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10.1146/annurev.micro.57.030502.090811
Annu. Rev. Microbiol. 2004. 58:649–90
doi: 10.1146/annurev.micro.57.030502.090811
c 2004 by Annual Reviews. All rights reserved
Copyright First published online as a Review in Advance on July 14, 2004
ENDANGERED ANTARCTIC ENVIRONMENTS
Don A. Cowan and Lemese Ah Tow
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Department of Biotechnology, University of the Western Cape, Bellville 7535, Cape Town,
South Africa; email: [email protected]; [email protected]
Key Words Antarctica, Dry Valleys, microbial communities, microbial endemism,
climate change, environmental impact, ssu rRNA
■ Abstract The Antarctic continent harbors a range of specialized and sometimes
highly localized microbial biotopes. These include biotopes associated with desiccated
mineral soils, rich ornithogenic soils, glacial and sea ice, ice-covered lakes, translucent
rocks, and geothermally heated soils. All are characterized by the imposition of one or
more environmental extremes (including low temperature, wide temperature fluctuations, desiccation, hypersalinity, high periodic radiation fluxes, and low nutrient status).
As our understanding of the true microbial diversity in these biotopes expands from
the application of molecular phylogenetic methods, we come closer to the point where
we can make an accurate assessment of the impacts of environmental change, human
intervention, and other natural and unnatural impositions. At present, it is possible to
make reasonable predictions about the physical effects of local climate change, but
only general predictions on possible changes in microbial community structure. The
consequences of some direct human impacts, such as physical disruption of microbial
soil communities, are obvious if not yet quantitated. Others, such as the dissemination
of nonindigenous microorganisms into indigenous microbial communities, are not yet
understood.
CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
COLD DESERT MINERAL SOILS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The Antarctic Dry Valleys . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Dry Valley Minerals Soils: The Physical and Chemical Environment . . . . . . . . . . .
Cold Desert Microbial Communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
LITHIC MICROBIAL COMMUNITIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The Physical and Chemical Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Composition of Lithic Communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
LAKE COMMUNITIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The Physical and Chemical Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Microbial Lake Communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Water Column Communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Microbial Mats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
FLOWING WATER SYSTEMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Microbial Communities in Aquatic Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impact . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ICE MICROBIOLOGY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sea Ice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Polar and Glacial Ice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Lake Ice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Cryoconites Holes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
FELLFIELD COMMUNITIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Fellfield Microbiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ORNITHOGENIC SOIL ENVIRONMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The Physical and Chemical Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Microbiology of Ornithogenic Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sensitivity to Environmental Impacts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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INTRODUCTION
The Antarctic continent offers a range of extreme climatic conditions that constitutes one of the harshest environments on Earth. Extremes of temperature, low
atmospheric humidity, low liquid water availability, and high periodic incident
radiation with long periods of complete darkness all contribute to rendering the
continent relatively inhospitable for the development of biological communities.
We must remember that the concept of an extreme environment is, in part,
anthropogenic and therefore artificial. The discomforts and difficulties that the
mesophilic mammal Homo sapiens experience in Antarctic conditions are not a
good yardstick for assessing the success, or otherwise, of microbial existence.
Nevertheless, the Antarctic environment does impose real thermodynamic and
kinetic limitations on microbial growth. This is evident in that higher eukaryotes
are restricted to the more northern latitudes (the Antarctic peninsula) and that
both microbial biomass levels and species diversity are significantly lower in the
most extreme ice-free region of Antarctica, the McMurdo Dry Valleys, than in
temperate environments. However, where suitable niches are found, microbial life
exists. The presence of liquid water stimulates the most productive and diverse
microbial communities: in shallow lake margins, glacial and snowfield melt water
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ENDANGERED ANTARCTIC ENVIRONMENTS
TABLE 1
Impacts on Antarctic microbial biotopes and communities
Source
Nature
Effect(s)
Anthropogenic
Movement, transport, physical
activities
Physical disturbance to soil surfaces;
dissemination of nonindigenous
microorganisms
Chemical contamination/eutrification
of soil and water systems
Production of waste materials
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Climatic
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Temperature rise
Temperature decrease
Elevated UV radiation
Loss of ice; increased microbial growth;
increased water availability
Increase in ice cover; reduced microbial
activity; decreased water availability
Changes in microbial distribution
streams and “flushes,” and meltwater pools in glacial ice. Elsewhere, microbial
communities are more physically restricted. Endolithic microbial communities,
taking shelter under stones, in cracks in rock strata, and even within the interstitial
spaces in crystalline rocks, have achieved a fine balance between the limitations
of light availability and desiccation.
Many of the Antarctic microbial communities are potentially sensitive to external impacts (Table 1). The physical fragility of the Dry Valley soils and Antarctic
peninsular fellfields makes their microbial communities susceptible to physical
and climatic deterioration. The extent to which the structures of these communities might be modified by the impact of nonindigenous microbial contamination
remains to be evaluated. Others, such as ice, lake, and flush communities, are
obviously susceptible to regional temperature changes.
It is important to understand the immediacy, significance, and ultimate consequence of these natural (climatic) and unnatural (anthropogenic) impacts. However, this will be possible only when we have a detailed understanding of the biological complexity of each habitat, and the way in which the community structures
and relationships respond to environmental changes and impositions. We review
the current state of knowledge of the microbiology of major Antarctic habitats
(see Figure 1 for principal locations), and consider these microbial communities
in light of known and projected environmental impacts.
COLD DESERT MINERAL SOILS
The Antarctic Dry Valleys
Ice-free regions represent less than 2% of the total land area of the Antarctic
continent (35). The McMurdo Dry Valleys of Eastern Antarctica comprise much
of the total ice-free land, although ice-free regions are also found in the Vestfold
Hills, the Bunger Hills, and at various sites in the Transantarctic mountains and
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Figure 1 Continental Antarctica, showing the most important sites for terrestrial
microbiological research.
on the Antarctic Peninsula. The Dry Valleys are the coldest and driest deserts on
Earth and experience a variety of harsh environmental conditions (Table 2). The
extremely low temperatures, low precipitation, low humidities, high salt content,
katabatic winds, steep physical and chemical gradients in the terrestrial habitats,
and low organic matter content impose major limitations on microbial growth and
survival (74, 165).
The McMurdo Dry Valleys are not homogeneous systems. They offer a range
of widely differing microbial biotopes that includes lakes (both freshwater and
saline), freshwater streams, and at least two types of soil, moist soils that are
exposed to glacial meltwater and desiccated mineral soils (153).
Dry Valley Mineral Soils: The Physical and
Chemical Environment
Dry Valley mineral soils are the most barren soils of the snow-free regions of the
Antarctic continent (Figure 2). The upper horizon of mineral soils typically has
a low water content (0.5%–2% wt) due to the low level of precipitation and exposure to the desiccating atmosphere. Low humidity (<10% RH in winter), low
precipitation and strong katabatic winds (especially during winter) result in long
periods of desiccation (74). The mean annual precipitation of 15 g cm−2 year−1
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TABLE 2 Ecological factors in Antarctic cold deserts (reproduced from Reference 165 with
permission)
Favorable conditions
Unfavorable conditions
North-south orientation of valley (across
katabatic wind direction)
East-west orientation of valley (along
katabatic wind direction)
Northern exposure
Southern exposure
Gentle north-facing slope
Flat or south-facing slope
High solar radiation
Low, sporadic solar radiation
Microclimate above freezing
Microclimate below freezing
Absence of wind
High winds
Northerly winds
Southerly winds
High humidities
Low humidities
Slow or impeded drainage
Rapid drainage
Lengthy duration of available water
Short duration of available water
Translucent pebbles
Opaque pebbles
Nonsalty soils, balanced ionic composition
Salty soils, unbalanced ionic composition
Approximately neutral pH
High (or low) pH
Organic contamination (e.g., skuas, seals)
No organic contamination
is entirely in the form of snow. However, because of the low atmospheric humidity, much of the snow sublimes with little moisture penetrating the upper soil
horizon.
A cemented permafrost layer is present at the base of the mineral soil profile (as
little as a few centimeters below the soil surface) (Figure 3). Despite the presence
of the permafrost layer, insufficient liquid water is obtained from the melted permafrost interface (owing to the steep desiccation gradient) to support consistent
microbial growth in the surface soils (164).
The Dry Valleys of Antarctica experience extremely low temperatures, the mean
annual air temperature ranging from –20 to –25◦ C (164). In summer, the mean air
temperature is ∼0◦ C, while surface ground temperatures average around +15◦ C
during periods of direct sunlight. Prolonged periods of extremely low temperatures
(−55◦ C) prevail during winter (159). Cameron (27) reported that a Ross Desert
soil experienced a temperature change from –15 to +27.5◦ C within 3 h. Such
temperature fluctuations lead to freeze-thaw cycles that are potentially lethal to soil
microbiota. The survival of microorganisms in Dry Valley mineral soils depends
on their hydration state, their compatible solute content, and their ability to switch
metabolism to synthesize cryoprotectants (24).
Besides tolerating the desiccating conditions and extreme temperatures, microorganisms inhabiting the mineral soils are subjected to osmotic stress due to
high salt concentrations from accumulated sodium, calcium, magnesium, chloride,
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sulphate, and nitrate (74). The high salt concentrations within the mineral soils
result from upward transport from the substratum as well as surface supplementation resulting from sea spray blown inland by onshore winds (153, 165). The
soluble nitrogen (N) concentrations measured in desert soils range from 0 to
−1
1250 µg g−1 soil in the form of NO−
soil in the
3 -N and from 0.3 to 40 µg g
+
form of NH4 -N (153). Nitrate concentrations in Antarctic mineral soils are the
lowest reported for terrestrial soils (such as forest and cultivated soils) and are
derived primarily from atmospheric precipitation (154). Soluble phosphorus (P)
concentrations in Antarctic desert soils are between <0.01 and 120 µg g−1 soil
(153).
The Dry Valley mineral soils contain low levels of organic matter (an average of 0.064 ± 0.035% total organic carbon) (93). Soil organic matter in
the Taylor Valley region arises from several sources, such as marine-derived
organic matter, lacustrine-derived organic particulates, cryptoendolithically derived organic matter, and airspora (22). Strong katabatic winds aid the dispersal
of organic matter from inland lakes (lacustrine-derived particulates) and marine
environments onto mineral soil surfaces. Physical abrasion of rocks by windblown sand allows the distribution of organic matter from endolithic microbial
communities.
