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Applied and Environmental Microbiology, February 2000, p. 712-717, Vol. 66, No. 2
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
In Situ Determination of Sulfide Turnover Rates in
a Meromictic Alpine Lake
Lucas
Lüthy,
Markus
Fritz, and
Reinhard
Bachofen*
Institut für Pflanzenbiologie,
Universität Zürich, CH-8008 Zürich, Switzerland
Received 18 August 1999/Accepted 17 November 1999
 |
ABSTRACT |
A push-pull method, previously used in groundwater analyses, was
successfully adapted for measuring sulfide turnover rates in situ at
different depths in the meromictic Lake Cadagno. In the layer of
phototrophic bacteria at about 12 m in depth net sulfide
consumption was observed during the day, indicating active bacterial
photosynthesis. During the night the sulfide turnover rates were
positive, indicating a net sulfide production from the reduction of
more-oxidized sulfur compounds. Because of lack of light, no
photosynthesis takes place in the monimolimnion; thus, only sulfide
formation is observed both during the day and the night. Sulfide
turnover rates in the oxic mixolimnion were always positive as sulfide
is spontaneously oxidized by oxygen and as the rates of sulfide
oxidation depend on the oxygen concentrations present. Sulfide
oxidation by chemolithotrophic bacteria may occur at the oxicline, but
this cannot be distinguished from spontaneous chemical oxidation.
| |
INTRODUCTION |
Lakes, like most ecosystems, are
open systems in a steady state with different trophic levels. To
understand the interactions between organisms and the environment,
inputs and outputs of the nutrients at each trophic level must be
known. Rates describe the turnover of chemical species at specific
sites and therefore describe elemental fluxes in biogeochemical cycles
as well as microbial activities in an ecosystem.
In physiology and ecology several methods for evaluating rates have
been described. In sediments microbial reaction rates are calculated
from concentration-depth profiles by using flux calculations based on a
modified Fick's first law; however, as incubations of several days are
necessary, only a low temporal resolution is achieved. Primary
production rates from phytoplankton are obtained by the use of
radioactive carbon isotopes. Samples are collected in a depth profile
and incubated with 14CO2 at the originating
depth for a few hours. But such results will also not give the actual
in situ reaction rates for rapidly cycling elements.
In this paper we present a new approach for determining in situ
reaction rates for production and consumption of sulfide in the open
water. Experiments were done in a meromictic alpine lake with a
pronounced biological sulfur cycle (7, 11, 12, 15, 20).
Under anoxic conditions sulfide is produced by sulfate-reducing bacteria, which reduce sulfate to sulfide at the expense of organic substrates. At the same time, if light is present, sulfide is oxidized
by anoxygenic phototrophic bacteria, which use it as an electron donor.
Concentration profiles for Lake Cadagno often show no sulfide in the
layer with the highest biomass concentration of the water column and
thus cannot give information on actual turnover rates of the sulfur
compounds because, in a steady state, sources and sinks are balanced.
The "push-pull" technique, which has been previously applied in
groundwater systems (9, 10, 17) was used to obtain real in
situ sulfide turnover rates with a high temporal resolution in an
undisturbed ecosystem.
| |
MATERIALS AND METHODS |
Site description.
Lake Cadagno is a meromictic alpine lake
about 21 m in depth and 300 by 500 m in size. It is located
at an altitude of 1,920 m in the southern part of the Alps in
Switzerland. The chemistry of the lake water is determined by the
geology of the region. A band with dolomite and gypsum in the catchment
area of the lake is surrounded by crystalline rock. Sulfate is leached
from the gypsum and enters the lake at the surface and by underwater
springs. The monimolimnion is constantly anoxic, and there sulfate is
reduced to sulfide by sulfate-reducing bacteria. At the redoxcline
between the oxic mixolimnion and the anoxic monimolimnion steep
gradients of oxygen and sulfide are observed (Fig. 2) (7, 11,
15). Just below this interphase the high turbidity indicates a
dense population of anoxygenic phototrophic bacteria composed mainly of
Chromatium okenii and Amoebobacter purpureus
(6, 15, 20). These bacteria use sulfide as the electron
donor during photosynthesis and oxidize it mainly to S0 and
SO42
. In the dark these phototrophs reduce
elemental sulfur again to sulfide in an anaerobic respiration (4,
21). This zone of primary production is of great importance for
the food web in the lake. Sulfate-reducing bacteria, which are present
in the same layer as the phototrophic bacteria as well as in the deeper water and the sediments, reduce sulfate to sulfide using products of
the degradation of settling biomass as electron donors. Besides these processes, sulfide is oxidized at the edge of the oxic
mixolimnion by chemolithotrophs as well as by spontaneous chemical
reactions (1, 14, 18). Many profiles of chemical parameters
including sulfide concentrations have been collected during the past
years. Interestingly enough, the depth of highest bacterial
density is often completely devoid of sulfide during daytime (Fig. 2)
(7, 11, 12), while the cells of Chromatium
species present in this layer are usually full of sulfur droplets
(S0, polysulfide).
