Limnol. Oceanogr., 38(2), 1993, 273-279
0 1993, by the American
Society
of Limnology
and Oceanography,
Inc.
Bacterivory in algae: A survival strategy during
nutrient limitation
Kari Nygaard
Norwegian
Institute
for Water Research, P.O. Box 69, Korsvoll,
N-0808 Oslo 8
August Tobiesen
University
Norway
of Oslo, Department
of Biology,
Section of Marine
Botany,
P.O. Box 1069, Blindern,
N-03 16 Oslo 3,
Abstract
Bacterivory in obligate phototrophic algal flagellates may be an important strategy for acquiring nutrients
during periods of inorganic nutrient limitation.
Several marine algal flagellates were shown to increase
bactivory when phosphate was limited. Grazing on bacteria by algal flagellates was found during blooms
of Prymnesium parvum in Sandsljorden, western Norway, in 1989 and Chrysochromulina
polylepis on
the south and west coast of Norway in 1988. Dissolved phosphate was not detectable in these situations.
Algal flagellates may graze bacteria to obtain phosphate, which may permit these algal flagellates to
develop blooms when phosphate becomes limited.
True mixotrophy,
defined as use of particulate organic matter for cellular growth, has
been conclusively demonstrated for only a few
species in the genus Ochromonas (Fenchel
1982) and for Poteiroochromonas malhamensis (Caron et al. 1990). Much more widespread
is the ability to use a restricted range of organic
substances, available at high concentrations,
as a dietary supplement or sole C source in the
dark (Antia 1980).
Mixotrophy in algal flagellates has been considered mainly a strategy for gaining C during
low light (Bird and Kalff 1987; Sanders and
Porter 1988) and therefore has been studied
in algae that use bacteria as their primary C
source. Doddema and Van der Veer ( 198 3)
suggested that phagocytosis might permit utilization of particulate organic N and P when
inorganic nutrients are in limited supply. Obligate phototrophs are the appropriate test organisms to evaluate this hypothesis. Bacteria
have a high P content even when phosphate is
limited (Andersen et al. 1986), although their
P content can be reduced when they are drastically starved (Tezuka 1990). Bacteria are
therefore a potential source of P when obligate
phototrophic
algal flagellates are subjected to
P limitation,
because bacteria are more efficient at sequestering P under these conditions
(Bratbak and Thingstad 198 5).
Blooms of toxic algal flagellates resulting in
fish kills have been a problem in the coastal
waters of Norway for several years. Field studies were undertaken during two of these toxic
prymnesiophyte
events, one dominated by
Chrysochromulina polylepis in 1988 (Borsheim et al. 1989) and one by Prymnesium parvum in 1989 (Johnson and Lein 1989). Both
species are obligate phototrophs. During both
bloom events phosphate was below the detection limit (Dahl et al. 1989). Phosphate limitation was found to increase the toxicity of C.
polylepis (Edvardsen et al. 1990); Manton and
Parke (1962) showed that it can phagocytize
graphite particles. Field studies during the
bloom events demonstrated bacterivory
for
both C. polylepis and P. parvum. A combination of toxin production and P nutrition
through bacterivory might give these algal flagellates a competitive advantage. Consequently, we investigated the potential for such nutrition in several laboratory experiments. All
of the species we tested are believed to be obligate phototrophs, except perhaps Ochromonas minima and Chrysochromulina ericina.
Acknowledgments
This investigation was supported by the Norwegian Research Council for Science and the Humanities.
We acknowledge E. Paasche and T. Kallquist for comments on earlier versions of this paper.
Material and methods
Methods used in both the field and the laboratory experiment-Chlorophyll
a was measured fluorometrically
273
and corrected for pheo-
274
Nygaard and Tobiesen
Table 1. Results from a field study of bacterivorous
algae in 1989 on the west coast of Norway. Bacteria grazed
per algal cell (cells h-l) measured by FLB; total grazing
(ml h-l x 105) measured by RLB.
