Abstract
In the profundal sediment ot Lake Constance (143 m depth) the temperature is constant at 4°C. Despite the constant
lemperature, CH, concentrations changed with season between about 120 PM in winter and about 750 ph4 in summer,
measured down to 30 cm depth. The acetate concentration profiles also varied between seasons. In summer, acetate
concentration reached a maximum at about 100 PM in 2 or 4 cm depth. In winter, maximal concentrations of about 5 PM
were observed over the entire depth. Input of organic material in late spring may be the reason for the seasonal change of
both compounds. To simu!ale such a sedimentation event, iriiaci sG,‘iment cores were covered with suspensions of
Porphyidium aer+ynhm or Syrteckococcrrs sp. The addirion of the phytoplankton material resulted in a drastic increase of
acetate concentrations with a maximum at 2 cm depth, similar to in situ acetate concentrations measured in summer. ‘l’he
same applies for CH, for which increased concentrations were observed down to 6 cm depth. H, concentrations, on the
other hand, showed no distinct increase. Treatment of intact sediment cores with “C-labeled S~~clto~u~cus cells resulted in
the formation of lJC-acetate ‘?H, and “CO,. Maximum concentrations of ” CH, were found at 4 cm depth, i.e. just
above the depth lo which “C‘-acetate pcnctrated:The results show that phytoplankton blooms may cause a sea:xmal [variation
of acetate and CH, in profundat sediments of deep lakes despite the constant low temperature. They also indicak that
acetate is the dominant substrate for methanogenic bacteria in the profundal sediments of Lake Constance.
Kc~v~I.I~.~:Methane; Acetate; Concentration
profile; Profundal sediment; Sedimentation;
B. Introduction
Microbial production of CH, is one of the major
pathways of degradation of organic matter in anoxic
aquatic sediments [I]. It takes place if oxygen and
* Corresponding author. Tel: + 49-6421-287053; Fax: + 49l- 16 1470; E-mail: ConradClr’mailer.uni-marhurg.dc
642
016%6496/95/$09.50
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SSDI 0168-6496(Y4300088-3
Seasonal change
alternate inorganic electron acceptors such as nitrate
and sulfate are not available [2]. This situation is also
given in the profundal sediment of Lake Constance,
a large, mesatrophic, monomictic preaipine lake [3].
Most of the research on CH, production in lake
sediments has been done in profundal sediments of
eutrophic lakes with a high input of organic matter
[4-61 or in littoral sediments with temperatures r+
quired by mesophilic bacteria [7-91. hn contrast,
European Microbiological Socictics. All rights rcscwcd
profundal sediment of Lake Constance is an environment with a relativeiy low input of organic Matler
and permanently low temperatures.
Temperature is one of the most important factors
which influences bacterial activity. Zeikus and Winfrey [lo] showed that methanogenesis was limited by
in situ temperature and that methanogenic bacteria
operated optimally at 30-40°C. The same was observed for methanogenic H, metabolism in anoxic
paddy soil [Ill.
In the profundal sediment of Lake Constance, the
in situ temperature is constant at 4°C. Despite the
constant low temperature, we observed seasonal variations of acetate and CH, concentrations. The seasonal variations could not be an effect of temperature, A conceivable explanation would be that seasonal blooms of phytoplankton caused the seasonality of acetate and CH, due to the input of organic
matter by sedimentation. This study describes the
seasonal change of acetate and CH, in the profundal
sediment, and presents experiments which show that
the seasonality can be explained by sedimentation of
phytoplankton.
2. Materials and methods
Lake Constance is a large prealpine lake. Sediment samples were taken in its western basin, the
’ uberlinger Set’, as described by Frenzel et al. 1121.
The samples were taken from the deepest part at a
depth of 143 m. The properties of the sediments of
‘Oberlinger See’ have been described in detail by
Miller [13,14]. The porosity was about 90% and
decreased to about 35% below 8 cm depth. The
temperature of the profundal sediment was constant
at 4°C. Cores were transported in styropor boxes to
the laboratory and kept in darkness at 4°C.
