BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-19-4351-2022Rapidly increasing sulfate concentration: a hidden promoter of
eutrophication in shallow lakesRapidly increasing sulfate concentrationZhouChuanqiaoPengYuChenLiYuMiaotongZhouMuchunXuRunzeZhangLanqingZhangSiyuanXuXiaoguangxxg05504118@163.comZhangLiminWangGuoxiangJiangsu Key Laboratory of Environmental Change and Ecological Construction, Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, School of Environment, Nanjing Normal University, Nanjing 210023, ChinaChina Aerospace Science and Industry Nanjing Chenguang Group, Nanjing 210022, ChinaSchool of Energy and Environment, Southeast University, Nanjing
210096, China
Except for excessive nutrient input and climate warming, the rapidly rising
SO42- concentration is considered as a crucial contributor to the
eutrophication in shallow lakes; however, the driving process and mechanism
are still far from clear. In this study, we constructed a series of
microcosms with initial SO42- concentrations of 0, 30, 60, 90, 120,
and 150 mg L-1 to simulate the rapid SO42- increase in Lake Taihu, China,
subjected to cyanobacteria blooms. Results showed that the sulfate reduction
rate was stimulated by the increase in initial SO42-
concentrations and cyanobacteria-derived organic matter, with the maximal
sulfate reduction rate of 39.68 mg (L d)-1 in the treatment of 150 mg L-1 SO42- concentration. During the sulfate reduction, the
produced maximal ∑S2- concentration in the overlying water and
acid volatile sulfate (AVS) in the sediments were 3.15 mg L-1 and 11.11 mg kg-1,
respectively, and both of them were positively correlated with initial
SO42- concentrations (R2=0.97; R2=0.92). The
increasing abundance of sulfate reduction bacteria (SRB) was also linearly
correlated with initial SO42- concentrations (R2=0.96),
ranging from 6.65×107 to 1.97×108 copies g-1.
However, the Fe2+ concentrations displayed a negative correlation with
initial SO42- concentrations, and the final Fe2+
concentrations were 9.68, 7.07, 6.5, 5.57, 4.42, and 3.46 mg L-1, respectively.
As a result, the released total phosphorus (TP) in the overlying water, to promote the
eutrophication, was up to 1.4 mg L-1 in the treatment of 150 mg L-1
SO42- concentration. Therefore, it is necessary to consider the
effect of rapidly increasing SO42- concentrations on the release
of endogenous phosphorus and the eutrophication in lakes.
Introduction
Nowadays, cyanobacteria blooms in eutrophic lakes have become one of the most
serious problems in freshwater lakes all over the world (Iwayama et al.,
2017; Ho et al., 2019). Phosphorus, as a necessary nutrient for biological
growth, is considered to be one of the main limiting factors of lake
eutrophication (Ni et al., 2020). In recent years, the input of exogenous
phosphorus has been effectively controlled, while the release of endogenous
phosphorus is still an urgent problem in eutrophic lakes (Liu et al., 2018;
Guo et al., 2020). The release of endogenous phosphorus is affected by many
factors, such as wind and waves and the cyanobacteria decomposition (Xu et
al., 2018; Zhao et al., 2019). There are many forms of phosphorus in
freshwater lake sediments, including aluminum bound phosphorus (Al-P), iron
bound phosphorus (Fe-P), etc. Among them, Fe-P, formed under the condition
of high dissolved oxygen (DO), is the most active form of phosphorus in the
sediments, which has a more obvious response to the change in DO (Zhang et
al., 2020). The accumulation and decay of cyanobacteria in eutrophic lakes
will change the physical and chemical environments of the water body and form
anaerobic reduction conditions (Yan et al., 2017). This will facilitate the
reduction of iron oxides and lead to the desorption and release of Fe-P in
sediments, resulting in the increase in endogenous phosphorus release (Zhao
et al., 2019).