Cold Desert Microbial Communities
Microbial abundance and diversity in Antarctic desert soils depend on a number
of specific ecological factors (29) (Table 1). This is evident from comparisons of
habitat composition and associated microbial composition in Ross Desert soils
collected from four different locations (all experiencing different edaphic characteristics) (Table 3) (24, 25, 28, 165). For example, soil water content and cell
numbers are positively correlated; low-organic-content saline soils contain lower
numbers of culturable microorganisms than nonsaline soils (29). However, caution must be exercised when interpreting quantitative data from culture-dependent
enumeration studies, which have repeatedly shown that Dry Valley mineral soils
contain low levels of microorganisms [e.g., 102–104 g−1; (24, 25, 28)]. However in
situ ATP analysis data have indicated that Dry Valley mineral soils contain three
to four orders of magnitude higher levels of microbial biomass than previously
reported (41).
Most microorganisms isolated from mineral soils are psychrotrophs, perhaps not
surprisingly because these organisms are better adapted to survive the temperature
cycling of surface soils than true psychrophiles. Psychrophiles are more abundant
in the permafrost layer, where temperature fluctuations are low. Most of the viable
(i.e., culturable) bacteria in Ross Desert soils are found in the permafrost layer
and toward the surface (30). Chromogenic bacteria colonize soil surfaces, whereas
nonpigmented bacteria were mainly found below the soil surfaces (30). Antarctic
soils are largely aerobic and most microorganisms isolated from this habitat are
aerobic heterotrophs. Although a few anaerobic bacteria have been isolated from
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TABLE 3 Soil edaphic and microbial characteristics at four Dry Valley sites (reproduced from
References 24, 25, and 28 with permission)
Properties
Victoria Valley
Coalsack Bluff
Barwick Valley
Wheeler Valley
Position
77◦ 20 S
84◦ 14 S
77◦ 20 S
77◦ 12 S
Substratum
Dune sand
Sand on
Berg Moraine
Pattern ground
sand
Gray-brown
sand
Moisture (% dry wt)
0.14
1.58
1.74
4.30
pH
8.0
6.5
8.3
8.1
Organic C (% wt)
0.02
0.38
0.02
0.17
Organic N (% wt)
0.003
0.024
0.004
0.024
Inorganic ions
(ppm dry wt)
Ca
NH4
NO3
Cl
PO4
SO4
140
1.0
2
835
0.05
6
50
0.1
742
110
0.00
120
1
0.8
1
5
0.15
3
20
ND
7
41
0.20
15
50
12,000
0
0
0
29,000
400
5100
0
0
52,000
85,000
300
—
0100
120,000
1.3 × 106
2
200
6.4 × 106
CFU (G.D.W.)−1
Bacteria
2–5◦ C
10–22◦ C
Yeasts
Microfungi
Algae
ND, not determined
Antarctic mineral soils, attempts to isolate anaerobic sulphate reducers from Ross
Desert soils have been unsuccessful (25). No anaerobic bacterial or archaeal 16S
rRNA gene signals have been observed in extensive phylogenetic studies of Dry
Valley mineral soils (J.J. Smith, L. Ah Tow & D.A. Cowan, unpublished results).
Both cosmopolitan and indigenous fungal, yeast, and protozoan species have
been isolated from McMurdo Dry Valley mineral soils (Table 4). Filamentous
fungal cell counts of less than 200 cfu per gram of soil were obtained from Ross
Desert samples, the lowest reported counts for the various Antarctic soil environments (25). Yeasts are relatively abundant in the surface horizons of certain
moist Antarctic soils (4, 26). The predominant algae isolated from Antarctic soil
were the oscillatorioids, Microcoleus sp., Schizothrix spp., Anacystis spp., and
Coccochloris spp. Flagellated and amoeboid protozoa have also been isolated
from moist Antarctic soils (29). Thus while a few endemic microbial species
have been isolated (78, 102, 128), most bacteria isolated from Antarctic soil
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TABLE 4 Microbial species isolated from Antarctic Dry Valley soils (summarized with
permission from Reference 153)
Microorganism Indigenous to Antarctica
Cosmopolitan genera
Fungi
Monodictys austrina,
Chrysosporium verrucosum,
Acrodontium antarcticum,
Chalara antarctica, Phialophora
dancoii, Thelebolus microsporus
Acremonium, Alternaria,
Aspergillus, Aureobasidium,
Beauveria, Botrytis, Camposporium,
Chrysosporium, Cladosporium,
Epicoccum, Exophiala, Fusarium,
Geotrichum, Gymnascella,
Helminthosporium, Hormoconis,
Myceliophthora, Nectria, Paecilomyces,
Penicillium, Phialophora, Phoma,
Racodium, Sepedonium, Sporothrix,
Sporotrichum, Stephanosporium,
Trichoderma, Trichophyton,
Tritirachium, Verticillium, Wardomyces,
Mortierella, Mucor, Rhizopus
Yeasts
Cryptococcus consortionis,
C. lupi, C. socialis,
C. vishniacii, Leucosporidium
have been found to be cosmopolitan in distribution (Table 4). Bacteria isolated
from McMurdo Dry Valley soils most commonly belong to the following genera: Achromobacter, Arthrobacter, Bacillus, Corynebacterium, Flavobacterium,
Micrococcus, Planococcus, Pseudomonas, Streptomyces, and Nocardia (23). Coryneforms are the most abundant bacteria isolated from Dry Valley soils (85% of
which were represented by Corynebacterium sepedonicum) (23).
It is widely accepted that culture-dependent methods are strongly biased and
that the 1% to 10% of microorganisms that can be detected by culture-dependent
techniques (70) are not representative of the natural population (3). Cultureindependent techniques such as small subunit (ssu) rRNA gene sequence analysis
and in situ hybridization (2, 3) have proved to be invaluable in phylogenetic studies
of soil microbiota (including viable, nonviable, and dormant microorganisms). It
is highly revealing that sequences retrieved from environmental clone libraries are
most often not represented by any cultivated organisms (156).
Although there have been numerous phylogenetic surveys of microbial species
present in various temperate and tropical soils (86, 92, 109), few published data
yet exist from phylogenetic studies of Antarctic Dry Valley mineral soil communities. Phylogenetic analysis of DNA extracts from mineral soils collected from
the slopes of the Miers Valley (Ross Desert) indicated that as many as 50% of the
retrieved sequences are from uncultured bacteria (J.J. Smith, L. Ah Tow & D.A.
Cowan, unpublished data). Most of the remaining sequences are from bacteria
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belonging to the Actinobacteria (27%), Bacteroidetes (11%), Acidobacteria (6%),
and Verrucomicrobia (6%). In a separate phylogenetic study performed on mineral soil collected from heavily impacted gravels from McMurdo station, bacteria
were identified as belonging to the following phylogenetic groups: Actinobacteria (12.5%), Bacteroidetes (25%), Firmicutes (12.5%), Planctomycetes (12.5%),
and Proteobacteria (37.5%) (E.M. Kuhn & D.A. Cowan, unpublished data). The
observation that a high percentage of bacteria inhabiting Antarctic mineral soils
has not been assigned to a phylogenetic group, let alone identified at the genus
level, is entirely consistent with phylogenetic data from many other microbial
biotopes.
Sensitivity to Environmental Impacts
The Dry Valleys and other ice-free regions of the Antarctic continent have a history
of human intervention of a little over a century. The combination of geographical
isolation and environmental extremes provides some protection against direct human impacts, but little against global or regional climatic change. The former is
further controlled by the existence of international treaties and by the designation
of particularly sensitive areas as Sites of Special Scientific Interest. The sum of
these factors means that much of the ice-free land area of the Antarctic continent
can still be regarded as pristine.
However, our fascination with this continent results in a continued increase
in human activities (research, exploration, tourism) on the continent. The impact
of these activities is by no means homogeneous: Research bases now constitute
sizeable towns, field research concentrates on a relatively limited number of sites
(such as the Taylor Valley, the Wright Valley, and Mars Oasis), and current tourist
activity is localized to sites of interest such as penguin colonies and historic hut
sites. All these activities impose physical, chemical, and biological burdens on the
local environment (see Table 1).
Possibly the most damaging effects resulting from increases in human activity in the ice-free areas of Antarctica are from physical (in the form of physical
abrasion, compaction, trampling, and disturbance of soils) and chemical (for example, eutrification, fuels spills, chemical debris) impacts. Physical disturbance
of the mineral soils lead to some disruption of stratified microbial communities.
In addition, the movement of individuals from one area to another results in crosscontamination of microorganisms between niches. Such impacts tend to invalidate phylogenetic studies performed on so-called pristine environments. There is
also an increased risk of contamination at the macroscopic level, for example, by
fuel-spill contamination (48). Although typically localized, such gross contamination is expected to have a dramatic and disruptive effect on the extant microbial
community.
Cold desert soils, once thought to be sterile, are now known to be inhabited by
a wide variety of microorganisms (55). Many of these microbial species appear
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to belong to cosmopolitan taxa (153), although some are apparently endemic.
Natural vectors aid the dissemination of microbes into and within the Antarctic
continent (151). These include atmospheric circulation, oceanic circulation, and
migratory mammals, birds, and fish, all of which contribute directly or indirectly to
the introduction of nonindigenous microorganisms. Given that natural processes
continuously seed nonindigenous microorganisms into the Antarctic continent,
researchers might argue that additional dissemination of bacteria from human
activities is of little significance.
That human activities do contribute nonindigenous microorganisms to the local
environment has been clearly established by a number of recent studies that show
contamination by human commensal and fecal microorganisms of mineral soils and
aquatic systems in the vicinity of permanent bases and temporary camps (5, 19, 20,
49, 97, 132, 143). Regardless if the human-derived contaminants can survive the
harsh environmental conditions in Antarctica, these results should be considered in
the context of lateral gene transfer (LGT) between nonindigenous and indigenous
organisms. Naked microbial DNA survives for long periods in Dry Valley soils (L.
Ah Tow & D.A. Cowan, unpublished results). LGT between bacteria in the soil
environment is a relatively common event (50, 71, 84). Evidence shows that LGT
can occur over large geographic distances owing to particulate dispersal (71, 151).
To date, there is no direct evidence for LGT in the Antarctic environment, nor is it
clear whether such a process would be relevant, advantageous, or disadvantageous
to Antarctic microbial communities.