Push-pull experiments.
The push-pull method was originally
developed in the oil technology field to determine residual oil
saturations in petroleum reservoirs (19). Recently, Istok et
al. (9, 10, 17) adapted the technique to quantify rates of
microbial processes such as aerobic respiration, denitrification,
sulfate reduction, and methanogenesis in a petroleum-contaminated aquifer.
In a push-pull experiment a pulse-type injection of a defined test
solution followed by a chaser for rinsing the test solution completely
into the analyzed site (groundwater or open water) is followed by the
extraction of the test solution-water mixture from the same site
after a defined reaction time, i.e., the time between injection and
retrieval. The test solution contains a conservative tracer (sodium
ions) and the reactant (sulfide). The conservative tracer is not
changed by a spontaneous chemical reaction or by microbial activity and
serves to compensate for losses of the reactant by diffusion and
fluxes. In contrast, the reactant may be changed by both spontaneous
chemical reactions and by microbial activity. During the extraction
phase the concentrations of the reactant and the conservative tracer
are continuously monitored in a flow cell.
The first-order reaction rate of the reactant is calculated using the
simplified method of push-pull test data analysis by
fitting the
natural logarithm of the ratio of the relative recovered
concentrations
of the reactant to the tracer versus the time since
the injection ended
in accordance with the following equations
(
9):
|
(1)
|
|
(2)
|
where
k is the sulfide reaction rate (turnover rate)
for netto sulfide consumption (equation 1) or production (equation 2),
t* is the time since the end of injection,
tinj is the injection
time,
cR is the relative concentration of the reactant
(sulfide),
and
cT is the relative concentration
of the conservative tracer
(Na
+).
Because in the open-water system high concentrations of conservative
tracer and reactant have to be injected, the concentrations
of both
rise rapidly in the flow cell at the beginning of the
extraction phase.
As the flow cell is not always free of oxygen
at the beginning of the
extraction phase, only the data obtained
after pumping up the dead
volume of the tube and flow cell were
used for calculations. Therefore
the intercept on the
y axis (equations
1 and 2) is not
considered, and the sulfide turnover rate is calculated
with linear
regression by using the ratio of the relative sulfide
and sodium
concentrations versus the time since the injection
ended, as given by
|
(3)
|
where
k is the sulfide reaction rate for both
consumption (
k < 0) and production (
k > 0) and
b is the term of correction
for production or
consumption of sulfide during the injection
time and for
losses.
The largest amounts of reactant and conservative tracer are detected
after pumping up the dead volume of the system. In the
monimolimnion
the high background concentration of sulfide (reactant)
has to be
considered, and only sulfide concentrations which were
higher than the
background concentration were used for data
analyses.
This model does not require the solution of a flow or transport model.
With respect to the open-water system considered here,
the main
assumptions are that the volume of test solution is well
mixed within
itself, that the reactant shows a pseudo-first-order
kinetics, and that
the retardation factors of tracer and reactant
are identical. To
measure the sulfide turnover in the open water
of Lake Cadagno, the
test solution contained 3 to 15 g of Na
2S
· 9H
2O liter
1, 0.02 M Ti(III) citrate as the
antioxidant, and 6.05 g of Tris-HCl
buffer (pH 7.5 to 8)
liter
1. Water from the anoxic part of the lake was used
as the chaser.
The analytical instruments and the pump were placed on a
working
platform situated above the deepest point of the lake (Fig.
1).
To ensure that the injection and
extraction sites were the same,
the injection/retrieval tube was fixed
on an underwater buoy,
which was stabilized with cables and weights to
the bottom of
the lake.