Iron reduction plays an important role in natural ecosystems. It has been
reported that dissimilatory reduction of iron accounts for 22 % of the
total amount of organic matter anaerobic mineralization in offshore areas
(Thamdrup et al., 2004). According to the classical theory, iron oxides or
hydroxides can adsorb phosphorus in the water and form Fe-P precipitation
(Gunnars and Blomqvist, 1997). In freshwater lakes, the lack of Fe(III) content or
the diagenesis of organic phosphorus may be the reason for the lack of
phosphorus in the overlying water. Therefore, the formation of iron oxides
on the surface of sediments is closely related to the phosphorus cycle
process (Amirbahman et al., 2003; Chen et al., 2014). The interaction
between iron and phosphorus is reflected in the effect of adsorption and
desorption of Fe oxide on the phosphorus content in the overlying water, since Fe-P
is the main internal source of phosphorus (Wu et al., 2019). Iron oxides can
be used as both the source and destination of phosphorus in lake ecosystems
(Mort et al., 2010; Azam and Finneran, 2014). In anaerobic reduction environments,
iron reduction can significantly promote the resolution of Fe-P. The
Fe2+ generated by the reaction can form solid FeS with soluble sulfide.
In addition, free Fe3+ will combine with humus to form a stable
complex, which further prevents the co-precipitation process of phosphorus
and iron oxides (Mort et al., 2010; Zhang et al., 2020). Therefore, the iron
reduction process driven by cyanobacteria decomposition affects the
circulation of phosphorus in freshwater lakes.
Due to the SO42- concentration in seawater reaching 28 mM, the sulfate
reduction process with the participation of sulfate reduction bacteria (SRB)
has received considerable attention in the basic material cycle of marine
biogeochemistry (Fike et al., 2015; Pan et al., 2020). In freshwater lakes,
the SO42- concentration is less than 800 µM, which is
generally considered insufficient for continuous sulfate reduction (Hansel
et al., 2015). However, in recent years, with the continuous input of
exogenous sulfur, the SO42- concentration in freshwater lakes
increases significantly, and the degree of the eutrophication and the
SO42- concentration show a positive correlation (Dierberg et al.,
2011; Yu et al., 2013). For instance, the SO42- concentration in
Lake Taihu, China, one of the typical eutrophic lakes, has increased from
30 to 100 mg L-1 in the past 70 years, and it will continue to rise in the
future (Yu et al., 2013; Zhou et al., 2022). The impact of sulfate reduction
on the material cycle of lake ecosystems may be far beyond our knowledge
(Baldwin and Mitchell, 2012; Yu et al., 2013). On the other hand, it has been
reported that the sulfate reduction process is one of the important ways of
anaerobic metabolism of organic matter in freshwater lakes, and ∑S2- produced by the sulfate reduction process can mediate the iron
reduction process (Jorgensen et al., 2019; Zhang et al., 2020). SRB mainly
use SO42- as the electron acceptor to complete anaerobic
respiration, and the sulfur compounds produced by anaerobic metabolism are
bound with iron and so on, which are fixed in the sediments and form AVS on
the surface of sediments (Holmer and Storkholm, 2001; Chen et al., 2016).
Therefore, with the input of exogenous sulfur,
∑S2- produced through the sulfate reduction process will further promote iron reduction in freshwater
lakes.
In freshwater lakes, the iron cycle affects the process of the phosphorus cycle, and the
sulfur cycle plays an important role in regulating the iron cycle. Therefore,
the cycle of iron, sulfur, and phosphorus in freshwater lakes is inseparable
(Wu et al., 2019; Zhao et al., 2019). Studies have shown that even when
SO42- content was as low as 20 mg L-1, the anaerobic metabolism of
organic substrates was still dominated by sulfate reduction. Therefore,
the sulfate reduction process plays an important role in the lacustrine
biochemical cycle (Hansel et al., 2015). In the absence of cyanobacteria,
sulfate reduction does not occur even if the SO42- concentration is
higher (Zhao et al., 2021). This is because the accumulation and
decomposition of cyanobacteria not only change the environment of the water
body but also release a large amount of organic matter, which provides the
necessary conditions for the circulation of iron, sulfur, and phosphorus (Yan
et al., 2017; Melemdez-Pastor et al., 2019). Therefore, under the co-effect
of the increase in SO42- and the cyanobacteria decomposition, the
sulfate reduction process and the effect of the iron reduction process on
endogenous phosphorus release from sediments need to be further studied.
