliates (Hickey and Singer 2004).
Ciliates have been occasionally reported living at temperature higher than 40 °C from several hot springs over
the world (Issel 1906; Kahan 1969, 1972; Noland and Gojdics 1967). They belong to only a few genera, e.g., Cothurnia, Chilodon, Cyclidium, Tetrahymena, Folliculopsis.
Among them, Tetrahymena spp. is well-known as model
organisms (Corliss 1973). Cyclidium is one of the commonest and most abundant genera in hot springs (Ruiz
1959; Vouk 1950). Kahan (1972) found Cyclidium citrullus
from Tiberias hot springs at temperatures of 50–58 °C and
determined that its optimal growth temperature is 44 °C.
Cothurnia sp. (Pax 1951) and Chilodon sp. (Dombrowski
1961) were found at 63 and 68 °C, respectively, the highest temperatures recorded for ciliates to data. Baumgartner et al. (2002) described Trimyema minutum from
submarine hydrothermal vents. It grows from 28 to 52 °C
with an optimal growth temperature of 48 °C.
Ciliates are often found in various submarine hydrothermal vents. Small and Gross (1985) first recorded at least
20 species of ciliates on the East Pacific Rise hydrothermal vents. Later, several studies reported ciliates from
vents elsewhere (Kouris et al. 2007 and references
therein). These work demonstrated that the most abundant ciliates were sessile peritrichids and folliculinids.
Psychrophiles
Water is the solvent for life and must be present in a
liquid state for growth to occur. This sets a practical lower
limit for growth slightly below 0 °C. Antarctic and Arctic
continents (sea-ice, fellfields, soil, and lakes) are extreme
with very low temperatures. Even though these are
extreme conditions, many ciliates are found in soils, freshwater, and sea-ice of these two continents, where they
demonstrate adaptation to growth at low temperature
(Laybourn-Parry and Pearce 2007; Petz et al. 1995, 2006;
Thomas and Dieckmann 2002). These organisms, known
as psychrophile, can grow optimally at temperatures
15 °C or lower.
Lee and Fenchel (1972) found that Euplotes antarcticus
is unable to survive above 17 °C, and Holosticha sp. was
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2014, 61, 410–418
411
Ciliates
Hu
reported to unable to divide above 2 °C. Euplotes focardii was a psychrophilic endemic Antarctic ciliate which
shows optimal survival and multiplication rates at 4–5 °C
that decline sharply at temperatures greater than 8–10 °C
(Valbonesi and Luporini 1990, 1993).
Garrison and Buck (1989a) found that the heterotrophic
biomass is dominated by flagellates and ciliates in the
Weddell Sea. The abundance was greatest in a well-developed ice-edge bloom in the spring. Garrison and Buck
(1989b) also reported that the sea-ice itself contains a rich
and varied population of microbes, which includes phototrophs (diatoms and flagellates) and heterotrophs (ciliates
and others). The presence of the heterotrophs indicates
an active food web.
Petz (2005) compiled all the ciliates recorded from Antarctic sea and got at least 161 morphospecies from 85
genera, of which more than 30 are new. These ciliates
belong to seven classes, representing an unexpectedly
rich diversity.
Investigations on Antarctic soil and moss ciliates are relatively sparse. Smith (1978) reviewed the old literature
and recorded about 50 species. Later, 200 more species
were identified from Antarctic moss and soil samples and
1 new family, 6 new genera, 20 new species were published by these authors (e.g., Blatterer and Foissner 1988;
Petz and Foissner 1996, 1997; Smith 1984).
So far, it was estimated that nearly 400 distinct morphospecies were overall identified from Arctic and Antarctic
ecosystems, ca. 20% were new (Di Giuseppe et al. 2013
and references therein).