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FIG. 1.
Installation for push-pull test experiments in Lake
Cadagno. 1, working platform; 2, underwater buoy; 3, tube; 4, distributor; 5, weight; 6, cable; 7, buoy stones.
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|
A homemade flow cell of polyvinyl chloride contained a pH electrode
(6.0202.100; Metrohm, Herisau, Switzerland), a sodium
electrode (Na61;
Schott Glaswerke, Mainz, Germany), a temperature
sensor (TF 185;
Wissenschaftlich-Technische-Werkstätten, Weilheim,
Germany), an
amperometric sulfide sensor (sulfide sensor type
II;
Analysenmesstechnik, Rostock, Germany) and a butyl rubber
septum for
sampling. Besides the flowthrough measurements, the
sulfide
concentration was determined potentiometrically after
sampling.
Two-milliliter samples were immediately stabilized with
an equal volume
of antioxidant solution (250 g of sodium salicylate,
65 g of
ascorbic acid, and 85 g of NaOH liter
1), and the
sulfide concentrations were measured with a sulfide
microelectrode
(ION-1MS and REF-1; Toepffer Lab
Systems).
During the retrieval phase of the push-pull experiments, samples for
protein, bacteriochlorophyll
a, and colorimetric sulfide
determination were collected and kept in the dark until
analysis.
Analytics.
Protein was determined with Folin reagent
(13), and bacteriochlorophyll a was measured by
absorption spectroscopy after extraction with acetone-methanol
(3).
Profiles of conductivity, oxygen, pH, temperature, and turbidity were
obtained with an Aqua-Check multisensor (water analyzer;
Perstop
Analytical Environmental) combined with a homemade turbidity
sensor
described by Egli et al. (
5). Vertical sampling in the
layer
with high spatial resolution for determining concentrations
of protein,
bacteriochlorophyll
a and sulfide in the redoxcline
was done
with a syringe sampler. The syringes were placed at intervals
of 10 cm
and were opened at the sampling site with compressed
air. For sulfide
determinations samples were fixed immediately
with 4% zinc acetate to
prevent oxidation and the sulfide was
determined later
spectrophotometrically (
8).
| |
RESULTS |
Chemical and biological profiles in Lake Cadagno.
Figure
2 shows typical profiles in Lake Cadagno
during summer stratification in 1997. Oxygen drops to zero below a
depth of about 10 m, and a redoxcline from oxic to anoxic
conditions is formed with increasing concentrations of sulfide towards
the bottom of the lake. At the redox boundary the turbidity is strongly
increased and large concentrations of bacteriochlorophyll a
are detected during the summer season. This indicates a dense layer of
anoxygenic phototrophic bacteria, dominated by C. okenii and
A. purpureus (5, 11, 15, 20). Gradients of
conductivity and temperature below 7 m in depth cause an increase
in the density of the water, which results in a stable stratification
of the lake. High-resolution profiles of sulfide show a steep gradient
in the redoxcline. Maximum sulfide concentrations are detected at the
lower edge of the redoxcline, with a decrease to 0 mM towards the top
of the bacterial layer. Thus, at maximum cell density often no sulfide
is detected (Fig. 3).
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FIG. 2.
Different profiles of Lake Cadagno (17 September 1997, morning). Profiles for conductivity ( ), oxygen ( ), temperature
( ), turbidity ( ), and pH ( ) are shown.
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FIG. 3.
High-resolution profiles (22 July 1998, afternoon) of
bacteriochlorophyll a (), protein (), and sulfide
() in the redoxcline.
|
|
Sulfide turnover rates.
The first push-pull experiments were
done at the lower part of the bacterial layer to ensure absolute anoxic
experimental conditions. In the absence of oxygen, sulfide turnover
rates will mainly originate from biological activities. Interestingly,
at this depth, which receives only small amounts of light, both sulfide production and sulfide consumption have been measured at different times during the day (Fig. 4 and
5). In contrast, during the night, sulfide turnover rates were always positive, indicating sulfide formation.
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FIG. 4.
(Left) Breakthrough curve during the extraction (19 September 1997). Conditions: 600-ml test solution; pump rate during
retrieval, 40 ml · min1. (Right) Tracer
(Na+) and reactant (S2) breakthrough curves
during the extraction phase (19 September 1997). Conditions: 600-ml
test solution; pump rate during retrieval, 40 ml · min1.
