Water Research 217 (2022) 118441

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Water Research
journal homepage: www.elsevier.com/locate/watres

Sulfate concentrations affect sulfate reduction pathways and methane

consumption in coastal wetlands
Wei La a, Xiaokun Han a, b, c, Cong-Qiang Liu a, b, c, Hu Ding a, b, c, Mingxuan Liu a,
Fusheng Sun a, b, c, Siliang Li a, b, c, Yunchao Lang a, b, c, *
a
Institute of Surface-Earth System Science, School of Earth System Science, Tianjin University, Tianjin 300072, China
b
Tianjin Key Laboratory of Earth Critical Zone Science and Sustainable Development in Bohai Rim, Tianjin University, Tianjin 300072, China
c
Critical Zone Observatory of Bohai Coastal Region, Tianjin University, Tianjin 300072, China

A R T I C L E I N F O A B S T R A C T

Keywords: Coastal wetlands are an important source of methane emissions, and understanding the mechanisms that control
Methane methane emissions from coastal wetlands is of great significance to global warming. Anaerobic oxidation of
Sulfate reduction methane driven by sulfate is an important process to prevent methane emissions from coastal wetlands. The
Anaerobic oxidation of methane
effects of environmental changes on this process and the function of the sulfate-methane transition zone (SMTZ)
Coastal wetlands
are poorly understood. In this study, spatiotemporal variations in pore-water geochemistry (concentrations of
Sulfate-methane transition zone
SO42-, CH4 and DIC as well as δ13C-DIC and δ13C-CH4) in the Beidagang wetland, Tianjin, China, were investi­
gated to unravel factors controlling the role of anaerobic oxidation of methane in coastal wetlands. Results show
that the geochemical profile of pore-water is characterized by significant spatial and temporal variability, which
may be related to changes in sulfate concentration, temperature and dissolved oxygen. The carbon isotope
fractionation factors (εC) during methane oxidation range from 8.9‰ to 12.5‰, indicating that the sulfate-driven
anaerobic oxidation of methane (S-AOM) dominates the methane oxidation in the Beidagang coastal wetland in
both winter and summer, in both high and low salinity wetlands, and in both open water and littoral areas.
However, sulfate concentration has a strong influence on the sulfate reduction pathways and methane con­
sumption. The consumption of methane and sulfate by S-AOM is more significant in coastal wetlands with high
sulfate concentrations, with S-AOM consuming nearly all of the upward-diffusing methane (96%) and
downward-diffusing sulfate (96%). In addition, the dissolved inorganic carbon (DIC) produced in the pore-water
mainly comes from methanogenesis, accounting for more than 80% of the total DIC pool, but in the areas with
high sulfate concentrations in water column, the contribution of S-AOM to the DIC pool is greater, although only
a small fraction of the total DIC pool (9%). The depth and width of the SMTZ show a clear spatial and temporal
pattern, with active methanogenesis activity and upward high methane flux shoaling the SMTZ and increasing
the risk of high methane emissions from coastal wetlands with low sulfate concentrations. Our findings highlight
the importance of sulfate-driven anaerobic oxidation of methane in coastal wetlands and the effect of sulfate
concentration on it. It contributes to our understanding of the mechanism of methane production and emissions
from the coastal wetland system, particularly in light of the increased demand for coastal wetland restoration
under global warming.

1. Introduction
Methane (CH4) is an important greenhouse gas that plays a critical
role in climate change with a global warming potential of ~28–34 times
greater than that of CO2 on a hundred-year time scale (Myhre et al.,
2013; Stocker, 2014). Methane has contributed 20% to global warming
since the Industrial Revolution (Beaulieu et al., 2019). According to
recent model estimates, global methane emissions from 2008 to 2017
were 737 Tg CH4 yr− 1, with over 40% of these emissions being from
natural sources (Saunois et al., 2020). Natural wetlands are the largest
natural source (Hamdan and Wickland, 2016), accounting for nearly 1/3
of global methane emissions (Bridgham et al., 2013). Coastal wetlands
cover only about 0.3% of the earth’s surface (Mcowen et al., 2017;
Pendleton et al., 2012), but contribute 7% to 30% of annual global