Acidophiles
Acidic extremes are typically described as those possessing a pH less than 5, which are often accompanied by high
concentrations of toxic metals, low nutrient level, and/or
extreme temperature. Classic examples of acidic environments include acid rock drainage (ARD) or acid mine drainage (AMD) systems often involving current or past mining
activities, hydrothermal vent fluids, and terrestrial geothermal environments. Microorganisms that have an optimum
growth in these acidic extremes are termed “acidophiles”
(Baker-Austin and Dopson 2007). Acidophilic eukaryotic
diversity is extensively studied, probably due to a large
number of accessible acidic environments. However, ciliates are seldom found in ARD and AMD environments
(Johnson 1998; Joseph 1953; Lackey 1938, 1939; McConathy and Stahl 1982). A hypotrich ciliate (Oxytricha sp.) was
listed as a frequently occurring protozoan by Lackey (1938,
1939) from highly acidic streams and strip pits. Joseph
(1953) preliminarily studied microorganisms from acidic
mining water and found ciliated protozoa represented by
Paramecium. A laboratory study of a ciliate (Cinetochilium
sp.) showed that it was obligately acidophilic (growing in
media poised at pH 1.6–2) and that they grazed mineral-oxidizing (and other) acidophilic bacteria (Johnson and Rang
€lfl et al. (1998) recorded the maximum ciliate cell
1993). Wo
density (3.55 9 105 cells/l) in the acidic (mining) lakes. Packroff (2000) investigated the planktonic protozoa, especially
412
ciliates in five mining lakes of various pH and acidity values
in the Lusatian and mid-German mining area. He found that
prostomatids (Urotricha sp.) and hypotrichids (Oxytrichidae)
were two main groups of ciliates in the plankton of the lake
117, and other taxa appeared only sporadically in very low
numbers, e.g., Frontonia sp., and ciliates were quantitatively important members of the plankton community and
reached cell densities of 1.4 9 104 cells/l. In the same
€lfl (2000) gave a review on the occuryear, Packroff and Wo
rence and taxonomy of ciliates in extreme acidic environments. They stated that Urotricha, Vorticella, and Oxytricha
are the most important genera in acidic mining lakes of pH
2–3. This finding was supported by a very recent study performed by Weisse et al. (2013), who found a new species
of Oxytricha, O. acidotolerans and Urosomoida sp. from
two acid mining lakes (pH = 2.6). Aguilera (2013) detected
that the protistan consumer community is characterized by
two different species of ciliates tentatively assigned to the
genera Oxytrichia and Euplotes in Rıo Tinto, Spain (mean
pH 2.3).
A few hyotrichous ciliates belonging to Orthoamphsiella
and Oxytricha were also rarely found in soil samples with
pH value of ca. 4 (Eigner and Foissner 1993; Foissner 1996).
Alkalophiles
Alkalophile prefers alkaline environments with high pH
(usually > 9), which include soda lakes, hot springs, hydrothermal vents, as well as environments shaped by industries such papermaking and textiles. Several well-known
pH extreme environments such as alkaline Mono Lake in
California, have been extensively examined for their bacterial and archaeal diversity but remain underexplored with
respect to ciliate diversity (Hollibaugh et al. 2001; Humayoun et al. 2003). However, at the present state of knowledge, only a few studies demonstrated the occurrence of
planktonic ciliates in alkaline environments (e.g., AmaralZettler 2013; Esteban et al. 2000; Finlay et al. 1987; Kudo
1966; Pomp and Wilbert 1988; Wilbert 1995; Yasindi et al.
2002).
Some East African Lakes are alkaline-saline ones. Two
soda lakes (Lake Nakuru and Lake Simbi), with a pH of
about 10, were firstly studied for their microbial populations, and more than 20 species of ciliates, most of which
belong to Cyclidium, Frontonia, Spathidium, and Holophrya, were reported (Finlay et al. 1987). Ong’ondo et al.
(2013) just studied ciliated protist assemblages of the shallow soda lakes Bogoria and Nakuru in Kenya and detected
22 ciliate morphospecies, a similar diversity as shown in
previous investigation. Cyclidium glaucoma was the most
abundant, whereas Frontonia sp., Condylostoma sp. and
Holophrya sp. dominated in terms of biovolume.
