Freshwater Biology (2001) 46, 1279±1287
Viruses in the plankton of freshwater and saline
Antarctic lakes
J O H A N N A L A Y B O U R N - P A R R Y , * J U L I A S . H O F E R ² and R U B E N S O M M A R U G A ²
*Institute of Environmental Sciences, University of Nottingham, University Park, Nottingham, U.K.
²Institute of Zoology and Limnology, University of Innsbruck, Innsbruck, Austria
SUMMARY
3
1. Virus-like particle (VLP) abundances in nine freshwater to saline lakes in the Vestfold
Hills, Eastern Antarctica (68° S) were determined in December 1999. In the ultraoligotrophic to oligotrophic freshwater lakes, VLP abundances ranged from 1.01 to
3.28 ´ 106 mL±1 in the top 6 m of the water column. In the saline lakes the range was
between 6.76 and 36.5 ´ 106 mL±1. The lowest value was found in meromictic Ace Lake
and the highest value in hypersaline Lake Williams. Virus to bacteria ratios (VBR) were
lowest in the freshwater lakes and highest in the saline lakes, with a maximum of 23.4 in
the former and 50.3 in the latter.
2. A range of morphologies among VLP was observed, including phages with short
(Podoviridae) and long tails, icosahedric viruses of up to 300 nm and star-like particles of
about 80 nm diameter.
3. In these microbially dominated ecosystems there was no correlation between VLP and
either bacterial numbers or chlorophyll a. There was a signi®cant correlation between VLP
abundances and dissolved organic carbon concentration (r ˆ 0.845, P < 0.01).
4. The data suggested that viruses probably attack a spectrum of bacteria and protozoan
species. Virus-like particle numbers in the freshwater lakes were lower than values
reported for lower latitude systems. Those in the saline lakes were comparable with
abundances reported from other Antarctic lakes, and were higher than most values
published for lower latitude lakes and many marine systems. Across the salinity spectrum
from freshwater through brackish to hypersaline, VLP concentrations increased roughly in
relation to increasing trophy.
5. Given that Antarctic lakes have a plankton almost entirely made up of bacteria and
protists, and that VLP abundances are high, it is likely that viruses play a pivotal role in
carbon cycling in these extreme ecosystems.
Keywords: Antarctic, heterotrophic bacteria, oligotrophic lakes, microbial loop,
virus-like particles
Introduction
Viruses are now recognized as an important component in the planktonic dynamics of both lakes and the
sea (e.g. Fuhrman & Suttle, 1993; Thingstad et al.,
1993; Steward et al., 1996; Fuhrman, 1999; Wommack
Correspondence: J. Laybourn-Parry, Institute of Environmental
Sciences, University of Nottingham, University Park, Notting2 ham NG7 2RD, U.K. E-mail: [email protected]
Ó 2001 Blackwell Science Ltd
& Colwell, 2000). They attack and lyse bacteria and
phytoplankton, and probably also heterotrophic
¯agellates and other protists, and thereby short-circuit
the microbial loop, reducing the transfer of carbon to
higher trophic levels. In the marine environment, it is
estimated that 10±20% of daily bacterial production is
lysed by viral attack (Suttle, 1994). The pioneering
work on viruses was undertaken in the marine
environment, but recently attention has turned to
lacustrine environments (e.g. Hennes & Simon, 1995;
1279
1280
J. Laybourn-Parry et al.
Maranger & Bird, 1995; Sommaruga et al., 1995; Pina
et al., 1998; Tapper & Hicks, 1998; Weinbauer & Hoȯe,
1998) where viral abundance has been shown to vary
among lakes of different trophic status. Among
Antarctic lakes, only those of the Dry Valleys have
been investigated for the presence of viruses (Kepner
& Wharton, 1998). This work suggested that the
abundances of viruses in Lakes Hoare and Fryxell and
other Dry Valley lakes were higher than most values
reported for freshwater and marine systems, and were
similar to those found in mesotrophic and more
productive nearshore marine systems. It therefore
appears that viral dynamics in Antarctic lakes may
differ from those in lower latitude lakes and that
carbon cycling in Antarctic lakes may have a signi®cant viral-mediated component. Antarctic lakes are
microbially dominated systems (Laybourn-Parry,
1997). They lack ®sh and have few or no zooplankton.