Regional or global climate change has the potential to dramatically impact
Antarctic environments. Interestingly, the hole in the South Polar ozone layer and
its associated increase in incident UV radiation may not have a direct impact on
Dry Valley mineral soil communities, which are thought to avoid the exposed upper
surfaces of mineral particles. However, the dependence of mineral soil communities on lacustrine-derived organic material as a key source of C or N suggests that
secondary effects from changes in lake productivity might be important. These
arguments may also be applied to a range of other climatic changes, including
regional temperature regimes. A net cooling of Eastern Antarctica during summer and autumn periods between 1966 and 2000 (47) appears to coincide with a
warming of the western side of the Antarctic Peninsula, especially in winter (1951
to 2000) (141), with an increase of 1.09◦ C per decade during winter and 0.56◦ C
per decade annually. Such regional differences suggest that it may be impossible (and unwise) to assume any continent-wide climate changes. Nevertheless,
temperature increases in ice-free areas are expected to increase the availability of
liquid water (from glacial and permafrost melting, and possibly from precipitation), with possibly dramatic changes in microbial biomass, microbial productivity, and community structure. Ross Desert soils subjected to temperatures above
0◦ C show large increases in culturable bacteria (11), while the enclosure of Dry
Valley desiccated mineral soils under transparent plastic cloches resulted in the
rapid growth of moss and cyanobacterial consortia (D.D. Wynn-Williams, personal
communication).
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LITHIC MICROBIAL COMMUNITIES
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Introduction
The harsh ground surface environment associated with the ice-free area of Antarctica, characterized by high seasonal radiation, low water activity, and extremely
low temperatures with high daily temperature fluctuations, has generated a variety
of highly specific biotopes. One of the more obvious examples of exploitation
of a biotope specifically to avoid climatic extremes is the existence of microbial
communities associated with porous and translucent rocks (endoliths).
Although endolithic microbial communities are distributed worldwide, including in hot deserts (62), they have been most intensively studied in the Antarctic
Dry Valleys through the efforts of Imre Friedmann and his coworkers. Several
comprehensive reviews of this work are available (108, 130, 165).
The Physical and Chemical Environment
The endolithic microbial communities of the McMurdo Dry Valleys are restricted
to rock types that offer suitable microhabitats. The most important physical characteristics are porosity (providing interstitial spaces for microbial colonization) and
translucence (facilitating photosynthetic activity in the endoliths). These properties are found in the fine-grained Beacon sandstones, the dominant substratum of
the Dry Valleys (108), but are also characteristic of coarse-grained quartzites (165)
and limestones (57).
Organisms inhabiting rock surfaces and shallow cracks are subject to physical
abrasion (from wind-blown sand) and rapid thermal fluctuations (165). However,
endolithic microbial communities, even if only a few millimeters below the rock
surface, are largely protected from extreme temperature fluctuations because of
the thermal buffering of the rock. Nevertheless, the endolithic microenvironment
is in equilibrium with the external temperature for much of the Antarctic year.
Friedmann and coworkers (61) have estimated that metabolism is possible in endolithic microbial communities for less than 1000 h per annum, based on an
assumption that the lower limit for endolithic metabolism is between –6 and –8◦ C
(144).
Water supply is generally thought to be limiting in endolithic environments,
particularly during the short summer period, when the elevated temperatures and
presence of sunlight are conducive to photosynthesis. Intermittent snowfalls may
be the only source of water (60), although the possibility that the upward diffusion
of water vapor or transport of liquid water from a melting ice–permafrost interface
can support microbial growth in hypolithic biotopes should not be discounted.
Endolithic communities wholly depend on photoautotrophic energy capture
(108). Substrate enrichment, culturing, and phylogenetic studies have provided no
reliable evidence for chemoautotrophy (45, 144, 165). The light-attenuating effect
of the crystalline rock strata is substantial (165), in which the surface photon
density may be reduced by three orders of magnitude at a depth of 2 mm (the
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upper surface of the lichen zone) and four orders of magnitude at a depth of 3 mm
(the green algal zone). Low light intensities notwithstanding, endolithic growth
may not be light limited (81). Instead, the limited availability of CO2, resulting
from its low atmospheric concentration (153), compounded by the low diffusion
rates into crystalline rock strata, suggests that C availability is the major factor
limiting productivity. The availability of CO2 is not expected to be limited in
cryptoendolithic communities that occupy marbles and other carbonate-rich rock
types because of solubilization by excreted organic acids (79).
Although N2 fixation in endolithic communities has been reported to be rare
(59), the failure of exogenous N additions to stimulate respiration has been taken
as an indication that N is not limiting. Fixed N in snow meltwater may be the
dominant supplement to the endolith community N cycle.
Composition of Lithic Communities
Rock-based microbial communities have been defined (58) on the basis of localization. Chasmoendolithic organisms inhabit cracks in weathering rocks (Figure 4a),
and cryptoendolithic organisms exist in the interstices of crystalline rock structures (Figure 4b). Hypolithic microbial communities reside on the underside of
translucent stones (Figure 4c). The upper or exposed surfaces of rocks are thought
to be essentially abiotic, at least as assessed by culture-based studies (108) and
ATP analysis (D.A. Cowan, unpublished results).
Chasmoendolithic microbial communities are widespread in ice-free areas
around the Antarctic continent, since freeze-fracturing of rock strata is a common occurrence. These biotopes are principally occupied by endolithic lichens
(fungal hyphae with the green algal symbiont Trebouxia) and cyanobacterial associations (Chroococcidiopsis or Gloeocapsa species) (108). Little is known of the
diversity of nonphotosynthetic prokaryotes that is almost certainly associated with
these photoautotrophic communities. To the authors’ knowledge, no phylogenetic
studies have focused on chasmoendolithic microbial communities.
The cryptoendoliths have been extensively studied, originally by microscopic,
chemical, and culture-based methods (108), and only recently by the use of phylogenetic tools (45). Two dominant community types have been identified: lichendominated and cyanobacteria-dominated assemblages. The different communities
generally have a clear zonal stratification where, for instance, the lichen-dominated
community has an upper layer of lichenized fungal mycobionts in intimate association with the phycobiont Trebouxia, while the lower zones are dominated by
cyanobacteria. Culture-dependent studies of heterotrophic bacteria associated with
lichen-dominated endolithic communities showed a dominance of gram-positive
cocci (129, 130) and various actinomycetes (108).
A recent comprehensive phylogenetic study of both lichen- and cyanobacteriadominated communities, in which more than 1100 individual 16S rDNA clones
were analyzed (45), has shown that these biotopes contain an extensive and varied bacterial population. Community DNA extracts were PCR amplified by both
eukaryal and universal bacterial primer sets, and over 50 groups of phylotypes
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(at greater than 98% identity, equivalent to species similarity) were identified. In
the lichen-dominated community, three phylotypes accounted for over 70% of the
clones: the fungus Texosporium sancti-jacobi (29%), the green alga Trebouxia
jamesii (22%), and chloroplast-related sequences (22%). Both Texosporium (mycobiont) and Trebouxia (phycobiont) form lichenized associations (56) and together almost certainly represent the dominant Buellia lichen constituent of the
endolithic community. Other fungal and algal phylotypic signals represented only
a minor proportion of the total clones (<2%). Bacterial phylotypes comprised over
15% of the clones sequenced, with members of the order Cytophagales dominating.
Phylotypes belonging to the class Actinobacteria (Blastococcus sp., Microsphaera
sp., Sporichthya sp., Rhodococcus sp.), to the α-proteobacteria (Sphingomonas
sp., uncultured clones), to the γ -proteobacteria (Actinobacter spp.), and to the
Planctomycetales were identified by BLAST analysis, though all at relatively low
frequency.
In the cyanobacteria-dominated community sample, cyanobacterial phylotypes
(principally from the Leptolyngbya-Phormidium-Plectonema group) (34) constituted over 30% of clones sequenced. Phormidium species have been widely identified in moist Antarctic environments (135) and constitute dominant phylotypes
in high-altitude and the (rare) carbon-rich McMurdo Dry Valley mineral soils
(D.A. Cowan, L. Ah Tow & J.J. Smith, unpublished results). Heterotrophic bacterial phylotypes represented nearly 60% of the clones tested, falling into two
major groups: the α-proteobacteria (∼34%, virtually all Blastomonas sp.) and the
Thermus-Deinococcus group (26%). The latter sequences showed an Antarcticspecific clade within this group, treeing with other uncultured Antarctic phylotypes
(45). The presence of the putative Blastomonas-like phylotypes suggests that the
cyanobacteria are not the sole contributors to primary productivity, as previously
suggested (108). Blastomonas and related species are aerobic anoxygenic phototrophs (166) that possess functional light-harvesting complexes. The authors (45)
also make the intriguing suggestion that the quantitative equivalence of cyanobacterial, α-proteobacterial, and Deinococcus-like clones implied that these organisms
were involved in a “tightly regulated syntrophic relationship.” The existence and
nature of this relationship can be addressed by culture and consortium assembly
approaches (probably with difficulty, given that members of this consortium have
so far proven to be unculturable) or by substrate labeling/tracing techniques.
Sensitivity to Environmental Impacts
The sensitivity of Antarctic endolithic microbial communities to climatic, human,
and other impacts cannot readily be quantitatively assessed. A qualitative analysis
may suggest that these communities, which have adopted an avoidance rather than
adaptive survival strategy (165), are rather delicately poised, both spatially and
metabolically, with respect to their requirements for adequate supplies of light,
water, and nutrients. Estimates of the low rates of photosynthesis may suggest that
any climatic changes that reduced the immediate ambient temperature (including
indirect effects such as an increase in cloud cover) may have drastic consequences
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in terms of primary productivity. Similarly, a significant reduction in atmospheric
humidity or in annual snowfall, both potential products of a fall in mean temperatures on the Antarctic plateau, may disturb the delicate balance in subsurface
positioning of endolithic communities. Should an increase in atmospheric desiccation reduce the viability of the upper layers of the community, total productivity
could be substantially reduced owing to the greater attenuation of light at increased
depth.
Endolithic communities are probably not at any particular risk from physical
impacts, either from an increase in human activities or from changes in the degree of abrasion induced by wind-blown sand. Most principal sites of Antarctic
endoliths are relatively remote from coastal areas, are at high altitude, are inaccessible other than by helicopter, and are therefore unlikely to suffer from excessive
physical impact by humans, even with the inevitable future expansion of nonscientific Antarctic activities. Key sites (such as Battleship Promontory) can readily
and effectively be protected if designated as Sites of Special Scientific Interest.
LAKE COMMUNITIES
Introduction
Antarctica contains numerous high-latitude continental lakes (such as Lake Vanda
in the McMurdo Dry Valleys; Figure 5a), most of which have existed for very long
periods. For example, lakes in the Taylor Valley are estimated to be 10,000–24,000
years old. Lakes arise from the collection of summer meltwater in catchment basins.
It has been proposed (119) that sand particles blown onto glacial ice could act as
solar collectors that initiate melting of the ice that surrounds the sand particles.
As a depression forms, more sand accumulates, enlarging the depression, until a
proglacial lake is formed. Many of the Antarctic lakes have a thick perennial ice
cover (Figure 5b).