Other similar environments are seldom studied. Lake
Van, Turkey is the largest soda lake on earth, and has
served as a model of the possible highly alkaline chemistry of the early ocean (pH ca. 10). A new species of Frontonia, F. anatolica was collected from the sediment on its
eastern shore and its morphology, ciliature, and silverline
system were described (Yildiz and S
enler 2013).
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2014, 61, 410–418
Ciliates
Hu
Ciliates were also found in some salt lakes with pH
value up to 9.5. Some of them, Holosticha gelei, Spathidium macrostomum, Cladotricha halophila, C. edaphoni, Euplotes pterotae, and Uronychia magna, were new species
(Wilbert 1986, 1995).
Esteban et al. (2000) investigated ciliates living in the
crater-lake of an extinct volcano in Australia, and identified
85 species, including one new species Lembadion
curvatum.
Several studies have been done to examine ciliates in
soil material with high pH value (Bayly and Williams 1966;
Pomp and Wilbert 1988). Twenty-seven ciliate species
were found and seven were described from southern Australian alkaline-saline soils (pH 8.1–9.5) by Pomp and Wilbert (1988), and 3 of them, Spathidium metabolicum,
Cinetochilum marinum, and Sagittaria australis, were new
to science.
Very recently, Amaral-Zettler (2013) studied eukaryotic
alpha and beta diversity in eukaryotic communities from
seven diverse aquatic environments with pH values ranging from 2 to 11. An unidentified Cyclidium species was
observed in the biofilm/sediment sample (pH 10.4) from
Mallard Lake, Sandhills NE, USA.
Halophiles
Hypersaline environments (generally > 9%; Oren 2002)
include salt or soda lakes, salterns, coastal lagoons, and
deep hypersaline anoxic Brines. Although they pose challenges to life because of the low water content (water
activity), many such habitats appear to support eukaryotic
microbes, including ciliates (Edgcomb and Bernhard 2013).
Investigations of protozoa from hypersaline habitats have
a long history (Gaievskaia 1925; Jahn et al. 1979; Larsen
1980; Oren 2002; Pack 1919; Ruinen 1938; Wilbert and
Kahan 1981).
Kirby (1932) described a small, new species of ciliate,
Rhopalophrya salina collected in concentrated brine from
Searles Lake, California. A small, unidentified ciliate species, possibly belonging to the genus Cyclidium, was isolated from the Dead Sea (Elazari-Volcani 1944).
Wilbert and Kahan (1981) found 16 ciliates in the algal
mats of the benthic area in Solar Lake where the salinity
ranged from 4% to 14% NaCl (w/w) over the year. They
concluded that all of these were probably marine or fresh
water forms more adapted to high salinity than continental
forms.
Post et al. (1983) investigated the protozoa in brines
(over 15% salinity) of a Western Australian hypersaline
lagoon and frequently observed 14 ciliates which feed on
bacteria and/or algae.
In 2005, Hauer and Rogerson (2005) reviewed heterotrophic protozoan from hypersaline environments. According to their estimation, about 30 species including
unidentified species have been reported from high-salinity
(> 15%) waters. It was found that species number of ciliates tends to decrease with salinities increasing. Recently,
a new species of ciliate, Trimyema koreanum was isolated
from extremely hypersaline water (salinity of 293&) from
a solar saltern in Korea, and its morphology and SSU rDNA
sequence were detailed investigated (Cho et al. 2008).
The results revealed that T. koreanum, as a new species,
differed from the most similar species, Trimyema marinum, by the presence of two distinct ciliary girdles. It was
found to consume both prokaryotes and small eukaryotes
(specifically, the alga Dunaliella sp.) and then be of ecological significance.
Very recently, Edgcomb and Bernhard (2013) gave brief
reviews of our current knowledge on eukaryotes of watercolumn haloclines and brines from DHABs of the Eastern
Mediterranean, as well as shallow-water hypersaline
microbial mats in solar salterns of Guerrero Negro, Mexico
and benthic microbialite communities from Hamelin Pool,
Shark Bay, Western Australia. Comparison study shows
several groups of eukaryotes including ciliates are commonly found in hypersaline habitats.