In this study, a series of different initial concentrations of
SO42- were set according to the variation trend of SO42-
concentrations over the years and the possible rising trend in the eutrophic
Lake Taihu. The effects of increased SO42- concentration and
cyanobacteria bloom on sulfate reduction coupled with the microbial
processes were investigated. The dynamic changes in Fe2+ and Fe3+
concentrations during iron reduction were studied in order to reveal the
effect of sulfate reduction on iron reduction. In addition, the dynamic
changes in phosphorus in the overlying water and sediment were investigated.
Finally, the coupled sulfate, iron, and phosphorus cyclic processes affected
by the increasing sulfate concentration and cyanobacteria bloom were also
comprehensively analyzed for elucidating the phosphorus release dynamics
to tracking the hidden promoter of cyanobacteria blooms in eutrophic lakes.
The findings may be beneficial for evaluating the effect of sulfate reduction
in freshwater lakes and its impact on the promotion of iron reduction and
the release of endogenous phosphorus.
Materials and methodsSample collection and preparation
Lake Taihu (31∘24′40′′ N, 120∘1′3′′ E) is one of the
largest eutrophic shallow lakes in China, with an average depth of 2.4 m and
an area of 2340 m2 (Mao et al., 2021). In this study, samples of
sediments and cyanobacteria were collected in July 2020. Sediments (0–20 cm)
from the west shoreline of the lake (31∘24′45′′ N, 120∘0′42′′ E) were collected using a gravity core sampler (length of 150 cm and
diameter of 20 cm). Cyanobacteria was collected and concentrated by sieving
water through a fine-mesh plankton (250 mesh). All the sediment and
cyanobacteria samples were stored in an incubator with ice packs and
delivered to the laboratory immediately. The sediment samples were blended
thoroughly, homogenized, and sieved (100 mesh) to the polyethylene bag. The
cyanobacteria samples were flushed and centrifuged at 1500 rpm for 5 min
by a CT15RT versatile refrigerated centrifuge (China) and freezed dried by
Biosafer-10A. Different gradient sulfate concentrations were prepared from
the high-purity water and Na2SO4.
Setup of incubation microcosms
To simulate the dramatic SO42- increase and cyanobacteria blooms
of eutrophic Lake Taihu, a series of microcosms were constructed in this
study. According to the ratio of surface sediments and the average water
depth and the cyanobacteria accumulation density of 2500 g m-2 during
the breakout of cyanobacteria blooms of Taihu Lake, 100 g of sediment, 200 mL of water, and 0.11 g of cyanobacteria powder were added into each bottle
(Zhang et al., 2020). Meanwhile, according to the change trend of
SO42- concentrations in Taihu Lake over the years and the
possibility of further increase in the future (Yu et al., 2013), the
SO42- concentrations in six microcosm systems were configured as
30, 60, 90, 120, and 150 mg L-1, as well as a control without SO42-. The microcosm system adopted anaerobic bottles (Φ75 mm,
length 180 mm, volume 500 mL) as the reaction device. There were three
replicates in each SO42- concentration experimental group. Each
group was sampled 17 times after 1, 2, 3, 4, 5, 6, 7, 9, 11, 14, 18, 23, 28,
33, 38, 43, and 48 d. Totally, there were 306 anaerobic bottles, and all the
anaerobic bottles were placed in a biochemical incubator at a temperature of
25∘C. The water, gas, and soil samples were collected by destructive
sampling; that is, at each sampling point, 18 anaerobic bottles were opened
for testing, which ensured the anaerobic environment and air pressure for
other bottles. A part of sediment was used for microbe determination and
kept in a refrigerator at -80∘C, and the rest of the sediment and other
samples were kept at 0–4∘C for less than 24 h before analysis.