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FIG. 5.
(Left) Breakthrough curve during the extraction phase (6 October 1997). Conditions: 600-ml test solution; pump rate during
retrieval, 40 ml · min1. (Right) Tracer
(Na+) and reactant (S2) breakthrough curves
during the extraction phase (6 October 1997). Conditions: 600-ml test
solution; pump rate during retrieval, 40 ml · min1.
|
|
For a better understanding of the dynamics of the sulfur cycle in situ,
sulfide turnover profiles were obtained at different
times of the day
and at different depths. Results from different
depths are presented in
Table
1. During the day, at the site
of
maximum bacterial density all sulfide turnover rates were negative,
i.e., they showed net sulfide consumption. Rates ranged from
0.93
to
23.48 h
1, indicating the high variability in the extent
of anoxygenic
photosynthesis. Both the bacteriochlorophyll
a
concentrations
and the specific bacteriochlorophyll
a
content (bacteriochlorophyll
a/protein ratio) were highest
at this depth in the lake.
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TABLE 1.
Results of different push-pull test experiments in the
redoxcline, redoxcline/monimolimnion boundary, and in
the monimolimnion
|
|
At the lower edge of the redoxcline towards the monimolimnion, both
positive and negative sulfide turnover rates were observed,
showing
sulfide production and sulfide consumption rates ranging
from
3.04 to
+3.86 h
1. On average, the specific bacteriochlorophyll
a content was about
10 times smaller than the one at the
maximum turbidity, indicating
a change from mainly phototrophs to
heterotrophic bacteria with
increasing depth. In the monimolimnion only
positive sulfide turnover
rates were calculated, indicating sulfide
production also during
the day, as essentially no light reaches this
depth to drive anoxygenic
photosynthesis. Rates ranged from +0.87 to
+3.35 h
1. The specific bacteriochlorophyll
a
contents were similar to
the ones at the lower edge of the
redoxcline.
Results obtained during the daily cycle for the mixolimnion, the layer
of maximum turbidity, and the monimolimnion are given
in Table
2. During daytime all experiments in the
oxic mixolimnion
resulted in a net sulfide consumption (
k < 0) due to spontaneous
oxidation of sulfide by the oxygen present.
Along the oxygen gradient
between 8 and 10 m (Fig.
2) the sulfide
turnover rates became
less negative, as less oxygen was present.
Negative rates increased
again in the zone of the phototrophic
bacteria.
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TABLE 2.
Results of different push-pull test experiments in the
mixolimnion, at the maximum turbidity in the redoxcline, and in
the monimolimnion
|
|
At maximum turbidity in the bacterial layer high rates of sulfide
consumption (
30.99 to
10.67 h
1) were measured during
the day. Because of the rapid decline of
the light intensity within the
bacterial layer (
7), sulfide
turnover rates below the
maximum cell density turned rapidly positive,
showing a net sulfide
production. As expected, in the night, only
the oxic mixolimnion gave
negative sulfide turnover rates due
to chemical sulfide oxidation. In
contrast, in the bacterial layer,
sulfide turnover rates were positive
because sulfide is produced
via the dark-adapted metabolism of the
phototrophic bacteria (
4,
21) as well as by the sulfate
reducers.
| |
DISCUSSION |
Oxidation and reduction processes of inorganic sulfur compounds in
nature are governed by both chemical and biological reactions. Besides
the linear reaction sequence from sulfide to sulfate and back,
compounds containing more than one sulfur atom are formed under certain
conditions. Thiosulfate is used as an electron donor by various purple
sulfur bacteria, and traces of thiosulfate are observed in the open
water, but also tri-, tetra-, and polythionates may be formed. Thus,
oxidation reactions starting from sulfide are diverse and complex and
yield different products (18).
Sulfide is spontaneously chemically oxidized with a half-time ranging
from 0.4 to 65 h. Millero and Hershey (14) determined a
50-h half-time in fresh water. Salts and increasing pH strongly accelerate the oxidation rate; metal ions, e.g., Ni2+ and
Co2+, may increase the rate by a factor of up to 1,000 (1).