Other extremophiles
Ciliates may be found actively growing in other extreme
environments, which, however, are not explored yet.
More investigations are needed to provide deeper insights
in the ways ciliates deal with various extreme conditions,
and that may also open the way to the development of
novel applications.
COMPARISON AND DISCUSSION
As shown, ciliates are relatively extensively investigated in
anaerobic and psychrophilic environments; by contrast, ciliates are poorly explored in other extremes because references are relatively few. Based on data available,
anaerobes and psychrophiles are more diverse than halophiles, thermophiles, alkaliphiles, and acidophiles (Table 1).
Among them, psychrophiles have the biggest species
diversity, followed by anaerobes, alkaliphiles, and halophiles, respectively. Acidophiles and thermophiles are very
low in species richness, i.e., the ciliate community in
acidic and very hot habitats is characterized by an extremely low diversity. Different taxa dominate ciliate communities in various extreme environments (Table 1).
In addition to concentration on species identification,
there are many investigations on community structure and
function of anaerobic ciliates. Anaerobes are often
described as the main bacterial consumers of anoxic freshwater and marine environments and their ecological functions are revealed in microbial food web (e.g., Guhl et al.
1994, 1996; Laybourn-Parry et al. 1990; Madoni 1990; Mass-Alio
1994). Meanwhile, increasing number
sana and Pedro
of investigations have been carried out to elucidate the ecological role of planktonic ciliates in harsh Antarctic and Arctic environments (e.g., Garrison 1991; Grey et al. 1997;
Kepner et al. 1999; Laybourn-Parry et al. 1991, 2002; Mieczan et al. 2013; Perriss et al. 1995; Roberts et al. 2004).
These studies reported a maximum ciliate community
reaching concentration of 1.5 9 105/l. However, to our
knowledge, only a few quantitative and ecological studies
are performed in very acidic and alkaline habitats from a
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2014, 61, 410–418
413
Ciliates
Hu
Table 1. Comparison of dominant taxa and approximate species number of ciliates from various extreme environments
Species
number
Dominant taxa
Studying sites
Euplotes, Frontonia, Oxytricha, Urotricha, Uroleptus,
Vorticella, Cinetochilum
20–30
Stentor niger, Strombidium viride, Strombidium sp.
< 10
Acidic lakes
Frontonia, Cyclidium sp, Cyclidium glaucoma
~20
Soda lakes, Kenya
Hypotrichs (e.g., Aspidisca), Metopus, Litonotus
scuticociliates (e.g., Cyclidium
Cyclidium citrullus, Cyclidium sp., Trimyema
minutum, peritrichids, folliculinids
85
Crater lakes, Australia
–
Acid mine drainage, Strip
mining lake, acidic river
20–30
Hot springs, hydrothermal vents
40–50
Salt lakes and lagoon, salterns,
and deep hypersaline brines
Lackey (1938, 1939), Johnson
(1998), Packroff (2000),
€lfl (2000)
Packroff and Wo
Bienert et al. (1991), Beaver
and Crisman (1981)
Finlay et al. (1987), Ong’ondo
et al. (2013)
Esteban et al. (2000)
34
Anoxic habitats from UK and Spain
Kahan (1972), Small and Gross
(1985), Baumgartner et al.
(2002), Kouris et al. (2007)
Post et al. (1983), Hauer and
Rogerson (2005), Cho et al.