Chemical analytical methods
All water samples were filtered through 0.45 µm Nylon filters.
Dissolved total phosphorus (DTP) was determined by colorimetry after
digestion with K2S2O8+ NaOH, and the ammonium molybdate and
ascorbic acid were used as chromogenic agents (Ebina et al., 1983). Water
DO and oxidation and reduction potential were measured using calibrated
probes (MP525, China) during destructive sampling. The SO42- was
detected using the turbidimetric method with the stabilizer of BaCl2
and gelatin (Tabatabai, 1974), and the ∑S2- was detected
by methylene blue (Cline et al., 1969). Fe2+ and Fe3+ were
determined by colorimetric analysis (Phillips and Lovely, 1987). The sediment total
phosphorus (TP) was extracted and determined by colorimetry (Ruban et al.,
2001). The schematic diagram of the method to test acid volatile sulfate
(AVS) is shown in Fig. S5 in the Supplement; briefly, 5 g of sediment was put into a 250 mL
glass flask, and inside a small beaker with 15 mL of ZnAc2⚫ 2H2O and NaAc ⚫ 3H2O was used to absorb H2S gas.
The tube A was connected by N2 for 5 min in order to discharge the air in the bottle from pipe B, and then the valves of tubes A and B were closed. A total of 2 mL ascorbic acid solution was added to prevent S2- oxidation,
and then 15 mL (6 mol L-1) of hydrochloric acid was added with the reaction at
room temperature for 18 h. AVS was determined by the zinc cold diffusion method
(Hsieh and Shieh, 1997).
Quantification of SRB in sediments
In order to confirm the changes in sediment SRB in the microcosms, quantitative reverse transcription polymerase chain
reaction (RT-qPCR)
technologies were used to determine the cell copy numbers of methane-producing archaea (MPA) and SRB after
0.7 and 38 d in the sediments.
The sediment samples were collected and frozen at -80∘C in an
ultra-low-temperature freezer. The E.Z.N.A.® Soil DNA Kit
(Omega Bio-Tek, Norcross, GA, USA) was used to extract the total genomic DNA
from each soil sample according to the manufacturer's instructions. Nucleic
acid quality and concentration were determined by 1 % agarose gel
electrophoresis and NanoDrop 2000 UV spectrophotometer (Thermo Scientific,
USA), respectively.
SRB in sediments were quantified using the quantitative polymerase chain
reaction (qPCR) method. The qPCR with primer sets targeting DSR1F+
(5′-ACSCACTGGAAGCACGGCGG-3′) and DSR-R (5′-GTGGMRCCGTGCAKRTTGG-3′) was
used for the SRB in this study. The qPCR experiments were performed on a
ABI7300 qPCR instrument (Applied Biosystems, USA) using ChamQ SYBR Color
qPCR Master Mix as the signal dye. Each 20 µL reaction mixture
contained 2 µL of the template DNA and 16.5 µL of ChamQ SYBR Color
qPCR Master Mix. Standard curves for each gene were obtained by the 10-fold
serial dilution of standard plasmids containing the target functional gene.
All operations followed the Minimum Information for Publication of Quantitative Real-Time PCR Experiments (MIQE) guidelines.
Statistical analysis
The Statistical Package of the Social Science 18.0 (SPSS 18.0) was used for
statistical analysis. The one-way analysis of variance (ANOVA) and
correlation analysis were carried out using bivariate correlations analysis.