As ecosystems in which micro-organisms (bacteria,
protists and algae) are virtually the only component,
they offer unique models for the study of the role and
impact of viruses.
The Vestfold Hills at 68°S in eastern Antarctica are
ideally suited for a study of this type. This coastal
oasis contains more than 300 lakes and ponds of
remarkable diversity. The lakes range from large and
deep freshwater ultra-oligotrophic systems such as
Crooked Lake (Laybourn-Parry et al., 1995) to smaller
oligotrophic freshwater lakes, brackish lakes, saline
meromictic lakes and hypersaline monomictic lakes
(e.g. Burch, 1988; Laybourn-Parry & Perriss, 1995;
Perriss et al., 1995; Bell & Laybourn-Parry, 1999).
The majority of these lakes were formed by isostatic
uplift which trapped pockets of seawater in hollows
or cut ®ords off from the sea (Adamson & Pickard,
1986). Some of these systems were ¯ushed by glacial
meltwater and ultimately became freshwater, while
the closed basins became saline lakes of varying
salinity, some of which have undergone meromixis.
Some of the freshwater lakes close to the Antarctic ice
cap, such as Lake Nottingham, have developed as the
ice has retreated. The saline lakes contain truncated
microbial communities of marine-derived species
(Burch, 1988; Perriss & Laybourn-Parry, 1997; Bell &
Laybourn-Parry, 1999). For example, the ubiquitous,
marine autotrophic ciliate Mesodinium rubrum is common in all but the most saline lakes (Perriss &
Laybourn-Parry, 1997) and Pyraminonas gelidicola is
common in a number of the lakes (Burch, 1988; Perriss
& Laybourn-Parry, 1997; Bell & Laybourn-Parry,
1999). The bacteria of the saline lakes are mainly of
marine origin (Franzmann & Dobson, 1993), and
where new species have evolved they are closely
4 related to marine species (S. Mills, J. Laybourn-Parry,
P. Hill et al., unpublished data).
The current investigation was undertaken as part of
a large scale programme aimed at characterizing
carbon cycling in some of the Vestfold Hills lakes, to
ascertain whether viruses play an important role in
microbial dynamics.
Methods
Study sites
Five freshwater lakes ranging from a large deep
ultra-oligotrophic lake (Crooked Lake) to a shallow
system (Lake Druzhby) were investigated in December
1999 (Table 1). Four brackish to hypersaline lakes
were also investigated (Table 1). Lake Williams had
Lake
Approx max
depth (m)
Approx
area (km2)
Salinity
(%)
Coordinates
Crooked
Druzhby
Nottingham
Lichen
Caroline
Ace
Highway
Pendent
Williams
160
40
18
16
10
20
10?
15
6
9
4
0.22
0.25
0.25
0.16
0.20
0.16
0.20
Freshwater
Freshwater
Freshwater
Freshwater
Freshwater
18*
4
15
56
68°37¢ S, 78°22¢ E
68°35¢ S, 78°20¢ E
68°27¢40¢ S, 78°29¢
68°29¢ S, 78°28¢ E
68°28¢30¢ S, 78°29¢
68°28¢45¢ S, 78°11¢
68°14¢ S, 78°28¢10¢
68°29¢ S, 78°15¢ E
68°29¢20¢ S, 78°10¢
Table 1 Characteristics of the lakes
sampled
E
E
E
E
E
*Ace Lake is meromictic, salinity value given applies to upper water (mixolimnion)
sampled.
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1
Viruses in plankton of freshwater and saline Antarctic lakes
1281
randomly selected until total numbers exceeded 200,
anoxic water below 4 m at the time of sampling.
or in case of low density, until 200 ®elds were
Ace Lake is a meromictic lake with a deep anoxic
examined, using a Zeiss (CEM 902, Carl Zeiss,
monimolimnion having a salinity close to seawater,
12
Welwyn Garden City, U.K.) transmission electron
and upper oxygenated waters (mixolimnion) with a
microscope at 80 kV and 85 000´ magni®cation. Taper
salinity half that of seawater. Pendent Lake had
corrections were implemented into ®nal calculations
largely oxygenated waters and only became anoxic
(Suttle, 1993).
in the limited deeper waters at its northern end.