For measurements of vertical CH, profiles, subsamples of the sediment were taken every second
centimeter through holes in the corer using plastic
syringes (10 ml) with cut-off tips. The sediment
samples were transferred into pressure tubes (26 ml)
and processed for measurements of porewater concentration ( PM) as described earlier [ 121, Biological
activity was stopped by injection of 1 ml of 1 M
H ZSi),. Gas bubbles were not removed befolt: extraction because, in contrast to littoral sediment, tests
showed that gas bubbles were not contained in profundal sediment [7]. Sediment porewater was recovered by centrifugalion (at 4°C) after addition of 100
~1 HgClz (stock solution 1 g 1-l) to about 5 ml
sediment to kill biological activity. The porewater
was filtered through membrane filters (regenerated
cellulose, pore size of 0.45 pm, Sartorius, GSttingen, Germany) and stored frozen ( - 20°C) until
analysis.
2.2. Analytical techrriques
Analysis of CH, and CO, was done by gas
chromatography using a flame ionization detector
(Carlo Erba, Milan, Italy). CO, was determined after
conversion to CH, with a methanizer (Ni-Catalyst at
33O”C, Chrompak, Middelburg, the Netherlands). HZ
was determined in a RGD2 reduced gas detector as
described by Cord-Ruwisch et al. [15]. ‘“CH, and
“‘CO, were analysed in a gas chromatograph
equipped with methanizer, flame ionization detector
and RAGA radioactivity gas proportional counter
(Raytest, Straubenhardt, Germany) [ 161. Dissolved
compounds (succinate, lactate, formate. acetate, :Jr*pionate, butyrate, isopropanol, valErate, n-butane: arid
caproate) were analysed by high pressure liquid
chromatography (Sykam, Gauting, Germany) with a
refraction index detector. Tht: detection limit was
S-50 PM [17]. The outlet of the detector was connected with a radioactivity scintillation monitor
(RAMONA; Raytest, Strauhennardt, Germany) with
a detection limit of 2500 dpm ml -’ for measuring
radioactive dissolved compounds.
2.3. Sedimematiorl experiments
‘JC-labeled
with urllabeled and
phytoplattktort cells
First experiment
Synechococcus
sp. (a cyanobacterium
isolated
from Lake Constance; [18] and Poipphyridium aerugerlium (red alga from stock cultures of Prof.
Wehrmeyer, Marburg) were grown ;t 3O”C, 2400 lux
and 2% CO,. After 1 week, cell suspensions were
centrifuged at 10000 rpm for 30 min and resuspended in demineralized water. One sediment core
(diam. 8 cm) was covered with 60 ml of a Sytze-
suspeusion with a cell density of 80” cells
(corresponding to a 1 cm-layer above the
sediment surface). A second core was covered with
Pmplzyridim cells in the same way, and two other
cores were treated with 60 ml water from the sampling site. The sediment cores were incubated at 4°C
in the dark. After three months, the sediment cores
were cut into 2 cm slices (corresponding to about 10
ml sediment for each slice). Half of the sediment
slices were transferred into pressure tubes (26 ml)
and the porewater concentrations of C
3
were measured as described above. Dissolved compounds were measured in the porewatcr of the other
half of the sediment slices,
chococcus
ml-’
mixture of three different S_wrcchococcus strains
(isolated from Lake Constance, [1X]) was grown as
described above. After I week, the cells were harvested and resuspended in demineralized water to
give 1 1 suspension. The suspension was shaken
horizontally by 100 rpm at 1900 lux and ambient
CO, for 3 days. Then 0.7 mCi Na”C-bicarbonate
(54 mCi mmol - *; Amersham-Buchlcr,
Braunschweig, Germany) was added. After 3 days, 97Yb of
the Na”C-bicarbonate
had disappeared and was apparently incorporated into the cells. A set of 5 sed:ment cores (diam. 3.5 cm) was each covered with Iti
ml of the SyrrecCrococcrr.s suspension (corresponding
to a 1 cm layer above the sediment surface) with a
cell density of 1 X 10’ cells ml ’ labeled with I x
10’ dpm ml ~ I. Another set of 5 sediment cores was
treated with IQ ml water from the sampling site. The
Syrreclrococcus suspension had a dry matter content
of 19.9 mg ml ~ ‘. With the assumption that 50% of
the dry mass was carbon [19], the cells added to the
surface area (10 cm’) of the sediment cores corresponded to a sedimentation event of 99.3 g C m - ‘,
and thus was similar to that observed in situ [2O].
The cores were closed with rubber stoppers and
incubated in a water bath at 5 + 1°C in the dark. At
intervals of 4 weeks, one sediment core with labeled
Sy’trechoc~ccr~s cells and one control core were analysed as described for the first experiment.
The experiments were done without
replicates.