ResultsFe2+ and Fe3+ dynamics in overlying water
The concentration variations of Fe2+ and Fe3+ in overlying water
during the incubation are presented in Fig. 1. In the treatment without
SO42-, they increased continuously to 9.68 and 10.15 mg L-1,
respectively. The concentration of Fe3+ in the remaining five
treatments decreased at the beginning and then increased to keep stable. The
higher the initial sulfate concentration was, the lower the final Fe3+
concentration was. In the initial 150 mg L-1 SO42-
concentration treatment, the final Fe3+ concentration was the lowest at
7.7 mg L-1. The Fe2+ concentration in the five treatments supplemented
with SO42- decreased significantly from 11 to 23 d and then
increased to a stable level. The final concentration of Fe2+ also
showed a negative correlation with the initial concentration of
SO42-. In the initial 30 mg L-1 SO42- concentration
treatment, the final Fe2+ concentration was the highest at 7.07 mg L-1.
The concentration variations of Fe2+ and Fe3+ in the
water column during the incubation.
SO42- and ∑S2- dynamics in overlying water
All treatments had an obvious sulfate reduction reaction, and the concentration
of SO42- decreased greatly except for the treatment without adding
SO42- (Fig. 2). The higher the initial sulfate concentration was,
the faster the sulfate reduction rate in the initial stage was
(Table 1). In the treatment with initial SO42- concentration of 150 mg L-1, the sulfate reduction rate was 39.68 mg (L d)-1, while it was
only 9.39 mg (L d)-1 in the 30 mg L-1 SO42- treatment. The
sulfate reduction rate at the beginning of other treatments was also
positively correlated with the initial SO42- concentration.
The higher the initial SO42- concentration was, the higher the
maximum concentration of ∑S2- was. In the treatment with initial
SO42- concentration of 30 mg L-1, the lowest concentration was 2.93 mg L-1 on the fifth day. However, the lowest SO42- concentration
appearing on the 23rd day was 1.18 mg L-1 in the treatment with the initial
SO42- concentration of 150 mg L-1. The maximum concentration of
∑S2- was positively correlated with the initial SO42-
concentration. In the initial SO42- concentrations of 30, 60, 90,
120, and 150 mg L-1 SO42- treatments, the highest ∑S2-
concentrations at 7 d were 0.61, 1.14, 1.55, 2.15, and 3.15 mg L-1,
respectively.
Sulfate reduction rate in the water column of microcosms
(mg (L d)-1).
The concentration variations of SO42- and ∑S2- in the water column during the incubation.
TP dynamics in overlying water and sediments
The dynamics of DTP concentrations in overlying water during the incubation
are presented (Fig. 3a). The concentrations of DTP in overlying water
were positively correlated with the initial SO42-. The higher the
initial concentrations of SO42- were, the higher the
concentrations of DTP in overlying water were. On day 11, DTP in overlying
water continued to rise and then kept stable. The highest DTP concentration
was 2.08 mg L-1 in the treatment with the initial SO42- concentration of
150 mg L-1, while the highest DTP concentration was 0.36 mg L-1 in the treatment
without SO42- addition.
The concentrations of TP in the sediments increased significantly in all
treatments with the cyanobacteria decomposition in the initial stage (Fig. 3b). Among all treatments, on the ninth day, the highest concentration
of TP in the sediments was 887.69 mg kg-1 in the treatment with the initial
SO42- concentration of 0 mg L-1. After 23 d, TP in the sediments
decreased significantly and then stabilized. During cyanobacteria
decomposition and sulfate reduction, the concentrations of TP in all
treatments negatively correlated with the initial SO42-
concentration. The final TP concentrations were 448.92, 335.32, 321.56,
259.32, 238.56, and 227.21 mg kg-1 in all treatments.
The concentrations of TP in the overlying water (a) and
sediments (b) during the incubation.