For the enumeration of bacteria, 10±15 mL of glutHighway Lake showed no signs of strati®cation at the
aradehyde-®xed material were stained with DAPI
time of sampling. All the lakes were ice-covered in
December with Lake Williams having the thinnest ice 13 (4,6-diamidino-2-phenylindole, Sigma, Poole, U.K.)
and ®ltered through 0.2 lm black polycarbonate
(1.7 m) and Lake Nottingham the deepest ice-cover
®lters. Bacteria were counted under epi¯uorescence
(3 m). Water samples were taken with a Kemmerer
5 water sampler through holes drilled in the ice-covers
microscopy (´1200) using UV excitation. Two replicate
6 with a Jiffy Drill (Feldman Engineering, Sheboygan
preparations were counted for each sample. A further
15±30 mL of glutaradehyde-®xed material were
Falls, WI, U.S.A.).
stained with DAPI, ®ltered through 1 lm polycarbonate ®lters and NANF counted under epi¯uorescence
Sampling
microscopy using both the UV and blue ®lters. Samples for DOC analysis were ®ltered through pre-ashed
Integrated samples from 0, 2, 4 and 6 m were taken
GF/F ®lters and analysed in a Shimadzu 5000 TOC
for the analysis of virus-like particles (VLP). These
samples were ®xed in buffered glutaradehyde to a 14 analyser (Shimadzu Europa, Milton Keynes, U.K.).
Freshwater lake samples were analysed with a high
®nal concentration of 4%. The samples were dissensitivity catalyst. Chlorophyll a samples were ®lpatched to the University of Innsbruck for analysis
tered through GF/C Whatman ®lters, extracted in
within 2 months of collection. Samples from each
methanol over a 24-h period at ±20 °C and the extract
individual depth were ®xed in glutaradehyde for the
enumeration of bacteria and nano¯agellates (NANF). 15 assayed spectrophotometrically (after Talling, 1969).
Inorganic nutrients were determined colorimetrically
Two to four litres of water (depending on the lake)
on GF/F ®ltered samples using the methods of
were taken for chlorophyll a analysis. Further samples were collected in acid washed bottles for 16 Mackereth et al. (1978).
inorganic nutrients [nitrate, ammonium and soluble
reactive phosphorus (SRP)] and dissolved organic
Results
carbon (DOC).
Virus-like particles ranged from 1.01 to 3.28 ´ 106 mL)1
in the freshwater lakes and between 6.76 and
Analysis of samples
36.5 ´ 106 mL±1 in the saline lakes (Fig. 1). The morVirus-like particles were enumerated by transmission
phology of the VLP included phages with short
electron microscopy according to Bergh et al. (1989).
(Podoviridae) and long tails (Fig. 2a, c), and icosaheBrie¯y, 6±60 mL of ®xed lake water were harvested
dric viruses without a tail of up to about 300 nm
directly onto electron microscope grids (400-mesh Cu
(Fig. 2b, e). Star-like particles of approximately 80 nm
grids) supported with a carbon-coated Formvar ®lm
diameter (Fig. 2d) were observed in Lake Druzhby,
(Plano, Marburg, Germany), using a Sorvall OTD-2
but they were not included in the counting of VLP.
ultracentrifuge (Du Pont, Newtown, CT, U.S.A.)
Among the freshwater lakes, Crooked Lake and Lake
8,9 (50 000 g or 20 000 r.p.m. for 6 h) with a swing-out
Caroline had the lowest concentrations. Lake Druzhby
10 rotor (AH627, Du Pont, Newtown, CT, U.S.A.). After
differed signi®cantly, with higher concentrations than
the removal of the supernatant, the grids were stained
the other freshwater lakes. This lake is unusual in
with 2% uranyl acetate for 30 s and then rinsed three
being composed of a number of shallow basins and
times with distilled water (®ltered through a 0.02-lm
one deeper basin, and having a phytoplankton dom®lter Anodisc, Whatman International, Maidstone,
inated by a monoculture of a small sausage-shaped,
11 U.K.). Virus-like particles were counted in view ®elds
mucus-invested cyanobacterial species. Among the
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1282
J. Laybourn-Parry et al.
The ratios of VLP to bacteria were highest in the
more productive saline lakes (Table 2), and relatively
low in the freshwater lakes, with the exception of Lake
Druzhby. There were also higher ratios of VLP to
NANF in the saline lakes. The exception was Pendent
Lake, which at the time of sampling was dominated
by a bloom of a small chlorophyte. Lake Druzhby had
a higher ratio of VLP to NANF than the other
freshwater lakes. Among the freshwater lakes studied,
Lake Druzhby was atypical not only in its unusual
morphometry but also in its biota.