The potential error was determined
by analysing
the
vertical profiles in 2 different sediment cores taken
from the 3me site on the same date. This experiment
A
was repeated 3 times. The CH, concentration
files were always identical within 2-25%.
pro-
CH, concentrations in the porewater of the profurdai sediment at tht: sampling site ’ Ubcrlingcr
Sre’
increased with depth and reached a constant
:-;,.,,,,---* 6.2.92
* -27.6.92
-1
~~~~~1.
20
0
-~
._
40
60
80
_I
100
acetate QJM)
Fig.
2. Vertical
bctwccn
August
concentration
profilcs
IYYO and August
IYYZ.
of acctatc cm three dates
254
A
+ Porphyrrdium
*control
100
50
1
150
200
acetate &M)
-.-.-_-
__.-..
.~~~
‘. .
100
200
W
300
--.‘,_
i
500
400
WV
5
C
value at about 10 cm depth (Fig. 1). The maximum
CH, concentrations showed a distinct change with
season. In spring (May 1990 and March l991), the
concentrations were lowest at about 120 EJ~Mand
increased during summer (July 1990 and August
1992) to about 550-750 FM. A similar seasonal
change was observed for the concentrations of acetate in porewater (Fig. 2). In summer 1990 and
1992, a maximum acetate concentration of about 100
PM was measured in 2-4 cm depth. Below this
depth, acetate concentrations were at 5-40 PM. In
winter, acetate decreased to values of about 5 PM
over the entire depth.
Temperature changes could not be the reason for
the observed seasonal change, since temperature was
constant at 4°C in this sediment. Therefore, we srudied the possibility that sedimentation of organic material was the reason for the seasonal variation of
CH, and acetate. To simulate a sedimentation event,
sediment cores were covered with either Pwphyridiwn or Syrrechococcrts cells. The influence of the
phytoplankton cells on intermediary metabolites of
anaerobic degradation and on the terminal product
CH, was determined in comparison to sediment
cores without addition of phytoplankton. Since the in
situ measurements had shown that CH, concentrations increased between spring and summer, the
exposure of the sediment to microbial cells was
terminated after 3 months, and the sediment cores
were tested for an increase of CH; and acetate
concentrations after this incubation time.
Sediment cores that were covered either with
Porphyridium
or Syneci~ococcus
cells exhibited a
distinct increase of acetate concentrations. In the
core with fWp!zyridiwn
(Fig. 3a), a maximum concentration of about 170 PM acetate was measured at
2 cm depth. Similarly, acetate concentrations of I10
PM were measured at 2 cm depth in the core with
Syrlechococcus
(data not shown). Both vertical acetate concentration profiles were similar to those
measured in situ in 1990 and 1992 (Fig. 2). However, the acetate concentrations in the control cores
25
Porphyridium
500
* control
Fig. 3. Vertical conccnlration prdilcs in scdimcnt cores amcndcd
1000
Hz VW
1500
2000
with Pmphyidim
acrugorium
out phytoplankkm cells
H 2’.
cells and in scdimcnt cores with-
( = control). (A) acct;% (B) CH,; (C)
without phytoplankton cells were similar to the in
situ profile measured in February 1992. The rest&s
indicate that sedimentation of organic material (i.e.
phytoplankton) may have caused an increase in acetate concentrations in 2-4 cm depth. No change
could be observed for other intermediary compounds
such as lactate, propionate, isopropanol or caproate,
neither under in situ conditions nor after artificial
sedimentation with Porphyridium or Synechscocc~rs.
The concentrations of lactate and other compounds
were always close to ihe detection limit of about 5
PM.
Addition of phytoplankton cells also increased the
Cl-I, concentrations in the sediment. In the core with
Porphyl-idium, CH 4 concentrations increased signifi-
cantly between 1-6 cm depth with maximum concentrations of 440 p
pth (Fig. 3b). In
the core with §yne
4 concentrations
were also increased compared to the Jntreated control (data not shown).
z concentrations, on the
other hand, showed no distinct increase, either with
Porphyridium (Fig. 3~1, or with Sy~ch~cnccus cells
(data not shown).