(2008)
Perriss et al. (1995),
Laybourn-Parry et al. (2002)
Petz (2003, 2005), Di Giuseppe
et al. (2013)
Dolan et al. (2013)
Esteban et al. (1995), Augustin
et al. (1987), Fenchel and
Finlay (1991), Kahl
(1930–1935), Lynn (2008)
Guhl et al. (1996)
25
Anoxic habitats from UK
Guhl et al. (1994)
25
7
Anoxic habitats from Israel
Anoxic habitats from Italy
Madoni (1990)
Madoni and Sartore (2003)
–
Antarctic saline lakes
Tintinnids, euplotids, Strombidium (400)
~400
Arctica and Antarctica
Cymatocylis affinis, C. convallaria, Condonellopsis gaussi 15
Metopids (e.g., Metopus), plagiopylids (e.g., Plagiopyla,
Trimyema), odontostomatids, scuticociliatids (e.g., Cyclidium)
15
~200
Antarctica
Various anoxic environments
Mesodinium rubrum
Caenomorpha, Cyclidium, Metopus Plagiopyla nasula, Epalxella,
Dexiotricha, Cristigera, prostomatid,
Dexiotricha, Cyclidium, Cristigera), Caenomorpha
medusula, Plagiopyla nasuta, Prorodon Saprodinium
mimeticum, Lacrymaria sapropelica, Tropidoatractus acuminatus
Saprodinium dentatum, Plagiopyla nusta, Dexiotricha plagia
Spirostomum dentatum, Metopus fuscus, Plagiopyla nasuta
Reference
– no data available.
limited number of countries, e.g., Germany, America, and
€lfl et al. 1998),
England for acidophiles (Packroff 2000; Wo
Australia and Kenya for alkaliphiles (Finlay et al. 1987;
Walker 1973). The highest record for ciliate cell density
from pH extremes is more than 1 9 106 cells/l (Table 2).
Many of the accounts of ciliates in hypersaline habitats are
observational and there have been few attempts to quantify
ciliate abundance. In the Antarctic Vestfold Hills, the plankton was dominated by one autotrophic ciliate, Mesodinium
rubrum, which reached abundances of 2.7 9 105/l and
spanned a salinity gradient up to 6.3% salt (Laybourn-Parry
et al. 2002; Perriss et al. 1995). Thermophiles have a very
low abundance, and thus have not been investigated quantitatively so far.
Noteworthily, with the exception of a limited number of
species, the ciliate taxa from very hot, extremely acidic
and alkaline habitats could be identified only down to the
genus level. The reason for this could be: most of the
identification of ciliates is based on live observations,
which cannot yield sufficient information for reliable identification; adequate specimens needed for cytological staining are unavailable in most cases; taxonomic experts in
ciliates are often in short supply.
414
Table 2. Comparison of maximum cell density (cells/l) of ciliates from
various extremes
Cell density
Type of extremes
Reference
1.21 9 10
3.55 9 105
0.5–3 9 104
> 1 9 106
1.6 9 103
1.5 9 105
2.9 9 104
3.2 9 104
2.2 9 103
> 2.7 9 105
1 9 105
377a
Acidic
Acidic
Acidic
Alkaline
Alkaline, saline
Extremely cold
Extremely cold
Extremely cold
Extremely cold
Extremely cold, saline
Anoxic
Anoxic
Bienert et al. (1991)
€lfl et al. (1998)
Wo
Packroff (2000)
Finlay et al. (1987)
Walker (1973)
Petz (2005)
Sorokin (1999)
Kepner et al. (1999)
Grey et al. (1997)
Laybourn-Parry et al. (2002)
Guhl et al. (1996)
Madoni (1990)
4
a
cells/cm2.
The richness of ciliate assemblage in extreme environments is low compared to other locations. The reduced
richness is very likely a consequence of a variety of
extreme conditions. However, extremophiles might be
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2014, 61, 410–418
Ciliates
Hu
ecologically important in these environments as already
demonstrated and could add to the diversity of the eukaryotic microbial community, although we have not yet fully
understood it due to under-sampling efforts.
ACKNOWLEDGMENTS
I thank Prof. Roberto Docampo and two anonymous
reviewers for helpful suggestions and comments. This
study was supported by the Natural Science Foundation of
China (Project numbers: 41176119, 41376141). I specially
acknowledge Prof. J. Clamp for kindly inviting me to give a
symposium talk on this topic in the ICOP XIV, Vancouver.
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