There was no signi®cant correlation between VLP
and chlorophyll a concentrations or between bacteria
and VLP in the lakes, but there was a correlation
between VLP and DOC concentrations (Fig. 4).
Fig. 1 Virus-like particle abundance in freshwater and saline
lakes (error bars ˆ ‹ 1 SD). Crooked, Caroline, Lichen, Nottingham and Druzhby are freshwater, Ace, Highway, Pendent
and Williams are saline.
saline lakes, Ace Lake had the lowest concentration of
VLP, and this value pertained to the upper oxygenated mixolimnion. The other saline lakes showed an
increase along the salinity gradient from brackish
(Highway Lake) to hypersaline (Lake Williams). The
meromictic lake should be viewed as a separate type of
saline lake, because permanent chemical strati®cation
confers rather different organic carbon and inorganic
nutrient dynamics than those encountered in the other
saline lakes in this study. This is re¯ected, for
example, in the chlorophyll a values (Table 2).
All of the freshwater lakes can be classi®ed as ultraoligotrophic to oligotrophic on the basis of inorganic
nutrients, DOC concentrations and chlorophyll a concentrations (Table 2), whereas the saline lakes, excluding Ace Lake, can be regarded as mesotrophic. The
abundances of potential host organisms for viruses
(bacteria, phototrophic and heterotrophic NANF and
algal species) varied considerably across the spectrum
of lakes investigated (Fig. 3a,b). Most of the phytoplankton in these lakes is made up of phototrophic
NANF. In the saline lakes there were also signi®cant
populations of autotrophic and heterotrophic dino¯agellates. In Lake Williams, dino¯agellate abundances
averaged 90 000 L±1 in the 0±6 m section of the water
column, in Pendent Lake 6300 L±1 and in Highway
Lake 1500 L±1. Abundances in Ace Lake were low at
the time of sampling (26 L±1).
Discussion
Virus-like particle abundances in the saline lakes of
the Vestfold Hills were comparable with those found
in the lakes of the McMurdo Dry Valleys (Kepner &
Wharton, 1998) (Table 3). Meromictic Lake Fryxell
with a mixolimnion salinity of up to 7.5& (Roberts
et al., 2000), had the highest VLP abundance
(33.5 ´ 106 mL±1) (Kepner & Wharton, 1998), while
Lake Hoare, which lies on the other side of the
Canada Glacier in the Taylor Valley, had a mean VLP
concentration of 10.9 ´ 106 mL±1. Lake Hoare is a
freshwater lake and has not undergone meromixis.
Another lake studied by Kepner & Wharton (1998)
was Lake Bonney, which in common with Lake
Fryxell is meromictic, but much less productive with
lower chlorophyll a concentrations, abundances of
bacteria, NANF and ciliates (Roberts, 1999). Virus
abundance in Lake Bonney was similar to that in Lake
Hoare (Table 3). Like the lakes of the Vestfold Hills,
the lakes of the Dry Valleys are dominated by a
microbial plankton, the only metazoans being small
numbers of rotifers (James et al., 1998). However, the
lakes of the Dry Valleys possess a more complex
microbial plankton which is probably related to their
greater age. Compared with the Antarctic marine
environment and the Arctic, Antarctic saline lakes had
higher VLP and virus to bacterial ratio (VBR) (see
Table 3).