AVS dynamics in the sediments
The concentrations of AVS in the sediments were positively correlated with
the initial SO42- concentrations. With the increase in TP in
overlying water, the AVS in the sediments also increased steadily and
reached the peak on the 11th day. In the treatments with the initial
SO42- concentrations of 0, 30, 60, 90, 120, and 150 mg L-1, the
highest concentrations of AVS in the sediments were 7.21, 7.99, 8.54, 8.99,
9.34, and 11.11 mg kg-1, respectively.
The concentration of AVS in the sediments during the incubation.
SRB dynamics in the sediments
During the decomposition of cyanobacteria, the SRB abundance significantly
increased compared with the initial stage (P<0.01). In the initial stage, the
SRB abundance was 1.09×108 copies g-1 and the final value was
positively correlated with the initial SO42-. On day 7, SRB of all
treatments showed a downward trend compared with the initial value, and
there was no significant difference in SRB values between each treatment. On
day 38, except for the initial SO42- concentrations of 0 and 30 mg L-1, SRB increased significantly in other treatments.
Discussion
It is generally acknowledged that climate warming and exogenous nutrient
input are the important contributors to the occurrence of cyanobacteria
blooms (Anneville et al., 2015; Yan et al., 2017). However, in this study,
we found that the dramatically increasing SO42- concentration in
eutrophic lakes is also a non-negligible promoter for the self-sustainment of
cyanobacteria blooms. In eutrophic lakes, the decomposition of cyanobacteria
consumed DO in the water and formed strong anaerobic reduction conditions
(Fig. S1). Fe-P was desorbed to form free Fe3+, which was reduced to
Fe2+ in anaerobic environments (Fig. 1). Free Fe2+ combined with
∑S2- which was generated by sulfate reduction and eventually formed
AVS fixed in the sediments (Fig. 4), and phosphorus was released from the
sediments (Fig. 3). It has been reported that SRB and iron reduction bacteria
(IRB) are the main microorganisms that drive sulfate reduction and iron
reduction, respectively, and cyanobacteria decomposition promotes these
microorganisms' growth (Wu et al., 2019). Consistent with these results, our
findings also revealed that cyanobacteria released large amounts of organic
matter to promote microbial growth during their decay and decomposition
(Fig. S2, Table 2) and ultimately promoted anaerobic reduction of sulfur and
iron (Holmer et al., 2001). Therefore, with increasing SO42-
concentrations in eutrophic lakes, the influence of sulfate reduction on
phosphorus release is worth further investigation.
Copy numbers of the dsrB gene of SRB in the sediments during the
incubation (copies g-1).
Correlation of initial SO42- concentrations with ∑S2-(a), AVS (b), sulfate-reducing bacteria (SRB) (c), and TP (d) in the
microcosm systems.
A simplified scheme of the relationship among climate warming,
lake eutrophication, and cyanobacteria blooms in eutrophic lakes. Under
climate warming scenarios, extreme abiotic and biotic conditions facilitated
the breakout of cyanobacteria blooms. After their collapse, the high amount
of N, P, and C were released into the overlying water and reacted with the
eutrophication. Furthermore, a large amount of CH4 and CO2 was
produced and emitted to the atmosphere, contributing to global warming from
freshwater lakes (Yan et al., 2017). With the external sulfur input, the
concentration of SO42- increased significantly, and sulfate
reduction was enhanced. The cyanobacteria decomposition created an anaerobic
reduction environment, which will promote iron reduction and sulfate
reduction. The free Fe3+ generated by Fe-P desorption was reduced to
Fe2+ and combined with ∑S2-, which through sulfate
reduction formed stable Fe-S in the sediments. Phosphorus was released from
the sediment into the overlying water. Therefore, there are three vicious
loops between cyanobacteria bloom occurrence, lake eutrophication, and
climate warming.