To find out whether the increase in C
caused by the increase of acetate concentrations, we
measured the degradation of “C-labeled SOWi
!
i
a
6
C
F6
j *acetate
3
* CHq
* co2
-a 10
4.;
after 4 weeks
after 6 weeks
14
16
1
i
0
200
400
600
800
1000
1200
t
I
1
16 L
0
1400
200
400
600
-800
1000
1200
1400
kdpm
kdpm
0
*
acetate
‘Co2
* CH4
alter 20 weeks
after t2 weeks
e
16 -----r-i
0
200
400
600
800
kpdm
100012001400
ID
j
16 j
0
200
400
600
/
803
kdpm
I
1000
1200
1400
i .._
0 200
~_
~___
_...._
_~ 400
600
acetate
14
I
-A___
800
0
1000120014b0
50
150
100
propionate
(uM)
200
(@I)
e
D
i
50
0
200
150
100
lsopropanol
50
WM)
100
caproate
150
200
GUM)
c-~,-514
- 4 weeks
* 8 WBBkl
+
12
weeks
"20weeks
-..._-~^l__-
0
200
400
600
800
1000120~1400
methane
(IA)
Fig. 5. Formaticm tlf (A) acctatc. (B) propionatc.
nftcr addition of labeled .~~?tcrhocorc~rs
culls.
(Cl
isoprqx~nol,
(1))
caproarc
;md (E) mcthanc
during
the
incubation
time of 20 weeks
c*lncpcoccuLscells to ‘k-acetate.
%I2 and ‘k
(Fig. 4a-d). No radioactivity
was detected in other
dissolved
tion
compounds.
of labeled
Already
4 weeks
celSs. radioactivity
of acetate,
CO,
after
in the
appeared
and CH,.
Both
esp pr0fundaI scdimcnts ;thc cnvirt~nmcnth wit11
addi-
“‘CO2
and
relatively
ment
constant
of Lake
conditions.
Constance
4 decreased with depth and were detected down
to 10 cm and 6 cm depth, respectively.
The concen-
stant at 4°C. Despite
trations
summer.
of “CO2
finally
increased
rcachcd down
to
with
of “‘C-acetate.
profiles
shycd
more or less constant.
20, the total
amount
decreased
d). This
from
“CH,
integrated
Simultanously,
over
from
total
to
1900 kdpm
about
4 to week
core increased
result is consistent
the following
[I
of
900 kdpm.
and
on the other hand,
From week
depth in the sediment
to about
time
> Ih cm depth. The concen-
tration
entire
incubation
of
with
CH,
acetate
the
and
wtsrc’ incrc;lsed
“C-acetate
could
ho caused
zero (Fig.
-Ic,
production
by
of
C&XWNW.~ cells
of
the
sediment
resulted
acetate, propionate,
Sa-d).
isopropanol
The concentrations
lites were below
our analytical
These
system.
and caproate
of other potential
the detection
metabolism
in littoral
limit
dal sediment.
centrations
After
in the surface
reached
he measured
after
20 weeks
trations,
i.e.
February
treated
acetate
similar
reached
to
cores,
dissolved
compounds
caproate)
showed
were
propionate,
no longer
creased between
depth
Se).
reaching
and
in phase
the
organic
done by Hansen
8
in
un-
NH;
The
0,
tluxcs.
results
the first
time
(Fig.
Sb-d).
After
isopropanol.
detectable.
CH,
and
simi-
stimulate respiratory
production
experiments
[X3.27]
in
were
marine
;I
but also CH,
The
simulation
plankton
the
cells
was
of
matter
in particular
from
derived
only
not
in the surface layer
sediment
cvcnt
layers.
with
phyto-
.S~~t1c~c.llcr~.oc.-
the concentrations
indicating
that
the phytoplankton
degraded via. acet;ltc tn CH4 ai about 4 cm
caproatc
(Fig.
dcmonstratc for
in the sediment
Constance, 0,
1m1
decreased.
or
i.e. F%lp,‘:;~~I:sr’i~~~
_.
increased
CO-
dunitrifica-
cvcnts
of ;t sedimentation
Like
in-
and
in dtxper
production
matzi;:!.
organic
and increased
reduction
degradation
12 weeks
CH,
the
primary
scdimcntation
of the sediment.
the top 0 cm
of 11100 PM
The
with
is seasonal
and nitrification
depth
concentrations
4 and 12 weeks within
a maximum
and
[ZS].
which
consumption
that
(‘11.~ cells,
shaped
matte;
of our experiments
<If acetate and CH,
were
observed
simulation
Sulfate
stimulated
The other
which
of the ben-
on sediment respiration and fluxes of I),.