The freshwater lakes of the Vestfold Hills had
signi®cantly lower VLP abundances than the saline
lakes in both the Vestfold Hills and Dry Valleys
(Table 3). Maranger & Bird (1995) reported a range of
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1
Viruses in plankton of freshwater and saline Antarctic lakes
1283
Fig. 2 Different phages and virus-like
particles. (a) Phage from Highway Lake
and scales from the phyto¯agellate
Pyramimonas gelidicola (the square scales
are box scales from the cell body and the
others are limulus scales from the ¯agella),
(b) icosahedric VLPs from Pendent Lake
(the scales are from a prasinophyte),
(c) phage (Podoviridae) from Lichen Lake,
(d) star-like particles from Lake Druzhby
and (e) large icosahedric VLP and one
bacterium from Lake Nottingham. The
bars in all TEM micrographs represent
100 nm.
VLP abundance for 22 lakes in Quebec, Canada, of
4.1 ´ 107 mL±1 to 1.1 ´ 108 mL±1. These values are an
order of magnitude higher than those presented here
(Table 3). However, the freshwater lakes of the Vest-
fold Hills can all be classi®ed as ultra-oligotrophic on
the basis of chlorophyll a concentrations and
inorganic nutrients (see Table 2). Correspondingly,
our data are closer to those reported for other
Table 2 VLP : Bacteria ratios, VLP : NANF ratios, mean inorganic nutrient concentrations, mean DOC concentrations and
mean chlorophyll a concentrations in the 0±6 m water columns of the lakes studied. ND ± Not detectable
Lake
VLP : bacteria
ratio
VLP : NANF
ratio
Nitrate
(lg L)1)
Ammonium
(lg L)1)
SRP
(lg L)1)
DOC
(mg L)1)
Chlorophyll a
(lg L)1)
Crooked
Druzhby
Nottingham
Lichen
Caroline
Ace
Highway
Pendent
Williams
8.41
23.42
0.15
3.53
1.43
40.23
50.33
28.29
9.17
4208
13 120
1364
5408
3164
7396
7719
300
27 862
36.0
3.7
72.1
55.0
83.1
60.2
98.0
97.2
121.0
9.2
8.7
2.1
1.9
2.4
1.9
2.3
3.7
93.0
ND
ND
5.0
5.2
4.0
52.0
9.1
44.2
961.0
0.88
1.99
0.80
1.39
1.79
6.20
8.21
4.72
30.72
0.35
0.17
0.39
0.93
0.17
0.63
12.61
21.62
4.6
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1284
J. Laybourn-Parry et al.
Fig. 4 Virus-like particle abundance versus DOC in freshwater
and saline lakes. r ˆ 0.845.
Fig. 3 (a) Nano¯agellate (heterotrophic and photosynthetic
combined) in freshwater and saline lakes and (b) Heterotrophic
bacteria in freshwater and saline lakes. Error bars indicate ‹ 1
SD.
oligotrophic cold-water (Pina et al., 1998) and warmwater lakes (Tapper & Hicks, 1998). Our results
extend the range of data on freshwater lakes worldwide, and demonstrate that viruses occupy a position
in the microbial dynamics of freshwater lakes, even in
the most extreme environments.
Information about viral abundance in saline lakes is
scarce. In a study of viral distribution in saltern ponds
17 (Guixa-Boixereu et al., 1996), the abundance of VLP in
the ponds with salinity of 37.5 and 64& was similar to
Lake Williams (56&). This is surprising, considering
that the abundance of prokaryotic cells was one order
of magnitude lower in Lake Williams than in those
saltern ponds (106 and 107 cell mL±1, respectively).
In terms of VBR, the freshwater lakes of the Vestfold
Hills possessed ratios similar to the lower and upper
ranges reported by Maranger & Bird (1995) for freshwater systems. These high VBR values support the
supposition made by Kepner & Wharton (1998) that
viruses may be particularly important in microbial
plankton dynamics and carbon cycling in Antarctic
lacustrine ecosystems. The same may be true of the
sea-ice zone in the Southern Ocean where VBR values
sometimes reached 40 (H.J. Marchant, A. Davidson,
S. Wright & J. Glazebrook, unpublished data) (see
Table 3). However, elevated VBR values may indicate
either a high infection rate or a long persistence of
viruses in the plankton. Consequently, the degree of
bacterial mortality caused by viral lysis needs to be
studied in these systems. A recent assessment of the
role of viruses in aquatic systems suggests that viral
lysis is not the main factor controlling prokaryotic
mortality (PedroÂs-Alio et al., 2000).