Depth
(m)
0
1
2
4
Bacteria
grazed by
P. parvum
C. ericina
Total
grazed
5.8
4.6
3.4
0
18.0
12.0
8.0
0.0
2.0
6.3
5.0
4.2
% algal
grazing
to total
gmzing
60
13
11
0
CO.05
SO.05
co.05
0.35
pigments according to Strickland and Parsons
( 1972). Phosphate was measured as soluble reactive P (Strickland and Parsons 1972). Cell P
was measured as particulate P on precombusted Whatman GFK filters according to Solorzano and Sharp (1980). Samples for measurements of particulate C and N were filtered
onto precombusted Whatman GFK filters and
analyzed on a Carlo-Erba CHN+ O/S elemental analyzer (model EA 1106).
Grazing rates were measured by labeling (18
h) bacteria (RLB) (0.06 pm3) from prefiltered
(1.6 pm), aged seawater (stored for l-2 months)
with [‘“Cl amino acid (Amersham CFB 25, 30
VCi final concn) (Nygaard and Hessen 1990).
Algal flagellates from the field, chemostats, and
batch cultures were fed with RLB and incubated for 0, 10, and 20 min. Triplicate samples
were filtered onto 1.0~pm Nuclepore filters.
Samples taken at time zero were subtracted as
background. Background values should not exceed 10% of cpm at time 20 min. Possible
direct uptake by the algae of [‘“Cl amino acid
and [‘“Cl amino acid-labeled metabolites excreted by the bacteria was tested by adding
[‘“Cl amino acid directly to the algae and by
adding 0.2-pm Nuclepore filtrate from the labeled bacteria; no rapid uptake was observed.
Ingestion rate was calculated from
Af
x Bs(sv/tv)
Cb(av/tv)
where I is the number of bacteria ingested per
flagellate per minute, Afthe activity in flagellates (dpm ml-l), Cfthe number of flagellates
ml-l, Ab the activity in bacteria (dpm ml-l),
Cb the number of radiolabeled bacteria ml-l,
Bs the number of bacteria in the sample, tv the
total volume, sv the sample volume, av the
added volume with RLB, and t the minutes of
elapsed grazing (to-tI). For all the present experiments t, = 10 min, except for Gyrodinium
gala,feanum where tl = 20 min.
In some cases, grazing was also measured
with FLB (0.12 pm3) {DTAF-[S-(4,6-dichlorotriazin-2-yl)-amino-fluorescein]-stained
bacteria} (Sherr et al. 1987). Bacteria were added
to samples and enumerated by epifluorescence
microscopy.
Species used in the laboratory experiment Ten species of algal flagellates were tested for
uptake of bacteria: C. polylepis, C. ericina, P.
parvum, 0. minima, Cryptomonas sp., Pavlova
sp., Pseudopedinella sp., Heterosigma akashiwo, G. galateanum, and Alexandrium tama-
rense.
Cultures were from the culture collection of
the Section of Marine Botany, University
of
Oslo. Chrysochromulina spinifera was provided by the culture collection of the Institute of
Marine Biology, Helsingor, Denmark.
The algae were grown in IMR/2 medium
(Eppley et al. 1967) modified to 3% salinity,
2.0 PM phosphate, 1.0 PM Na,SeO,; silicate
was omitted. The nonaxenic algal flagellates
were grown in P-limited single-stage chemostats at 12O”C, in a photoperiod of 12 : 12 L/D
provided by “white” fluorescent tubes giving
a light intensity of 300 PEinst m-2s-1. Batch
cultures were grown at 130 PEinst m-2 s-l
(Biospherical Instr., Inc., model Q 52100).
Che:mostats were run at a dilution rate of 0.3
d-l for 1 month before the experiment.
Batch cultures were kept in logarithmic
growth by frequent dilution. Analyses of reactive P determined that P remained continually available in the batch cultures.
Results
Field results-uptake
of FLB was first recorded during a bloom of C. polylepis in 1988.
Grazing rates measured for C. ericina and P.
parvum during the bloom in 1989 were highest
from 1 to 2 m and dropped to 0 at 4 m (Table
1). High grazing rates coincided with a lack of
‘phosphate down to 4 m (KO.05 PM). Community grazing, measured as total uptake of
radiolabeled bacteria by cells retained on a 1.Opm Nuclepore filter, compared to uptake of
FLB by algal cells, showed that algal bacterivary may contribute up to 60% of total grazing
on bacteria.
275
Bacterivory in algae
Table 2. Amount of orthophosphate present in culture at the start of grazing experiment,
and bacterial uptake by algae in chemostats (C) and batch cultures (B).
Part P
(Pg cell ‘)
Chrysochromulina
polylepis
Chrysochromulina
ericina
Prymnesium
parvum
Ochromonas
minima
Pseudopedinella
sp.
Heterosigma
akashiwo
Gyrodinium
galateanum
Alexandrium
tamarense
C
B
C
B
C
B
C
B
C
B
C
B
C
B
C
B
0.03
0.75
0.03
1.10
0.00
1.29
0.05
0.23
0.15
0.79
0.13
1.56
0.12
0.33
0.70
0.52
Laboratory study-At the onset of the experiments, phosphate was near the detection
limit for the chemostat cultures and in excess
in batch cultures (Table 2). The chemostat cultures were regarded as P limited and the batch
cultures, which were in log phase, were nonlimited. The molar ratio between P and N further established the culture conditions as respectively P limited and nonlimited;
cellular
C : N : P ratios indicate that all the chemostat
cultures, except for A. tamarense, had a lower
level of cellular P compared to batch cultures.
The low cellular C : N : P ratios in A. tamarense with no difference between chemostat
and batch culture, despite a sevenfold increase
in bacterial uptake (Table 2), may be a direct
result of the high uptake of bacteria in this
species. The phagocytized bacteria will, assuming a digesting time of 1 h, constitute -7
pg P per algal flagellate (Table 2, 700 bacteria
x 0.0 1 pg P cell- l) or a fourth of the measured
amount of P in A. tamarense (Table 2).
The algal flagellates grown in chemostats had
a linear uptake of RLB (Fig. 1). Direct uptake
of radiolabeled metabolites was tested by adding 0.2 pm of filtered RLB culture; no uptake
was found. The number of bacteria grazed was
1-57 bacteria (algal cell)-’ h-l for the small
species (0.33-4.48 x 104, specific filtration)
and 20-706 bacteria (algal cell)-’ h-l (0.271.84 x 104, specific filtration) for the larger
species (Table 2). Some of the algal flagellates
grown in batch cultures with excess phosphate
also grazed bacteria, though at a much lower
1.43
1.10
1.26
0.62
0.43
0.59
0.80
2.39
2.55
1.30
7.56
2.58
16.06
5.23
31.48
18.63
C:N:P
(molar)
171:24.6: 1
109: 13.4: 1
259:28.7: 1
205:22.8: 1
168: 18.5: 1
135:9.7: 1
269:30: 1
142: 19.3: 1
275:27.8: 1
131:18.7:1
104:6.7: 1
62 : 5.9 : 1
144:17.1:1
104: 10.1: 1
93:9.1: 1
96:9.2: 1
particulate
P,chlorophyll,
Chl a
(cell - I)
Bacteria
(cell ’ h ‘)
0.55
0.91
0.24
0.48
1.14
1.32
1.34
1.98
2.88
4.56
0.63
0.45
4.85
2.39
5.70
6.04
57.0
6.8
2.2
4.3
4.6
0.7
16.0
1.1
18.0
0
113.0
0
48.0
0
706.0
103.0
rate (Table 2). The exception is C. ericina, with
a higher measured grazing rate in the batch
cultures than in the chemostats.
Bacterivory measured by two d@erent methods-Of the species tested for uptake of bacteria, P. parvum, H. akashiwo, A. tamarense,
Pseudopedinella sp., G. galateanum, and PavNovasp. have not previously been reported to
graze bacteria. Some of the algal flagellate species fed with both RLB and FLB did not take
up FLB (Table 3). These uptake studies were
done in the laboratory during the stationary
phase in P-limited batch cultures. Uptake of
FLB was measured both in the laboratory and
in the field for P. parvum, C. ericina, and C.
polylepis.
Discussion
A possible connection between bacterial uptake in algal flagellates and limited supply of
reactive orthophosphate was observed during
two events of toxic algal blooms. There seemed
to be a close connection between lack of orthophosphate and degree of bacterivory. To
test the hypothesis that algal flagellates might
overcome phosphate deficiency by grazing
bacteria, we grew eight species of algal flagellates, of which six are not known to be able to
grow in absence of light, with (chemostat) and
without (batch) phosphate limitation. The results suggest a close connection between phosphate deficiency and bacterivory by algal flagellates, as we found a higher rate of bacterivory
in P-limited chemostats compared to batch
276
Nygaard and Tobiesen
Chrysochromulina polylepis
cl
10
20
Prymnesium parvum
800
700
600
Chrysochromulha ericina
500
400
3cNl
200
loo
ci
0
10
20
Pseudopedinellasp.
?
Ochromonasminima
14UQ-
I
12cm -.
/
lam -8al -I
/'
/7
r/
/’ /
/”
0
Heterosigma akashiwo
900
800
700
600 /
P
/’
/
10
I
20
Gyrodinium galateanum
7m600 -.
,/I’
0
I
10
20
Alexandrium tamarense
8
500 -.
/"
400 -.
300 -.
loo -.
OH
0
Time (min)
Fig. 1. Uptake rate
grown in chemostat.
ml-l,
@pm
I
10
I
20
Time (min)
filtered onto 1.O-pm filters) ol‘ 14C protein-labeled
cultures. This connection is also strengthened
by bacterivory by algae in field samples (Table
1) correlated with P limitation
(N : P ratio =
64, Kaartvedt et al. 1990). Bacterivory in order
to gain C is unlikely in our study (Table l), as
Time (min)
bacteria by eight species of
the highest ingestion of bacteria by algae was
found in the surface samples and decreased
with depth. Bacterivory by algae in order to
gain C would be expected to increase with depth
and with decreasing light intensity.
Bacterivory in algae
Table 3. Species (phosphate limited) tested for uptake
of bacteria, either with RLB or FLB. Uptake of bacteria
registered, ~5% of algae with bacteria in vacuoles after
1-h incubation, (+); uptake of bacteria not registered, < 5%
of algae with bacteria in vacuoles after l-h incubation,
C-h
Chrysochromulina
polylepis
Chrysochromulina
ericina
Chrysochromulina
spint$ra
Prymnesium parvum
Ochromonas minima
Pseudopedinella sp.
Heterosigma akashiwo
Gyrodinium galateanum
Gyrodinium sp.
Alexandrium
tamarense
Pavlova sp.
Cryptomonas sp.
* Uptake
of FLB registered
during
Uptake of
RLB
Uptake of
FLB
+
+
+
+
+
+
+
+
-*
+
+
+
-
+
f
+
1988 bloom.
Sanders and Porter ( 1988) found clearance
rates in the range 2.5-8.4 nl h- l in Lake Oglethorpe for three chrysophycean algae, using
microspheres. The uptake rates for the first five
species in Table 4 converted into a nanoliters
clearance rate (Table 4) are comparable to the
values found by Sanders and Porter. Cell volume specific filtration
rates (Table 4) (the
chemostat cultures) were highest for 0. minima and C. polylepis and lowest for C. ericina,
P. parvum, and A. tamarense. The filtration
rate for 0. minima is close to that measured
by Fenchel ( 1982) for Ochromonas sp. None
Table 4. Amount
of the earlier studies (Sanders and Porter 1988;
Bird and Kalff 1987) can definitely conclude
that carbon acquisition is the major objective
of bacterial phagotrophy by algae. Caron et al.
(1990) reported that P. malhamensis, an algal
flagellate known to grow heterotrophically,
utilizes C, N, and P from bacteria grazed.
The difference in measured uptake with either RLB or FLB may be due to discrimination
by some algal flagellates against heat-killed
bacteria. Sherr et al. (1990) stated that this is
a minor problem when studying heterotrophs.
Selectivity might be a problem when studying
mixotrophs, as they have lower grazing rates
(Table 4) compared to heterotrophs (Tobiesen
1990) and might be more selective.
We assumed that bacteria contain 0.0 10 pg
P per cell. Table 4 shows the potential amount
of P which the algal flagellates can extract from
engulfed bacteria. Divided by the amount of
P per algal cell in the P-limited algal flagellates
(grown in chemostat), the calculated amount
ingested per day ranges from 0.7 to 9.7 times
the amount required for 0.3 divisions per day.
All the P-limited algal flagellates seem to take
up P in excess of that needed to keep up with
the chemostat growth of 0.3 division d-l. High
uptake rates of P raise the important question:
to what degree are the algal flagellates able to
use the P compounds in the bacteria? Except
possibly Ochromonas and C. ericina, none of
the tested algal flagellates is known to grow in
the absence of light. They are therefore prob-
of phosphate gained by uptake of bacteria by algae in chemostats (C) and batch cultures (B).
Chrysochromulina
polylepis
Chrysochromulina
ericina
Prymnesium
parvum
Ochromonas
minima
Pseudopedinella
277
sp,
Heterosigma
akashiwo
Gyrodinium
galateanum
Alexandrium
tamarense
Culture
No.
bacteria
(X 106)
From
bacteria
(PtzPd
‘1
Potential
growth on
bacterial P
(div d-l)
C
B
C
B
C
B
C
B
C
B
C
B
C
B
C
B
5.47
2.24
3.62
1.60
5.80
1.49
3.09
1.24
3.49
2.57
7.25
1.52
3.62
1.49
4.74
1.41
13.81
1.64
0.53
1.04
1.11
0.17
3.99
0.27
4.49
0.00
27.2 1
0.00
11.53
0.00
169.36
24.73
9.66
1.49
0.42
1.67
2.58
0.28
4.99
0.11
1.76
0.00
3.56
0.00
0.72
0.00
5.38
1.33
Filtered
(nl cell-’
d-‘)
10.52
3.05
0.61
2.71
0.80
0.47
5.37
0.91
5.36
0.00
15.63
0.00
13.30
0.00
148.75
72.97
Vol.
specific
filtration
(X 104)
3.90
1.13
0.31
1.35
0.33
0.20
4.48
0.76
1.48
0.00
1.84
0.00
1.89
0.00
0.55
0.27
278
Nygaard and Tobiesen
ably obligate phototrophs and the number and
amount of digestive enzymes is probably restricted. One would therefore surmise that only
a relatively restricted range of P compounds
is usable by algal flagellates-mainly
those that
occur as constituents of the algal cells or are
closely related to them, such as nucleoside
phosphates, polyphosphates
and others. P
compounds unique to bacteria, such as peptidoglucan, may not be used.
If the algae are able to use bacteria as a P
source, they should have an advantage in situations where PO, is deficient, as was the case
in both the toxic blooms of prymnesiophytes
in 1988 and 1989 (Dahl et al. 1989; Kaartvedt
et al. 1990). Another prymnesiophyte,
Chrysochromulina leadbetteri, was observed on the
northwest coast of Norway in 199 1. This alga
was toxic and dissolved PO, was not found
during the bloom. Phosphate deficiency alone
may be insufficient for the success of bacterivorous algae because their growth requires that
other environmental factors are also favorable.
Bacteria have been shown to out-compete
algal flagellates in phosphate-limited
chemostats at low dilution rates (Currie and Kalff
1984; Bratbak and Thingstad 1985). Shortterm 32P04 uptake experiments showed bacteria to be superior to algae in taking up P
(Currie and Kalff 1984). Often algae seemingly
aggravate their own situation by producing
higher amounts of DOC during P limitation
(Bratbak and Thingstad 1985). Bjornsen (1988)
suggested that increased DOC production is a
constant proportion of cell biomass, irrespective of nutrient status. Our results suggest that
algae able to graze and use P compounds in
the bacteria will have a compensatory mechanism to overcome their competitive disadvantage.
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Submitted: 26 February 1991
Accepted: 15 July 1992
Revised: 27 October 1992