In contrast to the ice-covered lakes, Antarctic hypersaline lakes and ponds
are not ice-covered. An example of such a hypersaline pond is Don Juan Pond
(Figure 6, follow the Supplemental Material link from the Annual Reviews home
page at http://www.annualreviews.org). This water body is thought to have arisen
owing to deposition of sea spray on snow and glacial ice. Meltwater transports the
sea salts into the Dry Valleys, producing water with an ionic composition similar
to seawater. Evaporation and sublimation of the water lead to concentration of the
salts, particularly calcium chloride (157). The extremely high salt concentration in
the Don Juan Pond (∼33%) lowers the freezing point of this water body to –53◦ C
(31).
The Physical and Chemical Environment
Unlike the harsh environmental conditions experienced in the Dry Valley mineral soils, Antarctic lakes provide a buffered and protected aquatic environment
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to aquatic microbiota. Not uncommonly, Antarctic lakes are meromictic (stratified, nonhomogeneous) in nature because of a combination of factors that include
proximity to the sea, presence of an ice cover, the surrounding arid environment,
and inflowing streams (131).
A major physical factor contributing to the environmental buffering of the
lakes is the presence of ice cover. Ice cover prevents wind turbulence and reduces
temperature fluctuations (68). During summer, peripheral moats (melting of the
peripheral ice cover) allow the inflow of water from the melt streams, which results
in steep salt gradients in the water column that in turn produce specific niches that
are occupied by different aquatic biota.
Light penetration to the water column depends on the thickness of the ice cover
(112). For example, Lake Vanda has a thin ice cover that allows transmission of
solar radiation (18% of incident photosynthetically active radiation) through the
ice to heat the underlying water. Absorption of incident infrared radiation by the
benthic sediment results in temperatures at the bottom of the lake being warmer
than the overlying water (14). In lakes with thick (e.g., 4–6 m) ice cover, much
less light (<1% of incident photosynthetically active radiation) penetrates to the
water column.
Ice cover also restricts gaseous exchange between the atmosphere and the water column (159). Microbial mat photosynthesis and oxygenated inflow water at
peripheral moats contribute to the dissolved O2 content of lake waters. Owing to
stratification in most Antarctic lakes, a dissolved O2 gradient forms, ranging from
400% supersaturation immediately underneath the ice cover to anoxic conditions
near the bottom. Thin ice cover results in cracks that facilitate gas permeation,
reducing the O2 supersaturated zone.
One of the major environmental regulators of microbial activity in high-latitude
lakes is the deposition of sediment (107). Sediment cores collected from the bottom
of the Dry Valley lakes show alternating layers of organic and inorganic material.
Reduction in ice cover results in an increase in sediment deposition and an increased
rate of burial of microbial mats (131). The trapping and binding of precipitated
sediment by the microbial mats, particularly cyanobacterial mats, results in benthic
mat structures that resemble stromatolites (165).
A combination of salinity, temperature, and chemical stratification plays vital
roles in the microbial ecology of Antarctic lakes. Salt content of Antarctic lakes
originates from chemical weathering of rocks as well as from the marine environment (66). Lakes of marine origin such as Ace Lake and Deep Lake in the Vestfold
Hills possess ionic compositions similar to seawater (54), while others such as
Lakes Hoare, Fryxell, and Vanda, which are not of marine origin (66), have ionic
compositions consistent with glacial meltwater inflow (94).
Stratification within the lakes allows the formation of inorganic and organic nutrient gradients, and different Antarctic lakes have widely differing nutrient levels.
For example, Lakes Hoare and Fryxell contain low concentrations of fixed N and P,
similar to the levels found in their input streams (63). Fixed N (mainly in the form
of urea) is added into the lakes via glacial melt streams (at 100–200 mg N m−3),
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with ∼10% of the total N budget attributable to N fixation by cyanobacteria (75).
In contrast, Lake Vanda has a high N concentration but a low P concentration
(32), the latter precipitating as hydroxyapatite. Nitrifying bacteria contribute to N
stratification in lake water columns (145).
In general, Antarctic lakes are rich in dissolved organic compounds compared
with temperate-latitude lakes (131). Total organic carbon and dissolved organic
carbon vary with depth, and values as high as 110 and 186 mg C l−1, respectively,
have been determined (95).
Microbial Lake Communities
The presence of lake ice cover results in stratifications along the underlying water
column, producing unique niches that are occupied by various microbiota. Bacterial cell densities in four Dry Valley lakes (Lakes Hoare, Vanda, Fryxell, and
Miers) ranged between 105 and 106 cells l−1 and generally occupied the zones
of maximum photosynthesis (145, 148), while zooplankton seemed to be absent
(114). In contrast, zooplankton were found in many lakes in the Vestfold Hills. A
summary of the planktonic and associated microbiota in several lakes in southern Victoria Land can be found in the review by Simmons et al. (131). Bacterial
isolates representing new genera or species from the various Antarctic lakes have
been reported (Table 5).
TABLE 5
New microbial genospecies isolated from various Antarctic lakes
Lake
Water column
Ekho Lake (East Antarctica)
Lake Vanda (S. Victoria Land)
Organic Lake (Vestfold Hills)
Ace Lake (Vestfold Hills)
Sediments/mats
Cyanobacterial mat
Pond sediment (McMurdo Ice Shelf)
Pond sediment (McMurdo Ice Shelf)
New bacterial species
Reference
Antarctobacter heliothermus
Roseovarius tolerans
Staleya guttiformis
Sulfitobacter brevis
Saccharospirillum impatiens
Friedmanniella lacustris
Nocarioides aquaticus
Nesterenkonia lacusekhoensis
Carnobacterium strain
Flavobacterium gondwanense
Salegentibacter salegens
(87)
(88)
(90)
(90)
(89)
(91)
(91)
(40)
(14)
(46)
(46)
Methylosphaera hansonii
Flavobacterium tegetincola
Planococcus antarcticus
Planococcus psychrophilus
Psychromonas antarcticus
(9)
(96)
(124)
(124)
(105)
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Water Column Communities
Lake Vanda (Figure 5a) is the most oligotrophic lake in the world but nevertheless
supports three distinct algal communities distributed in the water column (148).
An algal community was found to occupy a large thermal convection cell, while
a microflagellate community is present immediately beneath the ice cover. Most
plankton occupy the bottom of the water column at the oxic-anoxic interface. This
planktonic community is called the deep chlorophyll maximum and coincides
with maximum biomass and photosynthesis in the lake (131, 165). In Lake Fryxell
(Taylor Valley) an abundance of Pyramimonas sp. and Chroomonas lacustris was
reported to coincide with the zone of maximum production (145). Protozoans and
rotifers were reported at the oxic-anoxic zone of Lake Fryxell.
Ace Lake (Vestfold Hills) is a seasonally ice-free meromictic lake. Only four
flagellate species from this lake have been reported: Pyramimosa gelidicola, Cryptomonas sp., a dinoflagellate, and a microflagellate (21). The major bacterioplankton were the photosynthetic green sulfur bacteria Chlorobium vibrioforme and
C. limnicola. Photosynthetic purple bacteria, methanogenic bacteria, and sulfatereducing bacteria were also identified, which suggests the presence of a complex
and sophisticated trophic structure.
Microbial Mats
Microbial mats, which develop on the upper surface of lake sediments (Figure 7),
are formed from filamentous matrices of cyanobacteria, particularly Phormidium
frigidum and Lyngbya martensiana (53). Heterotrophic bacteria, fungi, protozoa,
and eukaryotic algae are also present in these mats (160). P. frigidum is ubiquitous
in southern Victoria Land and has been isolated from various terrestrial and aquatic
environments. Five benthic mat morphologies have been identified thus far. The
three major morphologies are pinnacle mats (found in Lakes Bonney, Hoare, and
Vanda), “lift-off” mats (found in all Dry Valley lakes except Lake Vanda), and
prostrate mats (found in all Dry Valley lakes, especially Lakes Chad, Fryxell, and
Hoare) (115).
Pinnacle mats (Figure 8) are 2–5 cm high and 3–5 cm wide at the base and consist of alternating translucent light-brown and greenish-purple layers, interspersed
with sand and calcite crystals. Lift-off mats occur because of high concentrations of dissolved gases in shallow waters (160) and the genesis of gas bubbles
within the benthic mat. Lift-off mats remain fixed and form columnar calcite
structures (see Figure 7) or tear loose and float to the top of the water column
(160) (Figure 8), eventually penetrating the overlying ice to be dispersed by wind
to the surrounding environment as an inoculum or nutrient source. Phylogenetic
studies performed on mineral soils collected from the shores of an ice-covered
lake in Miers Valley showed a predominance of cyanobacteria (43%) including
Phormidium, Oscillatoria, Cylindrospermum, and Nostoc species (J.J. Smith, L.
Ah Tow & D.A. Cowan, unpublished data), some of which are likely to be of lake
origin.
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Figure 8 Structures of benthic cyanobacterial mats in Antarctic lakes (reproduced
with permission from Reference 131).
Prostrate mats include both aerobic and anaerobic microniches. An actively
photosynthesizing aerobic layer is located toward the upper surface of the mat.
The microbial diversity in the aerobic layer is similar to that found in pinnacle and
lift-off mats (131). Anaerobic prostrate mats contain Leptothrix sp., Achroonema
sp., Planctomyas sp., Thiothrix sp., Clostridium sp., as well as the anaerobic photosynthetic green sulfur bacterium, Chloroflexus (131).
Phylogenetic studies on Antarctic benthic mats have shown that they contain a
high microbial diversity (10, 13, 133, 138) (Table 6). A high diversity of purple
nonsulfur bacteria in Lake Fryxell was also observed (83). Phylogenetic studies
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TABLE 6 Microorganisms isolated from or detected in microbial mats from Lake Fryxell
(Taylor Valley)
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Phylogenetic taxa
16S clone library
Microbial isolation
Reference
Bacteria
Actinobacteria [3]
Clostridium-Bacillus [24]
Cytophaga-FlavobacteriaBacteroides [10]
α-Proteobacteria [11]
β-Proteobacteria [7]
γ -Proteobacteria [3]
σ -Proteobacteria [5]
Verrucomicrobiales [5]
Actinobacteria [4]
Clostridium-Bacillus [10]
Flavobacterium [2]
Planctomycetes [1]
α-Proteobacteria [1]
β-Proteobacteria [4]
γ -Proteobacteria [4]
(13)
Cyanobacterial order
Nostocales [2]
Oscillatoriales [16]
Nostocales [3]
Oscillatoriales [5]
(138)
Numbers in brackets in columns 2 and 3 indicate the number of different species identified within the given phylogenetic groups.
on Bratina Island meltwater pond sediments revealed the presence of sulfatereducing δ-proteobacteria, an indication of the low redox potential of the sediment
core fractions (133). Archaea belonging to the Crenarchaeota and Euryarchaeota
groups have also been detected in microbial mats by culture-independent methods
(10, 13, 133).