We found no correlation between VLP concentrations and chlorophyll a, bacterial abundances or
inorganic nutrients, unlike Maranger & Bird (1995).
We did ®nd a correlation between viral abundance
and DOC concentrations (Fig. 4). The lakes of the
Vestfold Hills usually receive no allochthonous carbon inputs. Only those lakes adjacent to penguin
rookeries or seal wallows are subject to exogenous
carbon and inorganic nutrient loading, and none of
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1
Viruses in plankton of freshwater and saline Antarctic lakes
1285
Table 3 A comparison of viral abundances and virus to bacteria ratios (VBR) in Antarctic lakes and in polar marine and
temperate lake systems
Location
Lake Hoare (75° S)
Lake Fryxell (meromictic) (75° S)
East lobe Lake Bonney (meromictic) (75° S)
Freshwater lakes Vestfold Hills
Saline lakes Vestfold Hills
Ace Lake (meromictic)
Southern Ocean
Southern Ocean Sea ice zone
Bering & Chukchi Seas
Twenty-two freshwater lakes in Quebec
21 Danube backwater system
Virus abundance
(´106 mL)1)
VBR
Source
10.9
33.5
10.0
1.01±3.28
7.55±36.5
6.76
< 0.1±0.65
4.6
1.7±141.1
1.9±120.6
1.5±5.5
1.4±23.4
9.2±50.3
40.2
2±15
15±40
1.0±10.0
41±110
12.0±61.0
±
4.9±25
2.0±17.0
Kepner & Wharton (1998)
Kepner & Wharton (1998)
Kepner & Wharton (1998)
This study
This Study
This study
Glazebrook (unpublished data)
H.J. Marchant, A. Davidson, S. Wright
& J. Glazebrook (unpublished data)
Steward et al. (1996)
Maranger & Bird (1995)
Matthias et al. (1995)
the lakes in the current study belonged to this 18 heterotrophic bacteria (e.g. Van Etten et al., 1991;
Fuhrman & Suttle, 1993; Garza & Suttle, 1995); consecategory. Thus all the DOC available to the bacterioquently unravelling the role of viruses in the dynamics
plankton in the Vestfold Hills lakes was originally
of the microbial loop will not be an easy task. Systems
derived from carbon ®xation by the phytoplankton.
like those of Antarctica offer us ideal, simpli®ed
The low concentrations of DOC in the freshwater
microbial planktonic food webs in which to attempt
lakes (Table 2) suggest that bacterial production is
it. Moreover the saline lakes in the Vestfold Hills are
limited not only by low temperatures, but by the
analogues for the marine environment, because they
availability of a biologically labile carbon source and
have a plankton of marine derived species.
inorganic nutrients.
Previous studies on Crooked Lake and Lake Druzhby have shown that bacterial production is low and
Acknowledgments
that the bacterioplankton is in a permanent state of
This work was funded by a Leverhulme Fellowship and
physiological stress (Laybourn-Parry et al., 1995;
an Australian Antarctic Science Advisory Committee
J. Laybourn-Parry, unpublished data). Even in this
(ASAC) grant to Johanna Laybourn-Parry. We wish to
state the bacteria must be subject to viral attack
acknowledge analytical assistance from Dr Wendy
(Schrader et al., 1997). In Crooked Lake, grazing by
Quayle and Tracey Henshaw and ®eld assistance from
heterotrophic and mixotrophic ¯agellates accounted
the various colleagues at Davis Station, Antarctica.
for 0.1±9.7% of bacterial production per day (Laybourn-Parry et al., 1995). If one assumes comparable
viral mortality, up to 20% of daily bacterial producReferences
tion is likely to be lost to viral attack and grazing.
Adamson D.D. & Pickard J. (1986) Cainozoic history of
There is evidence that grazing and viral lysis may be
the Vestfold Hills. In: Antarctic Oasis (Ed. J. Pickard),
comparable in their impact on bacterial mortality. For
pp. 63±97. Academic Press, Sydney.
example, in a strati®ed, eutrophic German lake,
Bell
E.M. & Laybourn-Parry J. (1999) Annual plankton
bacterial production was controlled by both grazing
dynamics in an Antarctic saline lake. Freshwater
and viral lysis, although viral lysis was much greater
Biology, 41, 565±572.
in the anoxic hypolimnion (Weinbauer & Hoȯe, 1998).