The iron, sulfur, and phosphorus cycles are inseparable in lake sediments (Zhang et al., 2020). With the increase in
SO42- concentration in eutrophic lakes, the effect of sulfate
reduction on phosphorus release from sediments may be more important than
previously recognized (Pester et al., 2012). Sulfate reduction driven by SRB
is an important organic metabolism pathway in natural systems. During the
sulfate reduction process, SO42- is an electron acceptor, and its
concentration variation can significantly affect the sulfate reduction rate
(Holmer and Storkholm, 2001; Nakagawa et al., 2012). SO42- is reduced to
∑S2- by acquiring the electrons supplied by SRB oxidation, and
thus SRB play an important role in sulfate reduction (Sela-Adler et al.,
2017). The increase in SO42- concentration promotes the SRB
abundance, as evidenced by a positive correlation (Wu et al., 2019). In the
case of increased SRB abundance (Table 2) and increased SO42-
concentration, the sulfate reduction reaction was enhanced. The
SO42- concentration in the overlying water decreased significantly
accompanied by a temporary increase in ∑S2- (Fig. 2). The highest
concentrations of ∑S2- also increased with the initial
SO42- concentrations (Fig. 5a). Interestingly, the ∑S2-
decreased rapidly after day 10 to almost zero at the end (Fig. 2). This may
result from two key factors: (a) hydrogen sulfide overflows from the incubator, and s
(b) sulfide migrates downward and combines with other substances in the
sediment and is immobilized (Zhang et al., 2020). In this study, TP in the
overlying water has a significant positive correlation with the initial
SO42- concentrations (R2=0.96; Fig. 3). The classical
theory presumes that iron reduction by IRB leads to the release of
iron-bound phosphorus in the anaerobic layer of sediments, and when the
formed Fe2+ enters the aerobic water layer, it is oxidized by
Fe3+ and bound to phosphorus again (Roden, 2006; Chen et al.,
2016). When the sulfate reduction process mediates the iron reduction
process, the released Fe2+ combines with the product ∑S2- of
sulfate reduction to form Fe-S, thus weakening the reoxidation process of
Fe2+ and increasing the release of phosphorus (Mort et al., 2010; Zhao
et al., 2019). Therefore, with the increase in SO42-
concentrations in eutrophic lakes, it significantly promoted the release of
endogenous phosphorus from the sediments.
From a thermodynamic point of view, iron reduction should take
precedence over sulfur reduction (Han et al., 2015). However, due to
chemical kinetics, sulfur reduction occurs before iron reduction, resulting
in the simultaneous appearance of ∑S2- and iron oxides (Han et
al., 2015; Hansel et al., 2015). This is consistent with the concentration
variation of iron and sulfur in this study (Figs. 1–3). It has been reported
that iron cycles in the water body will produce an intense response to the
accumulation of sulfide; that is, sulfate reduction can promote iron
reduction (Friedrich and Finster, 2014; Zhang et al., 2020). ∑S2- is
the final product of sulfate reduction, which is toxic to microorganisms and
easy to combine with heavy metals such as Fe2+ to form AVS in lake
sediments (Holmer et al., 2001). In this study, the concentration of AVS
showed a significant positive correlation with the initial concentration of
SO42- (Figs. 4, 5b), which was consistent with the highest
concentration of ∑S2- observed in the overlying water (Figs. 2,
5c). The concentrations of Fe2+ and Fe3+ in the overlying water
increased significantly, and Fe2+ significantly decreased in the middle
of the incubation (Fig. 1), suggesting that Fe2+ reduced by sulfate can
be combined with the product ∑S2- (Fig. 2). These results
are consistent with the trend that AVS in the sediments reached a peak after 11 d and ∑S2- in the water decreased rapidly after 9 d and
remained at a lower concentration (Figs. 2, 3). The reason for this
phenomenon may be the formation of Fe-S compounds that are finally fixed in
the sediments (Zhao et al., 2019).
The ∑S2--mediated iron chemical reduction may lead to more
environmental effects, such as phosphorus mobilization (Zhang et al., 2020).