* Corresponding author:
E-mail address: yunchao.lang@tju.edu.cn (Y. Lang).

https://doi.org/10.1016/j.watres.2022.118441
Received 20 January 2022; Received in revised form 24 March 2022; Accepted 7 April 2022
Available online 9 April 2022
0043-1354/© 2022 Elsevier Ltd. All rights reserved.
W. La et al.
methane emissions (Segarra et al., 2013). Marine environments make up
70% of the earth’s surface, but contribute only 1~2% of global methane
emissions (Wallenius et al., 2021; Weber et al., 2019), of which a sig­
nificant proportion (up to 75%) comes from coastal and estuarine en­
vironments (Hamdan and Wickland, 2016; Wallenius et al., 2021).
Microbial processes regulate the production and consumption of
methane in the natural environment (Knittel and Boetius, 2009). Since a
large amount of CH4 is produced in anoxic sediments through meth­
anogenesis (Knittel and Boetius, 2009) and has a huge potential impact
on climate change (Archer, 2007), the importance of anaerobic oxida­
tion of methane (AOM) as an effective global methane sink against
methane escape to the atmosphere from sediments has been widely
recognized for decades (Barnes and Goldberg, 1976; Dale et al., 2008;
Egger et al., 2015; He et al., 2019; Hensen et al., 2003; Hinrichs and
Boetius, 2002; Knittel and Boetius, 2009; Regnier et al., 2011; Segarra
et al., 2015). In marine sediments, methane is oxidized anaerobically by
a consortium of anaerobic methanotrophic (ANME) archaea and
sulfate-reducing bacteria (Boetius et al., 2000; Orphan et al., 2001) with
sulfate as the terminal electron acceptor (Boetius et al., 2000; Hoehler
et al., 1994). This process is commonly referred to as sulfate-driven
anaerobic oxidation of methane or sulfate-dependent anaerobic oxida­
tion of methane (S-AOM), which consumes both sulfate and methane
according to the reaction (Barnes and Goldberg, 1976):
CH4 +SO2−4 →HS− +HCO−3 + H2 O (1)
In surface sediments, sulfate consumption can also be driven by
organic matter that escapes degradation (Berelson et al., 2005; Komada
et al., 2016) and is referred to as organoclastic sulfate reduction (OSR)
(Jørgensen, 1977, 1982):
2CH2 O + SO2−4 →H2 S + 2HCO−3 (2)
The S-AOM process consumes 90% of the methane produced in
marine sediments (Knittel and Boetius, 2009) and 70% of the sulfate
diffused into marine sediments (Akam et al., 2020; Egger et al., 2018). It
is generally accepted that S-AOM occurs in sulfate-rich environments,
whereas S-AOM appears to be less important in sediments with lower
sulfate concentrations (Wallenius et al., 2021). In sulfate-poor envi­
ronment, when sulfate is restricted, AOM is likely to be mediated by
other energetically more favorable electron acceptors, such as Fe (III),
Mn (IV) (Egger et al., 2015; Segarra et al., 2013; Sivan et al., 2011),
nitrate and nitrite (He et al., 2016, 2019; Raghoebarsing et al., 2006;
Segarra et al., 2013; Shen et al., 2016; Wang et al., 2019). However, the
rates of iron-dependent anaerobic oxidation of methane (Fe-AOM) were
recorded at less than 5% of the methane oxidation rates (Wallenius et al.,
2021) and ~3% of the total methane removal (Egger et al., 2015), which
is significantly lower than that of S-AOM in coastal marine and brackish
surface sediments. Significant rates of nitrate/nitrite-dependent anaer­
obic oxidation of methane (N-AOM) were observed mainly in sediments
with high nitrate and nitrite concentrations (He et al., 2019; Wang et al.,
2019). In addition, S-AOM contributes 40% of the dissolved inorganic
carbon (DIC) produced in marine sediments pore-water (Akam et al.,
2020). The outflow of produced pore-water DIC into the water column
has a significant impact on surface water chemistry and potentially at­
mospheric CO2 (Akam et al., 2020). Previous studies have shown that