Bergh é., Bùrsheim K.Y., Bratbak G. & Heldal M. (1989)
In a coastal marine environment, the impact of
High abundances of viruses found in aquatic environgrazing and viral lysis were approximately equal
ments. Nature, 340, 467±468.
(Fuhrman & Noble, 1995).
Burch M.D. (1988) Annual cycle of phytoplankton in Ace
The largely microbial plankton of Antarctic lakes is
Lake, an ice-covered, saline meromictic lake. Hydrobicharacterized by low species diversity. Viruses are
ologia, 165, 13±23.
known to attack protists and cyanobacteria as well as
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1286
J. Laybourn-Parry et al.
of the Danube River. Applied and Environmental MicroFranzmann P.D. & Dobson S.J. (1993) The phylogeny of
biology, 61, 3734±3740.
bacteria from a modern Antarctic refuge. Antarctic
PedroÂs-Alio C., CalderoÂn-Paz J.I. & Gasol J.M. (2000)
Science, 5, 267±270.
Comparative analysis shows that bacterivory, not viral
Fuhrman J.A. (1999) Marine viruses and their biogeolysis, controls the abundance of heterotrophic prochemical and ecological effects. Nature, 399, 541±548.
karyotic plankton. FEMS Microbiology and Ecology, 32,
Fuhrman J.A. & Noble R.T. (1995) Viruses and protists
157±165.
cause similar mortality in coastal seawater. Limnology
Perriss S.J. & Laybourn-Parry J. (1997) Microbial comand Oceanography, 40, 1236±1242.
munities in the saline lakes of the Vestfold Hills
Fuhrman J.A. & Suttle C.A. (1993) Viruses in marine
(eastern Antarctica). Polar Biology, 18, 135±144.
planktonic systems. Oceanography, 6, 50±62.
Perriss S.J., Laybourn-Parry J. & Marchant H.J. (1995) The
Garza D.R. & Suttle C.A. (1995) Large double-stranded
widespread occurrence of the autotrophic ciliate
DNA viruses which cause the lysis of a marine
Mesodinium rubrum in the freshwater and brackish
heterotrophic nano¯agellate (Bodo sp.) occur in natural
lakes of the Vestfold Hills, Eastern Antarctica. Polar
marine viral communities. Aquatic Microbial Ecology, 9,
Biology, 15, 428±432.
203±210.
Pina S., Creus A., GonzaÂlez N., GironeÂs R., Felip M. &
Guixa-Boixereu N., CalderoÂn-Paz J.I., Heldal M., Bratbak
Sommaruga R. (1998) Abundance, morphology and
G. & PedroÂs-Alio C. (1996) Viral lysis and bacterivory
distribution of planktonic virus like particles in two
as prokaryote loss factors along a salinity gradient.
high mountain lakes. Journal of Plankton Research, 20,
Aquatic Microbial Ecology, 11, 215±227.
2413±2421.
Hennes K.P. & Simon M. (1995) Signi®cance of bacterioRoberts E.C. (1999) Protozoan Participation in Plankton
phages for controlling bacterioplankton growth in a
Carbon Cycling in the McMurdo Dry Valley Lakes,
mesotrophic lake. Applied and Environmental MicrobioAntarctica. PhD Thesis, University of Nottingham,
logy, 61, 333±340.
Nottingham.
James M.R., Hall J.A. & Laybourn-Parry J. (1998)
Roberts E.C., Laybourn-Parry J., McKnignt D.M. &
Protozooplankton of the dry valley lakes of Southern
Novarino G. (2000) Strati®cation and dynamics of
Victoria Land. In: Ecosystem Dynamics in a Polar Desert.
microbial loop communities in Lake Fryxell, AntarcAntarctic Research Series (Ed. J.C. Priscu), Vol. 72, pp. 255±
19 268. American Geophysical Union, Washington, DC.
tica. Freshwater Biology, 44, 649±661.