To quantify the formation and consumption of sulfide as a key species
in anoxic environments, the push-pull technique was successfully
adapted for in situ measurements of its turnover in the open water of
the meromictic Lake Cadagno. The different processes, reduction to and
oxidation of sulfide in the sulfur cycle, take place at different
depths of the lake. In the mixolimnion sulfide is absent due to highly
oxic conditions (Fig. 2). Sulfide produced in the anoxic part of the
lake hardly reaches the oxicline, as a dense layer of mainly
phototrophic bacteria acts as a filter for sulfide. The photosynthetic
processes often lead to a complete sulfide depletion in the upper part
of the bacterial layer. Spontaneous oxidation of sulfide by oxygen may,
however, take place at the upper edge of the chemocline during the
turnover of the water of the mixolimnion in late autumn. Clouds of
dispersed elemental sulfur are often observed at sites closer to the
shore where the oxic water reaches the sediment surface
(12).
The layer of phototrophic bacteria can be separated into two zones. In
the top zone down to the maximum turbidity enough light is available
for bacterial photosynthesis (7). This results in high rates
of sulfide consumption during the day. During the night sulfide is
produced at the same sites in rates similar to the ones in the
monimolimnion at greater depth, giving evidence for sulfur respiration
and sulfate reduction in the layer dominated by the phototrophs. At the
lower edge of the bacterial layer, photosynthesis may still be possible
at high solar insolation, although only a small fraction of the
incident light penetrates to the lower part of the layer
(7). Sulfate reduction and elemental sulfur respiration are
here the dominant processes, similar to what is found in the deeper
regions of the monimolimnion. Within the bacterial layer the buoyant
density of the water has often been found to be nearly constant,
indicating that the density gradient is disturbed (see conductivity in
Fig. 2) (see the results in references 7, 11, and
12). Calculations indicate that 105 to
106 actively swimming cells per ml may liberate enough
energy to destroy the density gradient in the water. Under these
conditions bioturbation may occur (16), with the result that
the bacterial layer is in constant motion. This allows the bacteria to
become transported from lower to higher parts in the bacterial layer and to collect both light and electrons from sulfide.
In this paper turnover rates are given as relative rates with the
dimension of inverse hours. It would be of interest to convert these
rates into absolute values to normalize them for biomass and sulfide
concentration and to be able to compare them with available laboratory
data. Our data do not allow us to properly calculate such specific
oxidation and reduction rates. First, the actual sulfide concentration
varies within the layer and often in the upper part is below the
detection limit. Furthermore, although bacteriochlorophyll and total
protein concentrations have been determined, the biomasses of the
producers and the consumers of sulfide cannot be distinguished from
these data. The rates obtained are real in situ rates, which means that
they are determined by the actual values of light intensity, sulfide
concentration, cell concentration, ratio between phototrophic and
nonphototrophic cells, redox potential, temperature, pH, and more. As
most of these factors vary in the region of the bacterial layer, such calculations would have large uncertainties. In contrast, it may be
possible to convert absolute rates from laboratory experiments into
relative ones for the conditions of the experiment. Given the initial
rate of sulfide oxidation of a dense culture of Chlorobium at relatively high light intensity, we arrive at a turnover number of
about 40 h1, a value similar to the highest rates
obtained in situ (2). It is still unclear what is meant by
the turnover rates obtained by the pulse method at sites where the
sulfide concentration is below or near the detection limit. Are these
the potential rates at conditions when sulfide is not limiting, or are
these the actual in situ rates before the pulse? Under light-limiting
conditions in the lower part of the bacterial layer an increase in
sulfide concentration will probably not change the turnover rate, but in the upper part of the bacterial layer sulfide may really be the
rate-limiting parameter. If so, the measured rates are instead maximum
rates under sulfide-saturated conditions at the available light intensity.
| |
ACKNOWLEDGMENTS |
We thank D. Bollier and H. P. Schmidhauser for technical
assistance in the construction of the specific equipment and P. Bosshard and D. Grüter for their help in the field work. We
greatly acknowledge M. Schroth for his cooperation in data analyses.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Institut
für Pflanzenbiologie, Universität Zürich,
Zollikerstrasse 107, CH-8008 Zürich, Switzerland. Phone:
41-1-634-82-80. Fax: 41-1-634-82-04. E-mail:
bachofen{at}botinst.unizh.ch.
| |
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Applied and Environmental Microbiology, February 2000, p. 712-717, Vol. 66, No. 2
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Tonolla, M., Peduzzi, R., Hahn, D.
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Abstract
Introduction