For instance, a previous investigation on the lakes along the Yangtze River
demonstrates that the effects of endogenous phosphorus release is probably
related to the increase in SO42- concentration (Chen et al.,
2016). In this study, the concentration of Fe2+ in the treatment
without SO42- continued to rise and was up to the highest
concentration among all treatments (Fig. 1). In contrast, the concentrations
of TP in the treatment without SO42- showed the lowest
concentration among all treatments (Figs. 1, 5a). This is caused by Fe2+
and Fe3+ recombining with phosphorus and being immobilized in the
sediments (Wu et al., 2019). In general, iron combines with phosphorus to
form siderite (FePO4⚫ 2H2O) and blue iron
(Fe3(PO4)2⚫ 8H2O) and is bound to the
sediments (Taylor and Konhauser, 2011). However, when precipitation or reduction
separates iron from iron phosphate minerals, phosphorus bound to iron is
released (Gu et al., 2016).
In order to further elucidate whether the increasing SO42-
concentrations in overlying water result in the self-sustainment of
eutrophication in shallow lakes, a conceptual diagram was put forward (Fig. 6). It has been accepted that exogenous nutrient inputs and climate warming
have positive effects on the breakout of cyanobacteria blooms. With the
continuous input of exogenous sulfur, the SO42- concentration in
the lake water increases significantly. When cyanobacteria blooms start to
decay, the overlying water shifts from the aerobic state to the strong
anaerobic state, providing a carbon source to promote the growth of
microorganisms such as SRB. The increasing SO42- concentrations
provide the electron for the sulfate reduction process, resulting in the
sulfate reduction and the release of a large amount of ∑S2-. The
Fe2+ released from the iron reduction process is captured by ∑S2-, and finally the combination of iron and phosphorus was reduced, promoting
the release of endogenous phosphorus. Therefore, it is necessary to pay
attention to the effect of enhanced sulfate reduction on endogenous
phosphorus release in eutrophic lakes.
Conclusion
The dramatic increase in SO42- concentration was up to more than
100 mg L-1 in eutrophic lakes. There was a coupling relationship between
sulfur, iron, and phosphorus cycles in lake ecosystems. The rapidly increasing
sulfate concentration enhanced the sulfate reduction to release a large
amount of ∑S2- mediated by the increasing abundance of SRB with
the adequate organic source from the decay processes of cyanobacteria
blooms. The iron reduction showed a positive relationship with the initial sulfate concentrations during the cyanobacteria decomposition. The Fe2+ released from
the iron reduction process was captured by ∑S2-, and finally the
combination of iron and phosphorus was reduced, promoting the release of endogenous
phosphorus. Therefore, except for climate warming and excessive nutrients,
the increasing sulfate concentration has been proven to be another hidden promoter
of eutrophication in shallow lakes.
Data availability
The data used in this paper can be accessed by contacting the first author (chuanqiaozhou@163.com) based on a reasonable request.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-19-4351-2022-supplement.
Author contributions
XX designed and led the study. CZ, YP, LC, MY, MZ, RX, LaZ, and SZ performed the investigation and analyzed the samples. CZ and YP wrote the original draft with major edits and inputs from XX, LiZ, and GW.
Competing interests
The contact author has declared that none of the authors has any competing interests.
Disclaimer
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Acknowledgements
We thank the editors and the anonymous referees for their insightful comments which substantially improved this paper.
Financial support
This work was supported by the National Natural Science Foundation of China
(grant nos. 42077294, 41877336, 41971043), the Cooperation and Guidance Project of
Prospering Inner Mongolia through Science and Technology (grant no. 2021CG0037),
the National Key Research and Development Program of China
(grant no. 2021YFC3200304), and the Guangxi Key Research and Development Program of
China (grant no. 2018AB36010).
Review statement
This paper was edited by Aninda Mazumdar and reviewed by four anonymous referees.
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