Schrader H.S., Schrader J.O., Walker J.J., Wolf T.A.,
Kepner R.L. & Wharton R.A. (1998) Viruses in Antarctic
Nickerson K.W. & Kokjohn T.A. (1997) Bacteriophage
lakes. Limnology and Oceanography, 43, 1754±1761.
infection and multiplication occur in Pseudomonas
Laybourn-Parry J. (1997) The microbial loop in Antarctic
aeruginosa starved for 5 years. Canadian Journal of
lakes. In: Ecosystem Processes in Antarctic Ice-Free
Microbiology, 43, 1157±1163.
Landscapes (Eds C. Howard-Williams, W.B. Lyons &
Sommaruga R., KoÈssbacher M., Salvenmoser W., Catalan
I. Hawes), pp. 231±240. Balkema/Rotterdam/BrookJ. & Psenner R. (1995) Presence of large virus-like
®eld, Rotterdam.
particles in a eutrophic reservoir. Aquatic Microbial
Laybourn-Parry J., Bayliss P. & Ellis-Evans J.C. (1995)
Ecology, 9, 305±308.
The dynamics of heterotrophic nano¯agellates and
Steward G.F., Smith D.C. & Azam F. (1996) Abundance
bacterioplankton in a large ultra-oligotrophic Antarctic
and production of bacteria and viruses in the Bering
lake. Journal of Plankton Research, 17, 1834±1850.
and Chikchi Seas. Marine Ecology Progress Series, 131,
Laybourn-Parry J. & Perriss S.J. (1995) The role and
287±300.
distribution of the autotrophic ciliate Mesodinium
Suttle C.A. (1993) Enumeration and isolation of viruses.
rubrum (Ciliophora: Haptorida) in the brackish lakes
In: Handbook of Methods in Aquatic Microbial Ecology
of the Vestfold Hills, Eastern Antarctica. Archiv fuÈr
(Eds P.F. Kemp, B.F. Sherr, E.B. Sherr & M.J.J. Cole),
Hydrobiologie, 135, 179±194.
pp. 121±134. Lewis Publisher, Boca Raton, FL.
Mackereth H.H., Heron J. & Talling J.F. (1978) Water
Suttle C.A. (1994) The signi®cance of viruses to mortality
Analysis. Freshwater Biological Association Publicain aquatic microbial communities. Microbial Ecology,
tions No. 36, Ambleside.
28, 237±243.
Maranger R. & Bird D.F. (1995) Viral abundance in aquatic
Talling J.F. (1969) General outline of spectrophotometric
systems: a comparison between marine and freshwamethods. In: A Manual for Measuring Primary Production
ters. Marine Ecology Progress Series, 121, 217±226.
in Aquatic Environments. IBP Handbook 12 (Ed. R.A.
Matthias C.B., Kirschner A.K.T. & Velimirov B. (1995)
Vollenweider), pp. 22±24. Blackwell Scienti®c PublicaSeasonal variations of virus abundance and viral
control of bacterial production in a backwater system 20 tions, Oxford.
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1
Viruses in plankton of freshwater and saline Antarctic lakes
Tapper M.A. & Hicks R.E. (1998) Temperate viruses and
lysogeny in Lake Superior bacterioplankton. Limnology
and Oceanography, 43, 95±103.
Thingstad T.F., Heldal M., Bratbak G. & Dundas I. (1993)
Are viruses important partners in microbial food
webs? Trends in Evolution and Ecology, 8, 209±212.
Van Etten J.L., Lane L.C. & Meints R.H. (1991) Viruses
and virus-like particles of eukaryotic algae. Microbiological Reviews, 55, 586±620.
Ó 2001 Blackwell Science Ltd, Freshwater Biology, 46, 1279±1287
1287
Weinbauer M.G. & Hoȯe M.G. (1998) Signi®cance of viral
lysis and ¯agellate grazing as factors controlling
bacterioplankton production in a eutrophic lake.
Applied and Environmental Microbiology, 64, 431±438.
Wommack E.K. & Colwell R.R. (2000) Virioplankton:
viruses in aquatic ecosytems. Microbiology and Molecular Biology Reviews, 64, 69±114.
(Manuscript accepted 13 December 2000)