NH;,
NO, and NO, . The xidcd algatl cells
time of 5 months.
isopropanol
e\.cnts
seasonal
is correlated
and Blackburn
decreased
(propionate.
are
the surfxc
with
where
consumption
consumption
Sedimentation
caused increased
concen-
in
community
in oxygen
hand,
profiles
to those of acetate
incubation,
concentrations
large
stimulating
Similar
sediments
in the oxygen
of particulate
CO,.
and
situ
to the sediment,
oceanic
flux
could
in
matter
sediment
change
tion were
background
of ;I
in Lake Constance
for
known
a maximum
slowly.
is observed
arc
and
measured
on the other
over the total incubation
larly
those
Acetate
1%2.
control
decreased
of phytoplankton
formation
proccsscs in the sediment.
acctaic con-
down to 4 cm depth. In the Mluwing
weeks, acetate concentrations
bloom
Our
change
algal cells
Constance
concentrations
seasonal
sediment to study the influence of sedimentation
to the profun-
incubation,
of 1300 PM (Fig. Sa). Increased
of
have previ-
of Lake
water
pm!
year in spring,
rjf organic
[24,25].
of anaerobic
is extended
4 weeks
(Fig.
metabo-
( < S-51!
compounds
sediments
Here, the observation
SJWP-
concentrati<ins
been shown to be intermediates
ously
[?I].
in increased
with
this
by sedimentation
Every
fluctuations
cores
that
to _3(1cm
to the winter.
&gradation
thic
Incubation
down
comp:mzd
111
4 cm
sedimentation
of the phyro[ 221. The subsequent
plankton
material in lotc spring WJSL’S an increased
input
+ ‘JCO,,
iit the upper
concentrations
demonstrate
phytoplankton
reaction:
,2]I’C - acetate -+ “CM,
meIhilne
in spring.
was observed.
concentrations
dcpt’!
sedi-
was con-
a seasonal change
concentrations
depth
experiments
zero
this stability
and CH,
acetate
In the profundal
the temperature
sediment
layer
In the profundal
is depleted
[12],
upper 5 mm and 2 cm,
personal communication).
sis can be expected
NO,
within
rhc
and SO:
respectively
Thclcforc.
to be the
sediment of
(P.
upper
in
2
the
Frenzc!.
mcthanogcnc-
dominant terminal step
in anaerobic degradation at depths > 2 cm. In the
upper 2 cm sediment layer of Lake Constance, 130
sulfate-reducing bacteria could be isolated with Xetate as substrate at the in situ temperature CF. Bak,
PhD thesis, Konstanz, 1988). Only spores of Des&
fotamacrtlun~ acetoxidms could be observed, but
they did not germinate at in situ conditions. In the
deeper sediment, the sulfate concentrations (about 20
PM) are too low to allow growth of sulfate-r,ducing
bacteria [2X]. Obviously, acetate is not degraded by
sulfate reducers in the upper sediment layers of Lake
Constance. Therefore, acetate can penetrate into
deeper sediment and be consumed by methanogenic
bacteria.
In most freshwater sediments, CH, is produced
from both acetate and H,\COI
at a ratio of about
7:3 [4,20]. However, in some freshwater sediments
H, may be the dominating substrate [30,31], whereas
in other sediments it may be acetate 1321. Our results
indicate that acetate was the more important
methanogenic precursor in the profundal sediment of
Lake Constance. This conclusion is mainly based on
the observation that “C-acetate penetrated into the
sediment just a little deeper than where the maximum concentrations of “‘CH -I appeared. Radioactive
CO,, on the other hand, penetrated much deeper. In
addition, H, concentrations were not affected by the
sedimentation experiment. Our conclusion is in
agreement with earlier experiments demonstrating
that H, turnover in the sediment of Lake Constance
is mainly due to homoacetogenic rather than to
methanogenic bacteria [ 1 l]. Conrad et al. concluded
that the activity of HI-dependent methanogens may
be limited by the low (4°C) temperature of the
profundal sediment.
Acknowledgements
We thank Claudia Nickel-Reuter and Dr. W.
Reuter for helpful advice during cultivation of phytoplankton cells and Captain K. Wiedemann of the RV
Roherr LnurcrAorr~ for his help and cooperation during sampling on the lake. This work was financially
supported by the Deutsche Forschungsgcmcinschaft
(SFB 248: Cycling of Matter in Lake Constance) and
the Fonds der Chemischen lndustrie.
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