the contribution of S-AOM to the pore-water DIC pool is greatest in the
ocean (Akam et al., 2020; Sauer et al., 2015), ranging from ~50% to
~80% (Feng et al., 2019; Liu et al., 2020), while the contribution of
S-AOM in estuaries is less than 20% (Wu et al., 2016). In freshwater
lakes, the contribution of S-AOM to the pore-water DIC pool is also high,
ranging from 50% to 70% (Kleint et al., 2021).
The zone where S-AOM process occurs is referred to as the sulfate-
methane transition zone (SMTZ) and is often defined as the depth in­
terval where non-zero sulfate and methane overlap (Barnes and Gold­
berg, 1976; D’Hondt et al., 2002). In addition to numerous reports in
marine environments (e.g. Egger et al., 2018 and reference therein),
2
Water Research 217 (2022) 118441
SMTZ has been reported in brackish sediments and low-sulfate envi­
ronments (Cao et al., 2021; Egger et al., 2015; Kleint et al., 2021;
Sawicka and Brüchert, 2017; Weber et al., 2016; Wu et al., 2015, 2016).
The SMTZ functions as an effective methane barrier, minimizing
methane release to the atmosphere (Kleint et al., 2021; Knittel and
Boetius, 2009). The efficiency of S-AOM affects the efflux of methane
(Boetius and Wenzhöfer, 2013; Sommer et al., 2006), and the surviving
methane that bypasses the SMTZ may undergo other pathways of AOM
and aerobic methane oxidation (MOx) or enter the overlying water
column, eventually escaping to the atmosphere (Egger et al., 2016; He
et al., 2019; Rasigraf et al., 2017; Wallenius et al., 2021). In addition, it
has been highlighted that the SMTZ not only serves as a methane sink,
but is an important diagenetic front for the DIC cycle, with authigenic
carbonate precipitated within the SMTZ comparable to ~15% of car­
bonate accumulation in the ocean (Akam et al., 2020).The latest
compilation reported the SMTZ to be ≤ 2 m in inner shelf sediments and
suggested that SMTZ depths increase with water depth (Egger et al.,
2018). Studies of marginal seas and estuaries have found that the SMTZ
depths became significantly shallower with decreasing sulfate concen­
trations (Cao et al., 2021; Myllykangas et al., 2020), which may be due
to the low sulfate flux into the sediment in low sulfate concentration
environment (Wu et al., 2015). The shoaling of the SMTZ may also
explain high methane emissions from coastal systems (Hamdan and
Wickland, 2016; Wallenius et al., 2021).
Coastal wetlands are critical transition zones between land and sea
that play an important role in mitigating global climate change (Brei­
thaupt et al., 2012; Ouyang and Lee, 2014) and are known as "blue
carbon" ecosystems (Mcleod et al., 2011; Pendleton et al., 2012). Coastal
wetlands have high carbon burial rates (Chmura et al., 2003; Duarte
et al., 2005; Houghton, 2007), but the effective accumulation of carbon
in coastal wetlands does not result in high methane emissions (Callaway
et al., 2012; Chmura et al., 2003; Connor et al., 2001; Holm et al., 2016;
Ouyang and Lee, 2014). This may reflect the large amount of sulfate
carried by seawater (Gupta et al., 2013; Poffenbarger et al., 2011) which
suggests that CH4 is likely to be consumed within the SMTZ via S-AOM
in coastal wetlands. Indeed, the average contribution of S-AOM to total
anaerobic methane oxidation was found to be as high as 34.5% in the
inter-tidal zone (Wang et al., 2019). In coastal brackish wetlands, AOM
was shown to be more dependent on sulfate reduction (Segarra et al.,
2013). In coastal freshwater wetlands, it has also been suggested that
S-AOM may contribute substantially to anaerobic consumption of
methane (Segarra et al., 2015). Although studies have shown that sulfate
has a significant impact on methane emissions from coastal wetlands,
the consumption of methane by S-AOM in coastal wetlands has not been
accurately quantified, and the contribution of S-AOM processes to the
sediment DIC pool remains unknown. Moreover, the effects of envi­
ronmental changes (e.g., changes in salinity and sulfate concentration)
caused by natural factors and anthropogenic intervention on S-AOM
processes and methane budgets remain unclear (Wallenius et al., 2021),
especially for the ecological restoration of degraded coastal wetlands
(Erkens et al., 2016; Kroeger et al., 2017; Lee et al., 2006) and the impact
of restoration measures on the global methane budget. For example,
impoundment and freshening result in enhanced methane emissions
(Kroeger et al., 2017). Methane emissions from coastal wetlands were
significantly elevated during flooding events (Gatland et al., 2014), and
increased methane emissions were also observed in low salinity portions
of tidally-restricted wetlands (Helton et al., 2014; Kroeger et al., 2017).
In contrast, sulfate derived from agricultural pollution and saltwater
intrusion may suppress methane emissions (Helton et al., 2014). Recent
studies have shown that significant CH4 and CO2 reductions from salt
marshes can be achieved by restoring disconnected saline tidal flows
(Kroeger et al., 2017). Understanding the mechanism controlling
methane emissions from coastal wetlands is of great significance to
global carbon neutrality programs and global warming mitigation (Suir
et al., 2019; Wang et al., 2021).
The objectives of this study are to investigate: (1) the contribution of
W. La et al.
S-AOM to methane consumption and DIC production in coastal wet­
lands; and (2) the impacts of sulfate concentration on the methane
budgets in coastal wetlands. To achieve these purposes, seasonal sam­
pling was conducted in a coastal wetland with large salinity differences
influenced by anthropogenic water delivery. Investigations were carried
out at four sites over two seasons to capture the temporal and spatial
variability of chemical conditions in sediments and their influence on
methane oxidation. We hypothesize that: (1) S-AOM dominates methane
consumption in coastal wetland sediments; (2) the contribution of S-
AOM to methane and sulfate consumption and DIC production varies
spatially and temporally depending on environmental variations (tem­
perature, salinity and sulfate concentration); and (3) in areas with lower
sulfate concentrations, S-AOM contributes less to methane and sulfate
consumption and DIC production, and shoals the SMTZ, weakening the
barrier function of the SMTZ.
2. Materials and methods
2.1. Study region
This study was conducted in the Beidagang Wetland Nature Reserve
(38◦ 36′ -38◦ 57′ N, 117◦ 11′ -117◦ 37′ E), southeast of Tianjin, China, 6 km
from the Bohai Bay (Fig. 1). Historically, the Beidagang Wetland was a
saline-alkali environment, but was impacted by a cofferdam construc­
tion and renovation project, resulting in its current configuration. In
September 2020, the Beidagang Wetland was included on the Interna­
tional List of Important Wetlands, becoming one of 64 internationally
important wetlands in China. The Beidagang Wetland is subject to a
temperate continental monsoon climate with an average annual tem­
perature of 11.3 ℃ (Yu et al., 2019). Rainfall is mainly concentrated in
July to August (Guo et al., 2009). The annual average precipitation is
about 550 mm and the annual potential evaporation is about 1777 mm
(Huo et al., 2017). The Beidagang Wetland Nature Reserve is the largest
wetland nature reserve in Tianjin, covering an area of 34,887 hectares.
The vegetation of the wetland is dominated by Phragmites communis. The
Beidagang Wetland is one of the most biodiverse areas in Tianjin,
inhabited by nearly 8 million wading birds, including 6 species of
national-level protected birds and 17 species of second-level protected
birds, e.g., Ciconia boyciana, Ichthyaetus relictus and Larus saundersi
(Chen et al., 2016; Yu et al., 2019).
2.2. Sample collection
Sediments cores were collected in late summer (August 22–29, 2019)
and late winter (February 24–26, 2021) (Fig. 1, S is for summer and W is
for winter). These coring sites were selected from different spatial areas
with significant differences in salinity and sulfate concentrations (Fig.
Fig. 1. (a) Location of the study area; (b) Sampling sites in the Beidagang Wetland, the red circles represent sampling in August 2019 (summer, represented by “S”)
and white circles represent sampling in February 2021 (winter, represented by “W”). (For interpretation of the references to color in this figure legend, the reader is
referred to the web version of this article.)
3
Water Research 217 (2022) 118441
S1). The sampling sites BR, BG and BT are located in the open water
areas, while the BTE site is located at the littoral zone (edge area) close
to reeds. Surface water samples were collected before sediment core
collection. Basic water chemistry parameters of surface and bottom
water were measured using WTW sensors (3430) in summer and YSI
sensors (EXO1) in winter, respectively (Table 1).
Two parallel sediment cores were recovered at each site, one for
obtaining pore-water and the other for collecting methane samples.
After the cores were recovered, the overlying water was collected with a
syringe approximately 1 cm above the sediment. Pore-water was
extracted using Rhizon samplers (Rhizosphere Research Products) con­
nected to 10 mL disposable syringes and the first 1–2 mL of pore water
was discarded. The obtained surface water, overlying water and pore-
water were quickly filtered through 0.22 µm size disposable filters.
1.8 mL of filtered samples were transferred into 1.8 mL septum vials for
measurement of major ions. Aliquots of filtered samples mixed with 40
μL 20% zinc acetate (ZnAc) were stored in 1.8 mL septum vials for
sulfate analysis. For DIC concentration and δ13C-DIC measurements,
filtered samples were transferred into 1.8 mL septum vials containing
10 µL saturated mercury chloride (HgCl2) without headspace. The rest of
the filtered samples were kept in centrifuge tubes, except for 1 mL for pH
and EC determination. To collect methane samples for methane con­
centration and δ13C-CH4 measurements, first, 4 mL of overlying water
above the sediment (< 1 cm) was taken using a syringe with a long PVC
tube attached. Then, 2.5 mL sediment samples were obtained from each
sub-core using 2.5 mL cutoff plastic syringes with a depth resolution of 2
cm. All samples including water and sediments were immediately
transferred to He-flushed serum vials (20 mL) containing distilled water
(4 mL) and NaCl (1.5 g) (Xiao et al., 2018). The serum vials were
immediately sealed with butyl rubber stoppers and aluminum crimp
seals, shaken and stored upside-down. Simultaneously, for each
sub-core, 1 mL of sediment was taken into a pre-weighed centrifuge tube
for porosity determination. All collected samples were placed in an
incubator and transferred to the laboratory, where they were stored at 4
◦
C.
2.3. Analytical methods
Sulfate, calcium and magnesium concentrations were determined by
ion chromatography (ICS-5000+) with analytical precision better than
5% based on repeat analysis of standards. DOC concentration was
determined using a Total Organic Carbon Analyzer (1030 W, America)
with an accuracy better than 5%. For DIC concentration and δ13C-DIC
measurements, 300 µL sample was transferred to a 12 mL acid-washed
and helium-flushed Exetainer (Labco, High Wycombe, UK) and 300 µL
of 85% phosphoric acid was added to drive CO2 into the headspace over
an equilibration phase of at least 15 h (Weber et al., 2017). DIC
W. La et al. Water Research 217 (2022) 118441

Table 1
Main characteristics of core sampling sites (“S” is for summer, and “W” is for winter).
Sites Latitude (N) Longitude (E) Depth (m)a Surface water Bottom water
T ( ◦ C) S (‰)b DO (mg/L) pH T ( ◦ C) S (‰)b DO (mg/L) pH

BRS 38.7146 117.4198 4.00 30.2 1.4 7.4 8.3 30.4 3.1 3.6 8.3
BRW 38.7147 117.4192 4.50 8.4 2.9 12.0 8.2 8.9 8.2 11.5 8.3
BGS 38.8024 117.3751 0.40 32.6 3.2 11.1 8.7 30.2 3.2 4.2 8.2
BGW 38.8016 117.3734 0.35 2.7 6.3 13.3 8.6 4.2 6.2 13.5 8.7
BTS 38.7974 117.4266 0.60 26.7 23.8 4.8 8.4 26.4 23.6 2.7 8.4
BTW 38.7979 117.4260 0.40 9.9 34.5 10.9 8.7 12.4 34.5 9.4 8.7
BTES 38.7862 117.4329 0.40 26.4 23.6 5.0 8.3 26.4 23.6 2.7 8.3
a
water depth.
b
salinity.

concentrations and δ13C-DIC were measured by a Gas Source Isotopic
Ratio Mass Spectrometer (GS-IRMS) equipped with gas bench intake
(Thermo Delta V with Gas Bench II), using NBS 18-Calcite as standard.
The concentration of DIC was determined according to the peak height
and calibration curve on the GS-IRMS with an error of 5%. This value is
consistent with that measured by the TOC Analyzer. The carbon isotopic
composition was reported in standard delta notation with deviations per
mil (‰) from Vienna Pee Dee Belemnite (VPDB) standard. The precision
for the standard samples was better than 0.1‰.
The vials used to determine dissolved CH4 concentrations were
shaken vigorously for 30 s and then placed on a rotary shaker (240 rpm,
11 ◦ C) for 1 h to drive all the dissolved CH4 from the solution into the
headspace (Tong et al., 2010). CH4 concentrations were measured using
a gas chromatograph (7890B, Agilent Technologies) equipped with a
flame-ionization detector. The column temperature was 40 ◦ C. The
measured CH4 concentrations were corrected for standard pressure and
temperature using the ideal gas law and multiplied by the headspace
volume (Tong et al., 2010). Porosity was measured by the weight loss of
a known wet sediment volume during drying at 50 ◦ C until a constant
weight was reached (c. 7 days) (Findlay et al., 2019).
The δ13C-CH4 values of methane were analyzed using the gas chro­
matography–combustion technique (GC–C). The headspace gas was
injected into the GC and peaks were separated using an HP-Plot Q col­
umn (30 m × 0.32 mm × 20 µm, isotherm 60 ◦ C). Then methane was
quantitatively converted to CO2 in the GC-Isolink interface and trans­
ferred via an open split interface to the isotope ratio mass spectrometer
(Delta V, Thermo Fisher). Results for the δ 13C ratio of methane were
given in the usual δ notation versus the Vienna PeeDee Belemnite
(VPDB) standard.
in this study, respectively, and the D0 values of 25 ◦ C and 10 ◦ C in
seawater reported by Schulz (2006) for the high salinity sites (BT and
BTE) in summer (August) and winter (February), respectively. Details of
the flux calculation can be found in the Supporting Information.
3. Results
3.1. Variations in temperature, salinity, dissolved oxygen and pH of
surface and bottom water
The temperature of the bottom water was close to that of the surface
water at each site, varying between 26.4 ◦ C and 32.6 ◦ C in summer
(Table 1), while water temperature in winter ranged from 2.7 ◦ C to 12.4
◦
C. In winter, the salinity of the water at all sites was higher than that in
summer. The salinity of water in the BR site was the lowest and the
salinity of water in the BT and BTE sites had the highest salinity, close to
that of Bohai Seawater (30‰). The variations of salinity and sulfate
concentration in surface water in different areas of the wetland are
spatially consistent with the sampling sites (Fig. S1). The dissolved ox­
ygen (DO) concentrations were higher in winter than in summer, with
the highest values in the BG site and the lowest values occurring in the
BT and BTE sites. The DO concentrations in the bottom water were lower
than the surface water at all sites in summer, while the DO concentra­
tions in the bottom water and the surface water were almost identical in
winter and values were similar at all sites (10.9 mg L− 1 to 13.3 mg L− 1)
(Table 1). The pH values of the surface water and the bottom water were
similar in summer and winter at all sites (range from 8.2 to 8.7).
3.2. Variations in sulfate, CH4, Ca2+, Mg2+ and DIC concentrations

diferença no SR verão In summer, although sulfate concentrations in the overlying water

2.4. Diffusive flux calculation
e inverno varied between the sampling sites (2.94 mmol L− 1 at the BRS site, 5.36
mmol L− 1 at the BGS site, 19.42 mmol L− 1 at the BTS site and 20.63
Diffusive fluxes of methane, sulfate, calcium and magnesium are
mmol L− 1 at the BTES site), sulfate concentrations all decreased sharply
calculated from linear pore-water concentration gradients according to
to near 0 in the surface sediments, and then showed a downward
Fick’s first law and assuming steady state conditions (Canfield, 1989,
increasing trend at the bottom (Fig. 2), except at the BTES site, where
1991):
sulfate concentrations dropped relatively slowly from the surface to the
dC deeper sediments (Fig. 2d). The sulfate profile pattern at the BRW, BGW
J = − φ ⋅ Ds (3)
dz and BTW sites in winter is significantly different from that in summer
− 2 − 1
(Fig. 3), with sulfate concentrations in the upper sediments remaining
where J is the diffusive flux (mmol m d ), φ is the porosity (mL constant (~6 mmol L− 1 between 0 and 8 cm depth at the BRW site, ~9
cm− 3), Ds is the diffusion coefficient in sediment (cm2 d− 1), and dC/dz is mmol L− 1 between 0 and 10 cm depth at the BGW site and ~30 mmol
the concentration gradient (mmol cm− 1) calculated by linear regression L− 1 between 0 and 4 cm at the BTW site) and then decreasing down­
of approximately linear pore-water profile. Diffusion coefficient Ds is wards gently and not being completely depleted at the deepest position
calculated according to Iversen and Jørgensen (1993): where the pore-water stops collecting. The pattern of the methane
D0 concentration profiles was opposite to that of the sulfate concentration
Ds = (4) profiles (Figs. 2 and 3). In summer, the bottom sediments methane
1 + n (1 − φ)
concentrations increased with depth upwards and reached maximum
with n = 2 for φ < 0.7 mL cm− 3 and n = 3 for φ > 0.7 mL cm− 3. The D0 (1.70 mmol L− 1 at 8 cm depth at the BRS site, 0.85 mmol L− 1 at 8 cm
values are listed in Table S1. We referred to the D0 values of 25 C and
◦
depth at the BGS site, 0.85 mmol L− 1 at 16 cm depth at the BTS site), and
10 ◦ C in infinitely diluted solutions reported by Boudreau (1997) for the then decreased sharply upwards at the top sediment, except for the BTES
low salinity sites (BR and BG) in summer (August) and winter (February) site, where the maximum was at the bottom of the sediment (1.00 mmol

4
W. La et al. Water Research 217 (2022) 118441
Qto < 0, origem biológica

fluxo ascendente de SO4

ou mar ancestral antigo.

22,8

26,2

Fig. 2. Depth profiles of concentrations of pore water SO42-, Ca2+, Mg2+, DIC and CH4, and depth profiles of carbon isotopic composition of pore water DIC and CH4
in summer. The overlying water is less than 1 cm above the sediment and is plotted at 0 cm. The gray horizontal bars indicate the estimated SMTZ depths.

L− 1 at 29 cm depth) and decreased with depth upwards (Fig. 2d).
Methane concentrations of the overlying water at the BRS, BGS, BTS and
BTES sites were 0.22 mmol L− 1, 0.04 mmol L− 1, 0.03 mmol L− 1 and 0.04
mmol L− 1, respectively. In winter, methane concentrations at the BRW
and BTW sites increased from the bottom upwards, reaching a maximum
of 2.24 mmol L− 1 and 0.66 mmol L− 1 at 30 cm depth, respectively, and
then decreased upwards to a value less than 0.01 mmol L− 1 at depth of 3
5
cm and 0 cm, respectively. Methane concentrations at the BGW site
decreased upwards from bottom to a value less than 0.01 mmol L− 1 at
depth of 10 cm. Methane concentrations of the overlying water at the
BRW, BGW and BTW sites were 0.42 μmol L− 1, 0.31 μmol L− 1 and 2.89
μmol L− 1, respectively, which were much lower than those in summer.
Pore-water profiles of sulfate and methane showed the SMTZ depth of
2.5 cm, 3 cm, 3.5 cm, 15 cm, 20 cm, 21 cm and 15 cm for BRS, BGS, BTS,
prof media e não a prof inicial.
W. La et al. Water Research 217 (2022) 118441

oxidação aeróbica de CH4

12C são oxidados 1º,
sobram 13C na
superficie, que nao foram
oxidados.

queda de 13C-DIC ,
enriquecimento de 12C no DIC,
provindo do CH4 biológico. Queda
no SO4, prova que S-AOM é
principal processo na oxidação do
CH4.

oxidação bacteriana de
CH4, enriquecimento
de 13C, os
remanescentes, que
não foram oxidados.

Fig. 3. Depth profiles of concentrations of pore water SO42-, Ca2+, Mg2+, DIC and CH4, and depth profiles of carbon isotopic composition of pore water DIC and CH4
in winter. The overlying water is less than 1 cm above the sediment and is plotted at 0 cm. The gray horizontal bars indicate the estimated SMTZ depths.

BTES, BRW, BGW and BTW, respectively, extending along with the
depth where sulfate and methane coexist.
In the BR and BG sites, the concentration profiles of dissolved Ca2+
were clearly different from those of dissolved Mg2+ (Figs. 2 and 3).
Generally, Ca2+ concentrations showed a downward decreasing trend
within the SMTZ and then increased, while Mg2+ concentrations
continued to increase with depth. BGW is slightly different with Ca2+
concentrations increasing and Mg2+ concentrations decreasing down­
wards within the SMTZ. In BT and BTE, both Ca2+ and Mg2+ concen­
trations decreased within the SMTZ. It can be found that significant
authigenic carbonate precipitation process occurred within the SMTZ at
all sites, as has been observed in ocean environments (Akam et al.,
2020). The DIC concentration profiles showed downward increase at all
sites but decrease in the deepest sediments at the BRS and BTS site. At
the BTS and BTES sites, The DIC peaks appeared in the SMTZ (22.82
mmol L− 1 at the BTS site and 26.20 mmol L− 1 at the BTES site), similar
to previous studies in the ocean (e.g. Hu et al., 2017; Knab et al., 2008).
In winter, the DIC concentrations were almost constant (~5 mmol L− 1 at
the BRW site, ~8 mmol L− 1 at the BGW site and ~9 mmol L− 1 at the
BTW site) at the top of the sediments and then increased downwards.
3.3. Variations in carbon isotopic composition of DIC and CH4
The δ13C-DIC values at the BRS, BGS, BTS and BTES sites decreased
from − 15.01‰, − 8.37‰, − 6.24‰ and − 8.94‰ in the bottom water to
minimum values of − 16.48‰ at 2 cm, − 14.20‰ at 3 cm, − 11.98 ‰ at 1
cm and − 11.82‰ at 19 cm, respectively, with these minimum values
being within the SMTZ (Fig. 2). However, the δ13C-DIC was inverted
below the SMTZ and DIC became δ13C-enriched with increasing depth,
especially at the BRS site, where this trend was particularly pronounced.
In winter, the δ13C-DIC values in the bottom water were − 5.15‰,
− 3.94‰, − 0.87‰ at the BRW, BGW and BTW sites, respectively, which
were heavier than in summer, and the δ13C-DIC decreased downwards.
The δ13C-CH4 profiles showed a consistent pattern, with the δ13C-CH4
values increasing upwards above the SMTZ (slightly in summer and
sharply in winter) and increased downwards below the SMTZ (Figs. 2
and 3). The minimum values of δ13C-CH4 were at the bottom of the
SMTZ.

6
W. La et al. Water Research 217 (2022) 118441

4. Discussion 4.2. