FEMS Microbiology Ecology 29 (1999) 13^22

Contribution of bacteria in the mucilage of Microcystis spp.

(Cyanobacteria) to benthic and pelagic bacterial production

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in a hypereutrophic lake
Anna-Kristina Brunberg *
Institute of Limnology, Uppsala University, Norbyvaëgen 20, S-752 36 Uppsala, Sweden

Received 6 September 1998; received in revised form 8 December 1998 ; accepted 11 December 1998

Abstract

The mucilage of cyanobacteria represents a unique habitat for both water column and sediment bacteria. In Lake
Vallentunasjoën, Sweden, the pelagic Microcystis-associated bacteria constituted 19^40% of the total bacterial abundance, and
their contribution to the total bacterial production was 7^30%. In the sediment, the mucilage bacteria constituted only 1^5% of
the total bacterial abundance, but contributed with 8^13% to the total bacterial production during the summer. Microcystis-
associated bacteria thus were less active (bacterial production/cell) than ambient water column bacteria, while in the sediments
the Microcystis colonies were `hot spots' with enhanced bacterial activity as compared to other sediment bacteria. z 1999
Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.

Keywords : Microcystis ; Attached bacteria; Bacterial production; Microhabitat

1. Introduction to particles also has certain risks as an adaptive

The attachment of bacteria to particles is an im-
portant process in aquatic ecosystems. Bacteria may
attach, either loosely or more permanently, to vari-
ous types of suspended particles ranging in size from
submicrometer colloids [1], algae and faecal pellets
[2], to the large aggregates that ecologists term ma-
rine or lake `snow' [3,4]. Attachment is normally
considered adaptive, e.g. by enhancing uptake of or-
ganic compounds and nutrients [5] or providing a
refuge from grazing [6], but since almost any particle
will be of a size suitable for some grazer, attachment
* Tel.: +46 (18) 182727; Fax: +46 (18) 531134;
E-mail anna.brunberg@limno.uu.se
strategy for survival [7,8]. Whether attachment to
particles is advantageous in a given environment de-
pends primarily on the types of particles available
for colonisation.
Normally, healthy phytoplankton are not colon-
ised by bacteria, but there are exceptions, especially
among the cyanobacteria, where attachment of bac-
teria to heterocytes is a well-known example [9]. Mi-
crocystis spp., common non-heterocytic colonial cy-
anobacteria in eutrophic lakes, are commonly found
with numerous bacteria embedded in the mucilage
[9,10]. Mucilage bacteria in old, moribund colonies
probably bene¢t from using substrate and nutrients
from decaying Microcystis cells, but the bacteria col-
onising young and healthy colonies may not neces-

0168-6496 / 99 / $20.00 ß 1999 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 6 4 9 6 ( 9 8 ) 0 0 1 2 6 - 3

FEMSEC 1010 21-4-99

14 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22
sarily be harmful to the host. Even symbiotic inter-
actions may occur that favour the Microcystis cells,
e.g. by supplying nutrients [11].
In contrast to the situation in lake water, bacteria
in sediments have numerous particles in their envi-
ronment, and a large part of the bacteria are more or
less tightly associated with these. Studies of bacteria
associated to various types of sediment particles
have, to my knowledge, not been performed. Re-
search is usually focused on di¡erent bacterial proc-
esses carried out by functional groups of bacteria
(e.g. denitri¢cation, sulphate reduction, methanogen-
esis), and their relative contribution to the degrada-
tion of organic material in sediments of various com-
position. For example, e¡ects of bioturbation and
sedimentation on microbial processes are frequently
examined [12,13].
Investigations in Lake Vallentunasjoën, Sweden,
have shown that living Microcystis colonies in the
sediment are a signi¢cant part of the benthic micro-
bial biomass, and a coupling has been shown be-
tween Microcystis biomass and bacterial production
in the sediment [14]. The purpose of this study was
to assess the production of bacteria embedded in the
mucilage of Microcystis colonies and to compare this
with the production of other bacteria in the sediment
and in the water column. In most studies of attached
and free-living bacteria, the separation has been
made with ¢ltration techniques. The partitioning of
particles into size-classes is never perfect [8] and it is
not possible to separate di¡erent types of particles
within the same size fraction. By removing individual
Microcystis colonies from the water column and
sediments, I was able to study an important category
of attached bacteria in Lake Vallentunasjoën.
2. Materials and methods
2.1. Lake description and sampling methods
Lake Vallentunasjoën is a shallow (mean depth 2.7
m), hypereutrophic lake near Stockholm, Sweden.
Until 1970, the lake was polluted by municipal sew-
age water during a period of 20 years, and substan-
tial cyanobacterial blooms still occur in late summer
yearly, frequently dominated by various Microcystis
species (mainly M. wesenbergii and M. viridis). For a
FEMSEC 1010 21-4-99
detailed lake description, see Brunberg and Bostroëm
[14]. The present study was conducted from June
1989 to May 1990. During this period, the surface
sediment was sampled on ¢ve occasions, using a
Willner core sampler. The sediment cores were sub-
sequently sectioned at the lake (0^1 cm layer used in
this study). The water column was studied on three
dates, including a diurnal study on 2 August. Water
samples were taken from the 0^2-m layer of the lake,
using a tube sampler.
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2.2. Abundance of bacteria and cyanobacteria
Samples for determination of microbial abundance
were preserved with 4% (v/v) formaldehyde. Cell
numbers of Microcystis (cyanobacterial cells s 3
Wm in diameter) were determined from auto£uores-
cence with £uorescence microscopy, after sonication
and ¢ltration onto 0.2 Wm polycarbonate ¢lters. Bac-
terial abundance was determined after sonication,
staining with acridine orange, ¢ltration on 0.2-Wm
polycarbonate ¢lters prestained with Sudan black
and counting of cells using £uorescence microscope.
Subtraction of auto£uorescing cells (small cyanobac-
teria, 6 2 Wm in diameter, counted with the same
technique as the larger cyanobacteria) from total
bacterial counts was made in the appropriate bacte-
rial cell size classes. To determine the colony size of
the Microcystis colonies and the number of attached
bacteria, 100 individual Microcystis colonies were
removed from the samples, sonicated, and the Micro-
cystis cells were counted using the Utermoëhl techni-
que with Lugol's solution and an inverted micro-
scope. The bacteria attached to these colonies were
enumerated using epi£uorescence microscope as de-
scribed above for the total bacterial counts. For a
detailed description of the abundance determina-
tions, see Brunberg and Bostroëm [14].
2.3. Bacterial production
All incubations were started within an hour after
sampling. Water samples (15 ml) were incubated in
20-ml glass scintillation vials with 30 nM [methyl-
3
H]thymidine for 2 h in situ, then formaldehyde
was added to a ¢nal concentration of 2% (v/v).
The ¢xed samples were transported to the laboratory
and 5-ml subsamples from three parallels and one