Sensitivity to Environmental Impacts
Temperature change potentially offers one of the major environmental impacts on
the lake systems in Antarctica. A continued decrease in atmospheric temperature
(47) may lead to a decrease in glacial melt streams, reduced inflow into the lakes,
and a reduction in lake volumes. Ice volume and coverage should increase, further reducing free water volumes. Thicker ice cover reduces light penetration to
the water column. Although the planktonic communities in Dry Valley lakes are
adapted to low photosynthetic photon flux densities, photosynthetic C fixation is
linearly related to light intensity (144). A reduction in photosynthetic capacity
clearly interferes with microbial community structure and nutrient cycling within
Antarctic lakes.
Conversely, a net warming such as that reported for the western side of Antarctica (141), leads to an increase in glacial meltwater volumes. Increased water flow
rates increase sediment scouring and transport. The effect of higher sediment loads
in lake water columns and enhanced deposition onto the lake floor is expected to
reduce lake productivity, possibly outweighing the positive effects of higher atmospheric mean temperatures.
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FLOWING WATER SYSTEMS
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Introduction
Antarctic streams and rivers originate from melting snow, ice fields, and glacial ice.
Flowing waters occur only seasonally for limited periods, from a few weeks to a
few months, depending on the warmth of the season. Coastal continental Antarctica
contains numerous flowing water systems that can be divided into three types: percolating flows, melt-streams, and rivers (67, 152). Percolating flows generally flow
over rock faces, down glaciers, and through saturated soils. However, the major
type of flowing water in Antarctica is melt streams. Numerous meltwater streams,
flowing in well-defined perennial channels in ice-free ground, have been observed
in southern Victoria Land and on Ross Island during the summer season periods
(66). Small streams have also been observed flowing across the surface of glaciers
and ice shelves on the McMurdo Ice Shelf (75) and the Amery Ice Shelf (100).
Flow rates may be considerable. The Onyx River (Wright Valley) discharges into
Lake Vanda at a rate of up to 14 m3 s−1 with an annual discharge of 2 × 106 m3 (37).
Stream flow rates are primarily controlled by solar radiation, which controls
the melting of snow and glacial ice. In southern Victoria Land, the glacier-fed
streams experience a short period of high discharge associated with early season
melt (76, 146). The sediment loads of input streams range from <1 to >1000 g m3,
depositing mineral particulates and micronutrients into lake systems (99). Streams
flowing out of lakes, such as the Miers River (147), contain lower sediment loads
because of prior settling.
Nutrient availability in Antarctic streams is subject to considerable seasonal
variation and is associated with freeze-thaw cycles. The highest nutrient concentrations correspond to the first flow. For example, the Onyx River contained three
times more nitrate and twenty times more dissolved reactive P on the first day of
flow than at any other time of the season (146). High concentrations of dissolved
organic nutrients have also been reported. In the Fryxell Stream (southern Victoria
Land), the dissolved organic nutrient concentration increased with distance downstream, possibly owing to extracellular release by the streambed microbial mat
communities (75). Other sources include wind-blown organic matter deposited on
glacier surfaces during winter, streambed soils, autochthonous algal production,
and ornithogenic deposits (152).
Microbial Communities in Aquatic Systems
Microalgae and cyanobacteria are the predominant biota found in Antarctic flowing
waters. However, most of the microbial studies performed on Antarctic flowing
waters have focused on phototrophs, and microbial heterotrophs have received
little attention.
In shallow meltwater channels flowing over glacial ice, Prasiola calophylla
(Carmichael) meneghini is the dominant green alga. The cyanobacteria Gloeocapsa
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kuetzingiana Naegeli and Nostoc are frequently associated with P. calophylla (18).
On the McMurdo Ice Shelf, a more complex microflora associated with ice channel
streams is observed, including benthic diatoms and Oscillatoriaceae (75).
Flushed mineral soils (flushes) are regions subject to periodic rather than continual inundation by meltwater. These soils develop surface microbial mats dominated by cyanobacteria, including Oscillatoriaceae and Nostoc. Flush communities in continental coastal regions, in nunataks (52), and in maritime Antarctica
(72) have been observed. Various potential N-fixing cyanobacteria [Nodularia
harveyana Thuret, Scytonema myochrous (Dillw.) Agardh, Calothrix parietina,
and Tolypothrix tenuis Kützing], oscillatoriacean genera (Oscillatoria, Lyngbya,
Phormidium, Schizothrix, and Microcoleus), and Gloeocapsa spp. are all associated with microscopic mats in the Vestfold Hills. Flushed soils at Cape Bird
(Ross Island) are dominated by Calothrix parietina and diatoms [Navicula muticopsis van Heurck and Achnanthes brevipes var. intermedia (Kützing) Cleve]
(17). Flushed soils exposed to saline aerosols contain Urospora sp. (a filamentous chlorophyte), while flushed soils of lower salinity contain P. calophylla (17).
The macroscopic Prasiola crispa (Lightfoot) meneghini is a prevalent colonizer
of water-flushed ornithogenic soils. P. crispa has been isolated from flushed soils
around penguin colonies in the Vestfold Hills (16) and on Ross Island (18). Flushed
soils are subject to drying (Figure 9, follow the Supplemental Material link from
the Annual Reviews home page at http://www.annualreviews.org) and the microbial mat communities may be dispersed as dry particulates and act as sources of
nutrient for surrounding oligotrophic mineral soils.
Perennial streams and rivers in Antarctica are colonized by the different groups
of phototrophic organisms: cyanobacteria, green algae, diatoms, mosses, and associated and epiphytic species (153). The most common cyanobacterial communities consist entirely of Oscillatoriaceae (146). An alternative type of cyanobacterial
community identified in the streams of the McMurdo Sound region is mainly composed of Nostoc commune Vaucher. The N. commune communities form a thick
(20 mm) black surface layer and are sometimes associated with mosses.
Many Dry Valley streams support rich growth of the chlorophytes Binuclearia
tectorum (Kützing) Beger and P. calophylla, as well as smaller growths of the
chrysophyte Tribonema elegans Pascher (147). Zygnema and Mougeotia, which
are not found in Dry Valley streams, are dominant, together with Klebsormidium,
in streams on Signy Island (maritime Antarctica) (69).
Diatoms are found mainly on alluvial sands and gravels in streams. Adams
Stream (Miers Valley) is colonized by Hantzschia amphioxys (Ehrenberg) Grunow
and Navicula spp. (76). The sands of the Onyx River (Wright Valley) are colonized
by the diatoms H. amphioxys, N. muticopsis, N. cryptocephala Kützing, Stauroneis
anceps Ehrenberg, and Tabellaria sp. (76).
Mosses are commonly found on the margins of streams and in flushes (99).
Epiphytes associated with mosses include bacteria, yeasts, filamentous fungi, and
microalgae (Nostoc is a common epiphyte of mosses) (42).
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Unlike the microbial mats found in maritime streams and rivers (e.g., Signy Island), the epilithic mats, cyanobacterial films, and chlorophytes found in southern
Victoria Land streams (continental Antarctica) can withstand the freezing winter
conditions (147). Processes such as photosynthesis occur only at low rates within
the microbial mat communities in continental streams. The low photosynthetic
rates are attributable to low ambient stream temperatures and to low viable chlorophyll a contents (147).
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Sensitivity to Environmental Impact
Antarctic streams arise from melting snow and glacial ice. The melting of snow
and ice is highly dependent on solar radiation and ambient temperature. Any
significant change in mean annual temperature obviously has a dramatic effect on
stream volumes. Decreased stream volume, probably also associated with lower
average meltwater temperatures, is expected to reduce microbial productivity in
streams. Conversely, increased stream volumes are expected to increase transport
and scouring processes. Together these reduce the physical stability and longevity
of stream ecosystems. Because streams and rivers are the main source of water
and nutrients to the Antarctic lakes, factors affecting streams and rivers ultimately
have an effect on the lake systems.
ICE MICROBIOLOGY
Introduction
It is arguable whether ice should be considered as a viable microbial biotope
at all. On one hand, glacial ice and snowfields may be considered as no more
than entrapment and storage systems. Microorganisms enter these systems as vegetative and resting cells, transported by wind-blown particulates, aerosols, and
ice crystals, and as unsupported cells. They are trapped by the further addition
and compaction of snow, to be finally released to the surrounding environment
by surface melting or ablation (for terrestrial glaciers), by melting at the glacial
underside-rock interface, or by calving and melting (for marine glaciers). The
timescales of this process can be short (for seasonal snowfields) or extremely long
(e.g., for the Antarctic continental ice cap). It is not clear whether, during the intervening period, these entrapped cells have significant metabolic activity. Certainly,
they have no community structure and should best be described as assemblages
(73).
Conversely, there is good evidence that lake, glacial, and sea ice harbor microniches where, at least during the Antarctic austral summer periods, active
metabolism and cell division occur. These microniches, even if transitory, may
be validly considered to be communities. There is evidence that even under the
most severe Antarctic conditions, viable microbial cells maintain a slow rate of
metabolic activity (33).
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Sea Ice
Sea ice differs substantially from terrestrial (glacial) ice in terms of its origin,
composition, and biology. It is formed by the freezing of seawater, accompanied
by a salting out process, whereby marine salts are excluded from the nascent crystals and concentrated in brine pockets. The ice composition is not homogeneous;
columnar crystals, brine pockets, and brine channels introduce a variety of microenvironments of various temperatures, light intensities, and salt and nutrient
concentrations. In addition, the underside of the sea ice is in intimate association
with the nutrient-rich and biologically active marine biosphere.
Sea ice offers a range of microbial habitats. The lower face of the ice sheet
provides an adhesion surface that is colonized by a wide variety of microorganisms, collectively known as the Sea Ice Marine Communities (137), that consist
of a complex and trophically dependent collection of bacteria, microalgae, zooplankton, and higher eukaryotic grazers (krill). Brine pockets and channels in the
ice interior provide a separate, but interconnected, microbial community and are
usually highly vertically stratified (85). In a detailed culture-based study of sea ice
microbiology, Bowman et al. (7) noted that “a variety of taxa were observed in sea
ice samples which have not been generally observed in open sea water samples.”
The physical, chemical, and microbiological composition of sea ice has been the
subject of several comprehensive and recent reviews (15, 111, 137, 149) and is not
discussed here in more detail.
Polar and Glacial Ice
With the exception of cryoconite holes (see below) and saline pond systems such
as in the vicinity of Bratina Island, polar cap and glacial ice is essentially liquidwater free, other than from transitory melting. More than in any other Antarctic
ice system, these structures act merely as repositories for wind-transported microorganisms. Indeed, microbial counts have been correlated with dust content in
Antarctic ice cores (117). The interest in the microbiology of glacial ice therefore
lies not in the development and function of microbial communities, but in the
survival and stability of deposited microorganisms. Continental glaciers (Figure
10) and ice caps develop by accumulation and compaction of snow, and entrapped
particulates undergo slow downward transport, driven by further accumulation and
lower face attrition (as a result of pressure-dependent melting). Depth is therefore
linked directly to age, and ice cores can be dated by counting annual depositional
layers (140) or chemical analysis (6).
Extensive culture-based studies of Antarctic polar ice cap microbiology have
been undertaken (reviewed in Reference 1). The 2.5 km of Vostok Station ice
cores, recovered during 1974–1989, represent an age period of some 200 kya (1).
Younger samples showed higher viable cell counts than old samples (Table 7). A
wide variety of bacteria, yeasts, and fungi have been isolated, with spore-forming
organisms dominating in older core samples.
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TABLE 7 Microbial isolates from the Vostok ice cores (reproduced with permission from
Reference 1)
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Depth of core
sample (m)
Approximate age of
core samples (year)
Number of innocula
tested
Percentage of
positive innocula
0–105
0–3000
144
20
105–208
3000–7400
129
14
208–320
7400–12,500
250
6
330–1500
12,500–107,000
207
6
1500–2400
107,000–200,000
176
3
Renewed interest in ice microbiology has come from the discovery that enclosed
lakes lie beneath the Antarctic ice sheet. The largest, Lake Vostok (14,000 km2,
maximum depth 670 m), has attracted particular attention because it has been proposed that the lake waters have been isolated from liquid interchange for at least 1
million years (80). The ice above the lake has been cored to 3623 m, approximately
120 m above the lake level, at least 200 m into transitional ice, and some 84 m into
refrozen lake water (accretion ice). A series of microscopic (116), isolation (39),
and phylogenetic studies (39, 120) showed viable microorganisms, particularly
members of the Brachybacterium, Methylobacterium, Paenibacillus, and Sphingomonas lineages, and phylotypes assigned to the β-proteobacteria (Acidivorax
and Comamonas), α-proteobacteria (Afopia), Actinomyces, low and high G+C
gram positives, and the Cytophaga/Flavobacterium/Bacteroides lineage. Cell densities in accretion ice samples have been estimated at between 2 × 102 and 3 ×
102 mL−1, and thought to be dominated by gram negatives (on the basis of the
quantitation of the lipopolysaccharide biomarker) (82).
It seems reasonable to assume that microorganisms entrapped in glacial ice
are metabolically inert. Ambient temperatures on the surface of the polar ice cap
rarely exceed –25◦ C and have been recorded as low as –88.3◦ C at Vostok Station
(131). Mid-winter temperature measurement in deep boreholes at the South Pole
indicated a surface temperature of –52◦ C, rising to –21◦ C at a depth of 2350 m
(118). Extrapolation of temperature-depth profile gave a predicted temperature of
–9◦ C at the 2810-m base of the ice cap. Under such low temperatures, both the
possible freezing of the cytoplasm and the temperature-dependent rigidification
of intracellular enzymes suggest that intracellular catalytic processes might be
halted. However, such a view is at odds with the apparent anomaly of long-term
survival of vegetative cells in ice cores, which intrinsically requires some degree
of metabolic turnover for molecular repair. Indeed, Deinococcus-like organisms
identified in South Polar snow (33) appear to maintain low levels of metabolic
activity (measured by incorporation of tritium labeled thymidine and leucine) at
ambient temperatures of –12 to –17◦ C, and photosynthetic activity in lichens has
been detected at –17◦ C (126). From a simply enzymological viewpoint, this is
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not so surprising because Arrhenius rate law predicts that catalytic (enzyme) rates
should be decreased by only a factor of about 6 from optimum (assuming a Topt
of 15◦ C and the presence of fluid zones in the cytoplasm). Daniel and coworkers
(12) have measured in vitro enzyme activity as low as –100◦ C, demonstrating that,
at least under artificial reaction conditions, some enzymes do not undergo any
dramatic conformational switch-off transitions.
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Lake Ice
Lake ice differs substantially from glacial ice. The permanent floating ice caps
of the Dry Valley lakes (Figure 5b), typically between 3 and 6 m in depth, exist in a dynamic equilibrium owing to freezing of lake water on the underside
and ablation from the upper surface (98). Only the marginal areas melt during
the summer season, to refreeze over winter. The upper surfaces of the permanent ice are subject to constant seeding by particulates of eolian origin (121)
and typically contain a layer of sand and organic matter within the ice profile.
Priscu and coworkers, who have extensively studied the physical, chemical, and
biological characteristics of Antarctic Dry Valley lake ice (65, 110, 121), have
demonstrated that liquid water inclusions within the ice during the summer months
(due to solar heating of the sediment layer) can constitute as much as 40% of the
total ice volume. Measurements of photoautotrophic and heterotrophic activity,
biomass, and chemistry in the sediment layer of Lake Bonney ice indicated that
the sediment layer supports an active microbial assemblage (110, 121). Microscopic analysis showed bacterial and cyanobacterial cells, the latter dominated by
Phormidium with lower numbers of Chamaesiphon and the N2-fixing Nostoc. 16S
rRNA sequence-based phylogenetic analysis showed numerous clones identified
as Leptolyngbya, Chamaesiphon, and Phormidium. Several phylogenetic clades
showed less than 93% identity with sequences in the public databases, indicating
the possible presence of novel cyanobacterial genera (121). Bacterial clones were
identified as members of the genus Rhodoferax, the Acidobacterium/Holophaga
group, the Planctomycetales, and an unnamed green nonsulfur bacterial isolate
(65). While the cyanobacterial phylotypes were similar, and therefore probably
derived from those found in the nearby terrestrial mats, novel bacterial phylotypes
were also identified. However, a much more comprehensive survey of Dry Valley
microbiology is necessary before any statement can be made on whether these
organisms are truly unique to either lake or ice habitats.
Cryoconites Holes
The deposition of solid particulates [e.g., stones (cryoconites), dust, desiccated
algal mat fragments] on the surface of glacial or lake ice is the precursor to the
formation of a unique glacial habitat, the cryoconite hole (Figure 11a). Solar
warming of the particulate body gradually melts the underlying ice, forming a
liquid inclusion in the surrounding solid ice (64). Each hole is spatially separate,
and therefore potentially a unique microcosm.
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Figure 11 Development of cryoconite holes in glacial and lake ice. (a) Cryoconite
hole that results from particulate (cryoconite) deposition on the ice surface. (b) Pseudocryoconite hole in lake ice that results from flotation of algal mat lift-off fragments.
The physical and chemical characteristics of Antarctic cryoconite holes are
well suited to biological activity. During the brief summer period, the holes contain
liquid water several degrees above freezing point. Nutrients accessed from melting
ice, biological N fixation, and fixed carbon from phototrophic activity provide the
basis for a complex community. Isolation and microscopic studies have identified
a wide range of bacteria, algae, diatoms, fungi, and rotifers that inhabit cryoconite
hole waters. This habitat may be one of few in Antarctica inhabited by metazoan
life (158).
During the Antarctic winter, cryoconite hole liquids freeze completely (38). At
some point in the evolution of the hole, the cryoconite will be at sufficient depth
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ENDANGERED ANTARCTIC ENVIRONMENTS
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such that the summer solar heating will fail to open the hole to the atmosphere,
thereby generating a liquid inclusion. In a further evolutionary stage, the inclusion
remains permanently frozen, thereby acting as a nondepositional mechanism for
seeding glacial ice with local concentrations of microorganisms.
A comprehensive analysis of the diversity of microorganisms inhabiting Antarctic cryoconite holes, based on phylogenetic analyses of isolated organisms and
community DNA extracts, has recently been reported (38). Isolated bacteria were
identified as members of the β-proteobacteria, Cytophagales, and Actinobacteria (Table 8), while PCR amplification with universal 16S rRNA gene primers
yielded phylotypes showing high identity with members of the cyanobacteria, γ proteobacteria, Acidobacterium, Cytophagales, Planctomycetes, α-proteobacteria,
Gemmimonas, Verrucomicrobia, and Actinobacteria (Table 8). Many of the sequences and some of the isolates were similar to organisms identified in other
TABLE 8 Organisms identified from culturing studies or inferred from phylogenetic analysis
of cryoconite hole community DNA (adapted with permission from Reference 38)
Cultured isolates
Bacteria
Group
Organisma
Group
Organism
α-Proteobacteria
β-Proteobacteria
α-Proteobacteria
β-Proteobacteria
Unidentified clone
none
γ -Proteobacteria
Acidobacterium
Cytophagales
Pseudoxanthomonas sp.
Unidentified clone
Flexibacter sp.
Planctomycetes
Gemmimonas
Verrucomicrobia
Actinobacteria
Cyanobacteria
None
Pseudomonas
saccharophila
Janthinobacterium
lividum
None
None
Flavobacterium
ferrugineum
Haloanella gallinarum
Flavobacterium sp.
F. succinicans
None
None
None
Arthrobacter sp. [2]
Cryobacterium
psychrophilum
n/a
Unidentified clone
Gemmimonas aurantiaca [2]
Prosthecobacter sp.
Nocardiodes sp.
Georgenia sp.
Unidentified clone
Chamaesiphon sp. [3]
Leptolyngbya sp.
Phormidium sp. [3]
Metazoa
n/a
Metazoa
Fungi
Viridiplantae
Alveolata
n/a
n/a
n/a
Fungi
Viridiplantae
Alveolata
γ -Proteobacteria
Acidobacterium
Cytophagales
Planctomycetes
Gemmimonas
Verrucomicrobia
Actinobacteria
Eukarya
a
Phylotypes
Cyanobacteria
Plectus sp.
Macrobiotus sp. [2]
Philodena acuticornis [3]
Chioromyces meandriformis
Pleurastrum sp.
Spathidium sp. [3]
Genospecies showing highest percent identity in comparison of 16S rDNA sequences with Ribosomal Database and
GenBank sequences. Numbers in brackets indicate numbers of similar clones identified. n/a, not attempted.
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glaciers of the Taylor Valley. In no instance were members of the same genera
observed in both isolate and clone libraries. Amplification of community DNA
with 18S (eukaryote)-specific primers yielded a single algal phylotype and clones
from tardigrades, rotifers, fungi, and ciliates (Table 8), emphasizing the complex
trophic structure contained within the cryoconite hole environment. There was,
however, little evidence of species uniqueness: Virtually all clones were closely related to previously identified Antarctic sequences, supporting the view that glacial
ice microbiology is seeded from the immediate surroundings. Nevertheless, this
conclusion is worth a cautionary note. This phylogenetic study had certainly not
accessed the full microbial diversity, and probably not even a minor fraction of
it. Unique (endemic) microbial species might be present in low numbers, which
would be detected only by examining much larger clone libraries (e.g., in excess
of 1000 clones) from several cryoconite holes.
A variant of the cryoconite hole is observed in Dry Valley lake ice. The transmission of light through the surface ice layer promotes growth of substantial cyanobacterial mats on the surface of the underlying sediment (160). At depths of less than
10 m, bubble formation on the underside of the mats causes lift-off (158), in which
portions of the mat break free and float to the underside of the ice (Figure 11b). The
mat fragments freeze into the ice, move upward by a combination of surface ice
ablation and melting, and eventually melt through the upper surface. In the latter
stages of the process, solar radiation generates a liquid inclusion around the mat
fragment. The cyanobacterial mat consortia remain viable (131) and presumably
support an active microbial community during the progression of the inclusion.
Sensitivity to Environmental Impacts
Ice microbiology populations, whether unique or cosmopolitan, are clearly susceptible to regional warming and the concomitant loss of ice volume. In the context
of terrestrial ice bodies (glaciers, ice caps), this may be of little relevance to microbiology per se. The broader environmental and climatic consequences of this
process are, of course, a separate issue of real importance.
The Dry Valleys are considered to be sensitive to climatic shifts (161). Meteorological data spanning 1966–2000 show a significant degree of cooling (0.7◦ C
per decade) in the Dry Valleys, with an associated decrease in soil water content,
reduced glacial melting, reduced lake input flows, increased lake ice thickness,
reduced primary productivity, and declining numbers of soil invertebrates (47).
One of the many consequences of the continuation of this trend is a dramatic
impact on sensitive lake ice microbial communities, for example, by decreasing
the extent and duration of the liquid-phase inclusions in ice and thereby limiting the
seasonal metabolically active period. More dramatically, a significant decrease in
glacial melting may substantially alter lake levels and lake ice dynamics, possibly
shifting the equilibrium between ice formation and ablation.
Contamination of Antarctic glacial and lake ice systems with nonindigenous
microorganisms and xenobiotic chemicals (from human activities rather than
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natural transport processes; 151) are potential future problems that require international awareness and legislative control. The current stipulations of the Antarctic
Treaty (http://www.nsf.gov/od/opp/antarct/anttrty.htm) provide a framework for
such control. However, this issue has become a focal point in the context of Lake
Vostok, where the deep drilling project has penetrated into lake accretion ice,
within ∼120 m of the surface of the lake. The open drill hole is maintained by
the presence of drilling fluid, some 60 tonnes of aviation fluid, and freons (150).
As a water body that may have been isolated for more than a million years, Lake
Vostok represents “one of the last remaining pristine bodies of water on the planet”
(150). It may also harbor genetically unique microorganisms. It is therefore imperative that further drilling is not commenced until technologies have been developed to (a) prevent the pollution of the lake water by organic drilling fluids, and
(b) minimize the transfer of nonindigenous microorganisms into a potentially
unique microbial environment.
FELLFIELD COMMUNITIES
Introduction
Maritime and continental fellfield soils (i.e., moist high-silt-content soils and drier
sand or gritty ash soils, with discontinuous cryptogamic vegetation; 165) are largely
restricted to the warmer, more northerly regions of the Antarctic continent (the
Antarctic peninsula) and to offshore islands (such as Signy and Marion Islands).
The physical topology of fellfields is governed by climatic factors, frost-heave and
particle sorting (36), desiccation, meltwater, and wind erosion (165). The particle sorting action of the freeze-thaw process generates semiregular surface structures including polygons (36). Unlike Dry Valley mineral soils, maritime fellfield
soils are generally not saline, because of regular leaching (165). N/P nutrient
contents are typically high compared with desert mineral soils (Table 9). Measurements of organic C in fellfield soils (Table 9) showed widely differing levels
(>50% under moss cover compared with 1%–2% in visually bare sites) (134), but
in all cases several orders of magnitude higher than measurements in Ross Desert
soils (0.064% ± 0.035%) (93).
Antarctic fellfields are dominated by cryptogams (mostly mosses and lichens),
but areas of visually barren soil fines also occur (165). The carpet of cryptogams has
a limited depth profile and is generally poorly anchored to the underlying sand-,
ash-, or peat-dominated soils (165). These ecosystems are therefore physically
unstable and highly susceptible to physical disturbance and erosion.
Fellfield Microbiology
The fellfield soils of the Antarctic Peninsula support a structurally complex but
low diversity vegetation that is composed of mosses, liverworts, lichens, and algae.
In more sheltered areas, two flowering plants, the grass Deschampsia antarctica
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Nutrient levels in Antarctic soils (reproduced with permission from References 136
Soil/location
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Fellfield soils
Marion Island
Signy Island
Signy Island
Coastal Antarctica
Desert soils
Ross Desert
Ross Desert
Pensacola Mountains
Pensacola Mountains
Ornithogenic soils
Marion Island
Signy Island
S. Shetland Island
Ross Island
Soil water
content (% wt)
10–20
0.26–5
0.26–5
20–35
Soluble
NO−
3 -N
(µg g−1)
Soluble
NH+
4 -N
(µg g−1)
Soluble P
(µg g−1)
Organic C
(% wt)
0
1.9–6
0.1
1–20
2
3–4
0.1
15–20
4
40–80
40
4–45
24
—
1–50
—
0–120
0–960
<1–1250
0.7–6.4
6–40
0–2.2
<1
0.3–1.1
80–120
0–2.2
0.25–0.5
<0.01
0.0037–0.32
—
—
—
0–130
90
18.8–35
0
101–664
1369
140–400
6000
146–675
4600
50–145
2400
—
—
—
21–24
and the herb Colobanthus quitensis, are found. The Signy Island eukaryotic plant
community supports extensive microbial populations, in particular the cyanobacteria Phormidium autumnale and Pseudoanabaena catenata with subdominant
populations of the diatom Pinnularia borealis (43). Other species identified include Nostoc sp., Achnanthes lapponica, Clamydomonas chlorostellata, Planktospheaerella terrestris, Cylindrocystis brebissonii, Cosmarium undulatum, and
Netrium sp. Species distribution within the polygon structure typical of fellfields
was not homogeneous: Most cyanobacterial cells were found in the top 1 mm of
the soil profile, and nonmotile species were more dominant at the edges of the
frost polygons (43). Filamentous microorganisms may be particularly important
in stabilizing soil structure. The filamentous morphology and the production of
extracellular glycoprotein (165, 127) are thought to bind soil particles and aid in
the production of stabilized microbial mats.
The continental and maritime fellfield communities support substantial heterotrophic microbial populations (44, 163, 164). A variety of bacterial (103), yeast
(104), and filamentous fungal (127) isolations have been reported. However, these
studies provide little information on the nature of the microbial community structure and on the trophic interactions within the community. To the authors’ knowledge, no comprehensive analyses of microbial distribution in fellfield habitats have
been undertaken. For example, the extent to which the vegetative components of
the community possess unique microbial associations (e.g., rhizospheric species)
is currently not known.
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Fellfield-like communities are uncommon in the more southerly regions of continental Antarctica. Only in localized and environmentally benign sites in the Dry
Valleys such as Botany Bay (104) do moss-dominated fellfield-like communities
exist.
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Sensitivity to Environmental Impacts
Fellfield communities, which physically depend on the presence of macroflora
(cryptogams) and filamentous microbiota (cyanobacteria), are potentially susceptible to physical impact. The relatively low eukaryotic species diversity and the
physical structure of the community (a relatively thin biological layer overlying
mobile gravels or peats) make these communities highly sensitive to physical disturbance [whether by human activities, local seal populations (155), or the actions
of wind and water].
Increases in continental snowfall may also impact negatively on communities
that depend on eukaryotic photosynthesis. Measurements of chlorophyll a fluorescence in continental lichen communities suggest that snow cover significantly
reduces the period of active photosynthesis (113). This contrasts maritime Antarctic and European alpine environments, where snow cover acts as a protective cover,
maintaining thallus hydration and extending the photosynthetic period (162).
ORNITHOGENIC SOIL ENVIRONMENTS
Introduction
Ornithogenic soils (i.e., soils modified or generated by the presence of birds; 142)
offer localized and specialized environments that differ widely from other Antarctic microbial habitats. Such soils are generated by the deposition of guano in the
vicinity of bird colonies; the most extensively studied are the Adelie Penguin
colonies of Ross Island and the Vestfold Hills. These environments are unique
among Antarctic microbial habitats in that they do not depend on in situ photoautotrophy, have continuous exogenous nutrient supplementation, and maintain high
nutrient levels, in particular, inorganic nitrogen, phosphorus, and organic carbon.
Relic ornithogenic soils, resulting from the abandonment and subsequent maturation of rookeries, are widespread through maritime Antarctica. These soils provide localized regions of high nutrient concentration in an otherwise nutrient-poor
environment (139).
The Physical and Chemical Environment
Ornithogenic soils (Figure 12) are characterized by high levels of inorganic and
organic nutrients, compared with virtually any other Antarctic terrestrial environment (see Table 9). The soil profile is typically a compacted upper horizon, with an
underlying moist, soft, and sandy loam horizon (136). Both horizons have a high
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saturation level (up to 30% H2O by weight). The nutrient composition is a direct
result of the continued deposition of guano (Figure 13) and shows the high uric
acid and ammonia-N levels typical of guano deposits in other parts of the world
(77). Uric acid degrades to allantoin, urea, and finally ammonia (77), accounting
for the high NH+
4 -N levels (∼5% dry wt.) (136) in ornithogenic soils. Nitrate-N
can also be present at significant levels, much higher than is typical of normal
terrestrial soils (0.5% dry wt; compare with <0.001%) (136). Nitrates can derive
from microbial nitrification, abiotic weathering processes, and auroral activity
(154). Evidence for biological nitrate production in ornithogenic soils is currently
indirect, and no culture-dependent or phylogenetic evidence for the presence of
nitrifying bacteria has yet been published.
Ornithogenic soils also carry a high soluble salt load [>0.7% dry wt; (136)],
levels which are thought to be deleterious to plant growth (101). This may account
for the virtual absence of lichen, moss, and algal growth within the bounds of
active bird colonies, with the exception of ornithocoprophilous lichen growth on
protruding rocks.
Microbiology of Ornithogenic Soils
The organic C contents of ornithogenic soils (Table 9) are high, particularly in comparison with Dry Valley mineral soils. The high levels of organic C are consistent
with estimates of microorganisms by direct microscopic counts [2 × 1010 cells
g−1; (8)] and by ATP analysis [5 × 107–7 × 108; (41)]. Interestingly, low levels
of in situ 3H-glucose uptake have led to suggestions that ornithogenic soil bacteria
are inactive (possibly because of the suppressive effect of organic molecules) or
dead (122). A comparison of the microscopic- and ATP-derived numerical data
suggests that a relatively high proportion of the visible cells may not be viable.
Microscopic examination of ornithogenic soils has shown that up to 50% of the
microbiota are gram-negative nonmotile cocci (123). Although only a low proportion of the cell types were culturable (8), a high proportion of the isolates were
phenotypically similar. Several new species of Psychrobacter were isolated, all of
which could grow on urate as a sole C source. This study led to a proposal that the
genus Psychrobacter predominates in ornithogenic soils (8). To date, no comprehensive phylogenetic analyses of the true microbial distribution in ornithogenic
soils have been reported. More than in other more complex microbial ecosystems,
such studies might be expected to provide useful guidelines for the pathways of
nutrient cycling.
Sensitivity to Environmental Impacts
The dependence of ornithogenic soils, and their associated (possibly unique) microbial diversity, on a constant source of guano is obvious. Abandoned rookeries
undergo a variety of chemical, physical, and biological successional changes (136,
139). Erosion and leaching processes reduce the inhibitory salt concentration, resulting in a proliferation of cryptogamic vegetation and, in maritime sites, plant
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growth. The high level of easily available nutrients in relic ornithogenic soils might
be maintained for centuries and even millennia (106). Although there have been
no comparative studies reported on the microbial distribution in active and relic
ornithogenic soils, the documented changes in nutrient profiles (such as the rapid
loss of uric acid) (136) and the subsequent growth of fellfield-like cryptogamic
and higher-plant-dominated communities suggest that major changes in microbial
population distribution are inevitable.
Climatic change may be the major long-term factor in rookery abandonment
(51), although disturbance caused by human activities has a major impact on
penguin breeding and short-term colony viability (125). Given the attraction of
penguin colonies as targets for tourist activity, careful control of these activities
is critical to avoid detrimental impacts on both the penguin populations and their
associated microbial communities.
CONCLUSIONS
To address the question of whether Antarctic microbial biotopes are truly endangered by human activities on the continent and by current and projected changes
in climatic conditions, we must first ask ourselves if we understand sufficiently
the true microbial diversity and microbial community structure in these biotopes
to appreciate the effects of such impacts. The answer to this question is clearly
negative, at least for most Antarctic biotopes. A large proportion of the many
microbiological studies have either focused on macroscopic biota (such as cryptograms and cyanobacteria) or have addressed the issue of microbial diversity using
culture-dependent methods. The latter are valuable, but may be highly misleading.
Detailed phylogenetic studies of microbial diversity have only recently started to
emerge and are currently restricted to some of the more specialized Antarctic communities (such as endoliths and lake ice and cryoconite hole communities). Other
much more extensive microbial niches, such as cold desert soils and fellfields,
have yet to be characterized in detail.
Understanding microbial community structure in detail is a precursor to meaningful studies of climatic and other impacts, based both in the field and in the
laboratory. To date, such studies have monitored only gross biological changes
(such as the development of moss and cyanobacterial consortia in cloche-enclosed
desert soils, and the disintegration of fellfield mats by trampling) or gross metabolic
changes (e.g., the reduction in lake productivity in response to atmospheric cooling). Though important, these studies reveal little of detailed effects at the level of
microbial diversity, community structure, and trophic interactions.
Our current state of knowledge on Antarctic microbiology is incomplete. In
consequence, our ability to accurately assess the sensitivity of Antarctic microbial communities is limited to the more obvious physical effects. It is clear that
some Antarctic microbial communities are physically unstable (such as fellfield
and flush mats, and moss communities) and steps have already been taken to minimize physical disturbance in these areas. For other communities and for other
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impacts, we do not have the necessary data to assess the sensitivity of the first or
the importance of the second. Therefore, until such data exist, it is appropriate to
maintain a policy of considerable care and caution with respect to these communities. Where possible, the direct effects of human activities should be minimized:
restricted access to particularly sensitive areas, control of nonscientific activities
on and around continental and maritime Antarctica, and minimization of chemical
and biological contamination. Together with a growing awareness of the consequences of climatic change, these restraints will help retain Antarctica as the last
pristine continent.
ACKNOWLEDGMENTS
The authors would like to express their gratitude to those individuals, organizations, and agencies who have collaborated, supported, and funded our research
on Antarctic microbial diversity. Particular thanks are extended to Professors Roy
Daniel, Alan Green, and Craig Cary of the Waikato University Antarctic Terrestrial
Biology Research Program, to Antarctica NZ, and to the South African National
Research Foundation and the SA National Antarctic Program. The authors also
wish to dedicate this article to friend and colleague David Wynn-Williams, who
died tragically in 2002.
The Annual Review of Microbiology is online at http://micro.annualreviews.org
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Figure 2 Dry Valley mineral soils in the Miers Valley, Eastern Antarctica.
Figure 3 Depth profile of a west-facing Dry Valley mineral soil clearly showing the
dry surface horizon (0–10 cm) overlying moist gravels (a depth of ~10–30 cm). The
permafrost layer is at a depth of ~30 cm. Spatula scale: ~15 cm.
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Figure 4 Lithic microbial community habitats. (a) Freeze-fractured rocks that provide chasmoendolithic habitats, (b) cryptoendolithic organisms in coarse sandstone, and (c) a hypolithic habitat.
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Figure 5 The permanent ice cover of (a) Lake Vanda, Wright Valley (picture courtesy of
Dr. David Wynn-Williams), and (b) Lake Miers, Miers Valley. Panel (b) clearly shows the
marginal moat and the accumulation of wind-blown sand/sediment on the ice surface.
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Figure 7 Cyanobacterial mat structures in shallow marginal waters of Lake
Fryxell, Taylor Valley.
Figure 10 The Adams Glacier, Miers Valley. A typical hanging glacier of the
Dry Valleys.
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Figure 12 Ornithogenic soils (evident as the contrasting brown areas of loam) in the
Cape Crozier Adelie Penguin colony, Ross Island.
Figure 13 Genesis of ornithogenic soils. Accumulation of guano in the vicinity of an
Adelie Penguin nest, Cape Royds, Ross Island.
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CONTENTS
FRONTISPIECE, Arnold L. Demain
PICKLES, PECTIN, AND PENICILLIN, Arnold L. Demain
ANAEROBIC MICROBIAL DEHALOGENATION, Hauke Smidt and
Willem M. de Vos
SIGNALING IN MYXOBACTERIA, Dale Kaiser
ANAEROBIC OXIDATION OF METHANE AND AMMONIUM, Marc Strous
and Mike S.M. Jetten
SELECTION FOR GENE CLUSTERING BY TANDEM DUPLICATION,
Andrew B. Reams and Ellen L. Neidle
THE VIBRIO SHILOI/OCULINA PATAGONICA MODEL SYSTEM OF CORAL
BLEACHING, Eugene Rosenberg and Leah Falkovitz
STATIONARY-PHASE PHYSIOLOGY, Thomas Nyström
VIRAL ERROR CATASTROPHE BY MUTAGENIC NUCLEOSIDES, Jon P. Anderson,
Richard Daifuku, and Lawrence A. Loeb
THE ECOLOGY AND GENETICS OF MICROBIAL DIVERSITY, Rees Kassen
and Paul B. Rainey
RIBOSOMAL CRYSTALLOGRAPHY: INITIATION, PEPTIDE BOND FORMATION,
AND AMINO ACID POLYMERIZATION ARE HAMPERED BY ANTIBIOTICS,
Ada Yonath and Anat Bashan
HERPES VECTOR-MEDIATED GENE TRANSFER IN TREATMENT OF DISEASES
OF THE NERVOUS SYSTEM, Joseph C. Glorioso and David J. Fink
EARLY MOLECULAR INVESTIGATIONS OF LICHEN-FORMING SYMBIONTS:
1986–2001, Paula T. DePriest
THE SMALL RNA REGULATORS OF ESCHERICHIA COLI: ROLES AND
MECHANISMS, Susan Gottesman
JOHNE’S DISEASE, INFLAMMATORY BOWEL DISEASE, AND MYCOBACTERIUM
PARATUBERCULOSIS, Ofelia Chacon, Luiz E. Bermudez, and
Raúl G. Barletta
MOLECULAR AND CELLULAR BASIS OF BARTONELLA PATHOGENESIS,
Christoph Dehio
vi
xii
1
43
75
99
119
143
161
183
207
233
253
273
303
329
365
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CONTENTS
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CELL-MEDIATED IMMUNITY AND THE OUTCOME OF HEPATITIS C VIRUS
INFECTION, Naglaa H. Shoukry, Andrew G. Cawthon, and
Christopher M. Walker
RECENT ADVANCES IN THE CHARACTERIZATION OF AMBIENT PH
REGULATION OF GENE EXPRESSION IN FILAMENTOUS FUNGI AND YEASTS,
Miguel A. Peñalva and Herbert N. Arst, Jr.
BIOSYNTHESIS OF NONRIBOSOMAL PEPTIDES, Robert Finking and
Mohamed A. Marahiel
CIRCADIAN RHYTHMS IN MICROORGANISMS: NEW COMPLEXITIES,
Patricia L. Lakin-Thomas and Stuart Brody
THE CELLULOSOMES: MULTIENZYME MACHINES FOR DEGRADATION
OF PLANT CELL WALL POLYSACCHARIDES, Edward A. Bayer,
Jean-Pierre Belaich, Yuval Shoham, and Raphael Lamed
BIOPHYSICAL ANALYSES OF DESIGNED AND SELECTED MUTANTS OF
PROTOCATECHUATE 3,4-DIOXYGENASE, C. Kent Brown,
Matthew W. Vetting, Cathleen A. Earhart, and Douglas H. Ohlendorf
MOLECULAR DETERMINANTS OF LISTERIA MONOCYTOGENES VIRULENCE,
Olivier Dussurget, Javier Pizarro-Cerda, and Pascale Cossart
BACTERIAL IRON SOURCES: FROM SIDEROPHORES TO HEMOPHORES,
Cécile Wandersman and Philippe Delepelaire
ENDANGERED ANTARCTIC ENVIRONMENTS, Don A. Cowan
and Lemese Ah Tow
INDEXES
Subject Index
Cumulative Index of Contributing Authors, Volumes 54–58
Cumulative Index of Chapter Titles, Volumes 54–58
ERRATA
An online log of corrections to Annual Review of Microbiology chapters
may be found at http://micro.annualreviews.org/
vii
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611
649
691
735
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