 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22
blank were extracted in 0.6 N NaOH containing
0.1% (w/v) SDS and 25 mM EDTA, acidi¢ed with
cold 100% trichloroacetic acid (TCA), ¢ltered onto
0.45-Wm cellulose acetate ¢lters, and subsequently
rinsed with 5U1-ml portions of cold 5% (w/v)
TCA and 5U1-ml portions of ice-cold 80% (v/v)
ethanol [15]. From the remaining three water sam-
ples and blank, 100^500 Microcystis colonies were
removed by micropipette and processed according
to the same protocol. Filters were placed in plastic
scintillation vials, scintillation solution was added,
and the samples assayed for radioactivity using an
LKB Rack-Beta liquid scintillation counter.
Sediment bacterial production was estimated via
[3 H]thymidine incorporation into DNA following
the protocol of Bell and Ahlgren [16]. In short, six
parallel samples (0.5 g wet sediment) and two form-
aldehyde-killed blanks were incubated at in situ tem-
perature with 60 WCi [methyl-3 H]thymidine (40^60 Ci
mmol31 ; Amersham) for 2 h. The incubation was
stopped by addition of formaldehyde to a ¢nal con-
centration of 2% (v/v). Three samples and one blank
were subsequently assayed according to Bell and
Ahlgren [16]. From the remaining samples and
blank, 100^500 Microcystis colonies were removed
with a micropipette, washed three times in 0.2-Wm
¢ltered water (distilled and tap water, 1+1) and
transferred to 5 ml of ¢ltered (0.2 Wm) lake water
containing 4% (v/v) formaldehyde. These samples
were then ¢ltered as described for the lake water
samples.
The NaOH extraction was used in processing sedi-
ment samples [16]. For water samples, radioactivity
retained on ¢lters after this procedure was less than
that retained after extractions in 5% (w/v) cold TCA
extraction (total macromolecules) and slightly more
(up to 10%) than the radioactivity incorporated into
a DNA fraction using the chloroform^phenol proce-
dure of Wicks and Robarts [17]. Because v70% of
the thymidine incorporated into macromolecules in
this lake was in DNA (Bell 1990, unpublished), the
NaOH extraction procedure in this study was con-
sidered to be roughly comparable to the DNA frac-
tion. Here it was considered advantageous to have a
similar procedure for sediment and water samples.
Incubation times are usually kept 960 minutes [18].
However, because low total counts were expected,
and to ensure di¡usion of thymidine throughout
FEMSEC 1010 21-4-99
15
the colonies, a longer incubation time was chosen.
Normally in this lake, although 5 nM gave maximal
incorporation rates, 15^20 nM was the thymidine
concentration used to measure production of pelagic
bacteria (Bell, unpublished). The higher concentra-
tion was used to ensure that the bacteria in the mu-
cilage received a high e¡ective concentration. This
was tested in October by measuring the incorpora-
tion of [3 H]thymidine at concentrations varying be-
tween 15 and 75 nM into material retained by a 12-
Wm pore-sized cellulose nitrate ¢lter. During this pe-
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riod, Microcystis biomass in the lake water was max-
imal (Chl a s 100 Wg l31 ) and Microcystis colonies
were the dominant particles of the s 12 Wm fraction.
Concentrations s 30 nM increased the incorpora-
tion rate by about 20%, but using higher concentra-
tions increases the risk that macromolecules other
than DNA are labelled [19]. Microcystis cells lack
the ability to incorporate [3 H]thymidine [15,20].
Autoradiographic studies have shown that the
[3 H]thymidine is incorporated in mucilage bacteria,
but not in Microcystis cells [20].
2.4. Statistical treatment
Di¡erences in speci¢c [3 H]thymidine incorporation
rate between mucilage bacteria and total bacteria
were tested statistically with Mann^Whitney test.
The di¡erences were considered signi¢cant at a level
of P 6 0.05.
3. Results
3.1. Abundance of bacteria and cyanobacteria
The abundance of Microcystis-associated bacteria
in the lake water closely followed the abundance of
Microcystis cells (Table 1). The maximum abundance
of Microcystis cells and Microcystis-associated bac-
teria, 110U103 cells ml31 and 4.07U106 cell ml31 ,
respectively, were observed on 26 September. The
Microcystis-associated bacteria constituted 40% of
the total pelagic bacterial abundance on this occa-
sion. From late autumn through spring, pelagic Mi-
crocystis colonies were not present in the amounts
large enough to allow an investigation of this type.
In the sediment, the abundance of Microcystis was
16 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22

Table 1
Abundance of Microcystis and bacteria in Lake Vallentunasjoën, and the percentage of bacteria associated with Microcystis colonies
Date Microcystis Bacteria Bacteria associated with Microcystis Number of bacteria/
abundance abundance Microcystis cells in
Abundance % of total bacteria colonies
31
Lake water (abundance in cells ml )
2 August 1989 59.7U103 9.34U106 2.33U106 26 39
26 September 1989 110.0U103 10.10U106 4.07U106 40 37
8 November 1989 17.3U103 7.19U106 0.415U106 6 24

Sediment (abundance in cells g31 dry wt.)

21 June 1989 1.29U108 14.0U1010 12.9U108 0.92 10

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2 August 1989 1.74U108 12.6U1010 57.4U108 4.6 33
26 September 1989 0.84U108 13.1U1010 42.0U108 3.2 50
6 December 1989 4.40U108 16.0U1010 66.0U108 4.1 15
17 May 1990 0.72U108 17.6U1010 24.4U108 1.4 34

highest in December, after the sedimentation of col-
onies from the lake water. The quotient between
bacteria and Microcystis cells varied between 10
and 50 (Table 1) and did not di¡er signi¢cantly
from the quotient found for pelagic colonies (Stu-
dent's t-test). The Microcystis-associated bacteria
constituted between 1 and 5% of the total benthic
bacteria.
3.2. Bacterial production in pelagic samples
The speci¢c incorporation rate of rate of
[3 H]thymidine by the pelagic Microcystis-associated
bacteria was always lower compared to bacteria
which were free-living or attached to other particles
in the water column (Fig. 1). This was especially
pronounced during the diurnal study. The largest
di¡erence was in the morning sampling (10 a.m.),
when the total bacterial community had a speci¢c
thymidine incorporation rate that was c. 9 times
higher than for the mucilage bacteria. In the middle
of the day (2 p.m.) the mucilage bacteria showed the
highest measured contribution to the total
[3 H]thymidine incorporation; about 30%. On 26 Sep-
tember, the water temperature had decreased (15³C,
compared to 19³C on 2 August). The total
[3 H]thymidine incorporation was lower than in Au-
gust, with a minor contribution from mucilage bac-

Fig. 2. Speci¢c [3 H]thymidine incorporation rate of benthic muci-

3 lage bacteria vs. total sediment bacteria in Lake Vallentunasjoën.
Fig. 1. Speci¢c [ H]thymidine incorporation rate of planktonic
mucilage bacteria vs. total planktonic bacteria in Lake Vallentu- *Signi¢cant di¡erence between mucilage bacteria and total bacte-
nasjoën. Data from two sampling dates, including a diurnal study. ria.

FEMSEC 1010 21-4-99

 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22 17

3.4. Pelagic vs. benthic bacterial production

A comparison between thymidine incorporation

rates in pelagic and benthic Microcystis colonies
has to be done with caution. It is more complicated
to determine thymidine incorporation rates in sedi-
ment bacteria than in pelagic bacteria [21]. Thymi-
dine readily adsorbs onto particles in the sediment,
and to be able to calculate a correct value of the
incorporation rate the isotope dilution has to be de-
termined, i.e. the degree of participation for the la-

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Fig. 3. Speci¢c [3 H]thymidine incorporation rate of benthic muci-
lage bacteria and total sediment bacteria at di¡erent in situ tem-
peratures in Lake Vallentunasjoën.
belled thymidine in the thymine synthesis [22]. Fig. 4
shows the thymidine incorporation rate for pelagic
and benthic Microcystis colonies, calculated both
with and without the isotope dilution estimated for
Lake Vallentunasjoën sediments. The data suggest
that there is a di¡erence in thymidine incorporation

teria. In November, when the water temperature was

7³C, no [3 H]thymidine incorporation was detectable
in the Microcystis-associated bacteria.

3.3. Bacterial production in benthic samples

The rates of [3 H]thymidine incorporation in sedi-

ment bacteria had a pattern that partly contrasted
with the pelagic bacteria (Fig. 2). On two sampling
dates, in June and August, the speci¢c [3 H]thymidine
incorporation rate of the mucilage bacteria was 8
and 3 times higher, respectively, than for the total
benthic bacterial population. The production of
benthic mucilage bacteria increased dramatically at
temperatures s 15³C (Fig. 3). When temperatures
were lower, the speci¢c production was low in all
samples, and the di¡erences between the two bacte-
rial fractions were small. On 26 September, at a tem-
perature of 15³C, the mucilage bacteria had a sig-
ni¢cantly lower speci¢c incorporation rate of
[3 H]thymidine than the other sediment bacteria.
The results from 6 December were close to the de-
tection limit of the thymidine method, even when the
sample size was 500 Microcystis colonies, and there
was no signi¢cant di¡erence between incorporation
rates for mucilage bacteria and total bacteria on this
date. Also, in May, when the temperature was 14³C,
Fig. 4. Speci¢c [3 H]thymidine incorporation rates of mucilage
there was no signi¢cant di¡erence in bacterial pro- bacteria in Microcystis colonies from sediment and water column
duction between mucilage bacteria and total bacte- in Lake Vallentunasjoën, with (A) and without (B) assessment of
ria. isotope dilution.

FEMSEC 1010 21-4-99

18 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22
rates between pelagic and benthic colonies, with
higher rates in the benthic colonies.
In conclusion, this study showed that the speci¢c
incorporation rate of [3 H]thymidine by the pelagic
Microcystis-associated bacteria was always lower
compared to bacteria which were free-living or at-
tached to other particles in the water column, while
in the sediment, Microcystis-associated bacteria were
more active than other bacteria on two of the ¢ve
sampling occasions (Figs. 1 and 2).
4. Discussion
The thymidine method has been widely used to
measure heterotrophic bacterial production in the
water column and surface sediments of both marine
and freshwater environments [18,22,23], but the anal-
ysis protocols may not be applicable for measuring
production of bacteria embedded within the muci-
lage of Microcystis colonies. If the di¡usion of thy-
midine into the mucilage is slow, the bacteria in the
Microcystis colonies may be exposed to a lower con-
centration of thymidine than other bacteria in the
surrounding environment. In this study, we tried to
optimise the [3 H]thymidine concentration and the
incubation time to minimise this risk. The results
suggest that the rate of thymidine incorporation in
mucilage bacteria is not largely underestimated. In
the lake water, the incorporation rate in total bac-
teria was nine times higher than in mucilage bacteria.
However, the results were opposite in the sediment,
where the mucilage bacteria incorporated up to eight
times more [3 H]thymidine per cell than the total bac-
terial community.
There are several possible explanations for the dif-
ferences in [3 H]thymidine incorporation rates be-
tween mucilage bacteria and total bacteria. First,
there may be di¡erent taxonomic composition of
the bacterial community in the mucilage of Micro-
cystis colonies, compared to other bacteria in the
water column and sediments. The microenvironment
of the mucilage may be di¡erent regarding e.g. oxy-
gen concentration, redox potential and pH [24] as
well as nutrient concentrations. The mucilage even
may host bacteria unable to grow outside the colony
[25,26].
Besides taxonomic di¡erences in growth rate, there
FEMSEC 1010 21-4-99
may also be di¡erent abilities to take up and incor-
porate the thymidine into DNA among the bacteria
[22,27^30]. This might explain the lower production
measured in pelagic Microcystis colonies compared
to other pelagic samples. However, autoradiograms
[20] indicated that a large part of the mucilage bac-
teria in Microcystis colonies from Lake Vallentunas-
joën had incorporated [3 H]thymidine. Although thy-
midine incorporation in aerobic waters is now
considered a measure of `heterotrophic' bacterial
production (e.g. [23]), this interpretation should be
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applied with caution to sediment environments in
general.
In the pelagic zone, attached bacteria generally
incorporate radiolabelled organic compounds at
higher rates than free-living bacteria [31], but for
[3 H]thymidine the rates are generally lower
[5,32,33]. Kirchman [34] suggested that attached bac-
teria have a lower growth e¤ciency, which may be
due to the larger release of extracellular polymers by
these bacteria, both for attachment [31,34] and to
degrade the particle or the macromolecular com-
pounds bound to the particle [35]. This view is in
accordance with the observation that attached bac-
teria are generally larger than free-living bacteria,
although the reverse has also been reported [5,8].
Another cause of low bacterial production in pe-
lagic Microcystis colonies may be slow di¡usion
within the mucilage. The chemical composition of
the mucilage may di¡er substantially with the time
of the year and the condition of the Microcystis cells,
but the main constituent is carbohydrate [36]. Low
di¡usion rates of nutrients from the lake water might
cause C:N:P quotients that do not meet the require-
ments of the growing bacteria. Furthermore, slow
di¡usion out of the colonies of inhibiting or toxic
exudates from the cell metabolism of the Microcystis
cells may restrain the growth of attached bacteria.
Finally, the lower production of pelagic Microcys-
tis-attached bacteria may be due to low mortality.
Bacterial production depends on both the growth
rate and abundance of bacteria. Pelagic environ-
ments where bacterial grazers are suppressed develop
high abundances of bacteria that are growing slowly,
and a major fraction may be inactive. On the other
hand, intensive grazing on bacteria keeps the bio-
mass low, but the bacteria are growing rapidly
[6,37]. Microcystis is generally considered to be
 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22
grazed only to a limited extent [38,39]. Bern [40] did
not ¢nd any grazing on [3 H]thymidine-labelled bac-
teria attached to large colonies of Microcystis wesen-
bergii in Lake Norrviken, adjacent to Lake Vallen-
tunasjoën. Consequently, the biomass of mucilage
bacteria in many colonies could be near `carrying
capacity', having lower speci¢c growth rates than
the other pelagic bacteria.
Contrary to this study, Worm and Sondergaard
[41] found a higher speci¢c growth rate of Micro-
cystis-attached bacteria than for ambient pelagic
bacteria. The Microcystis colonies were characterised
as `bacterial incubators' which supply the ambient
lake water with bacterial biomass through shedding.
This contrasting result might be due to di¡erences in
natural environmental conditions, but may also be
explained by di¡erences in methodology. Worm
and Sondergaard [41] used ¢lters to separate Micro-
cystis colonies from the lake water. Filtration collects
also other lake water particles, which may host nu-
merous bacteria and have a high microbial activity.
The method used in the present study, on the other
hand, may have a slight bias towards fresh and
healthy Microcystis colonies and thereby possibly
lower microbial activity. Decaying Microcystis colo-
nies are sometimes di¤cult to distinguish from other
organic debris in a stereomicroscope and may thus
be under-represented when picking out samples with
micropipette.
In autumn, Microcystis colonies settle to the bot-
tom of Lake Vallentunasjoën. Their survival in the
sediments is very long, probably several years in
some cases, but ultimately the majority of the colo-
nies will be decomposed. Decay and lysis of Micro-
cystis cells will drastically change the extracellular
release of inorganic nutrients and organic com-
pounds, but also a switch to a resting stage with
changed metabolism may a¡ect the leakage from
Table 2
Bacterial abundance, [3 H]thymidine incorporation rates and the relative contribution of mucilage bacteria to these numbers in the sedi-
ments of Lake Vallentunasjoëna
Bacterial abundance, 1010 cells g31 dry wt.
% of sediment bacteria attached to Microcystis
[3 H]Thymidine incorporation rate (average June^September), 10322 mol cell31 h31
% of total [3 H]thymidine incorporation in mucilage bacteria (June, August)
a
1985 data from Bostroëm et al. [10], 1989 data from this study. n.a., not assayed.
FEMSEC 1010 21-4-99
19
the cells. Empty Microcystis colonies are easy to
identify by epi£uorescence microscopy after acridine
orange staining. The mucilage keeps the typical
shape of a Microcystis colony, especially the muci-
lage from M. wesenbergii. The mucilage is empty of
Microcystis cells, but certainly not of bacteria. In a
detailed seasonal study of benthic Microcystis colo-
nies, Brunberg (unpublished) found that 66%
(S.D. = 12, n = 36) of the colonies in the surface sedi-
ment (0^10 cm) of Lake Vallentunasjoën were devoid
of living Microcystis cells. Degradation of moribund
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Microcystis cells would possibly enhance the bacte-
rial growth in the mucilage, and thus a higher
[3 H]thymidine incorporation rate would be expected
in the benthic mucilage bacteria compared to the
pelagic mucilage bacteria (cf. Fig. 4).
The results from 26 September indicate that there
may be other reasons, in addition to temperature
dependence, for the declining speci¢c production of
benthic mucilage bacteria (Fig. 2). The lower value
for mucilage bacteria than for total bacteria suggest
that the remaining population in the sediment on
this occasion was more resistant to decomposition
than earlier during the summer. The autumn sedi-
mentation of the water population had not yet
started at this time, and the benthic population prob-
ably to a large extent was composed of Microcystis
colonies which had survived for 1 year or more in
the sediment. Results from experimental laboratory
studies with Microcystis from Lake Vallentunasjoën
[42] also support the conclusion that colonies with
di¡erent age and pre-history have di¡erent resistance
to decomposition and bacterial attack.
Generally, a large percentage of sediment bacteria
are inactive [43,44]. Although a small fraction may
be growing rapidly, the speci¢c activity and growth
rates calculated for the whole sediment population
are low. The activity of sediment bacteria is consid-
1985 1989
3^14 9^18
10^40 1^5
59 11
n.a. 8^13
20 A. Brunberg / FEMS Microbiology Ecology 29 (1999) 13^22
ered to be governed by the availability of substrate
and electron acceptors, and by the temperature. Bos-
troëm et al. [10] concluded that the bacterial activity
in the sediments of Lake Vallentunasjoën was primar-
ily governed by temperature. This is further implied
by the data in Fig. 3. The results are also in accord-
ance with Kirchman [34], who found that attached
bacteria were larger than free-living bacteria in the
water of a freshwater pond during July and August,
but not in February and May. These ¢ndings indi-
cated that attached bacteria were relatively more ac-
tive than the free-living bacteria in the summer, but
during the winter the activities of the two groups of
bacteria were equal.
A comparison with data from 1985, when an ex-
tensive study of the benthic microbial community
was made in Lake Vallentunasjoën [10], demonstrates
the importance of Microcystis colonies as sites of
enhanced bacterial activity in the sediments (Table
2). The 1^5% of Microcystis-attached bacteria in
the present study (1989), were responsible for 8^
13% of the total bacterial production in the sedi-
ment. In 1985, the biomass of Microcystis in the
sediment was about ¢ve times higher than in 1989,
and up to 40% of the sediment bacteria were at-
tached to Microcystis colonies. No corresponding
data on the bacterial production of mucilage bacteria
are available for 1985, but they may have been re-
sponsible for a large part of the high total bacterial
production in the sediment that was measured that
year. Moreover, the data from a 5-year study of
microbial biomass and activity in Lake Vallentunas-
joën showed a co-variation of Microcystis biomass
and bacterial production in the sediment [14].
The immediate advantages and/or disadvantages
for bacteria attached to Microcystis colonies thus
seem to vary, depending on the environment in
which they are situated, but also due to the condition
of the Microcystis cells as indicated by the data.
However, there is also a long-term aspect on the
advantages for mucilage bacteria. The Microcystis
colonies may provide microenvironments for bacte-
ria that would not survive in the prevailing environ-
mental conditions of the lake water (cf [45]). When
the right conditions occur, the mucilage bacteria may
serve as an inoculum which facilitates renewed
growth. A low bacterial activity and growth rate in
the pelagic Microcystis colonies in the short-term
FEMSEC 1010 21-4-99
may thus be well paid back in the long-term, when
the situation changes and the Microcystis cells start
to decay and provide potentially high-quality sub-
strates for the bacteria.
Acknowledgments
This work was performed in close cooperation
with the late Dr. Russel T. Bell. Originally, he was
a co-author, and participated in the preparation of
Downloaded from https://academic.oup.com/femsec/article-abstract/29/1/13/765462 by guest on 26 January 2019
the ¢rst draft of this paper. Russ's expertise on thy-
midine incorporation methods was important for the
planning of the study and in the methodological
modi¢cations that we made. Thanks are extended
to Jan Johansson for expert technical assistance,
and to Dr. L. Tranvik and Dr. J.J. Cole for critical
reading of the manuscript. This work was supported
by grants from the Swedish Natural Science Re-
search Council (NFR).
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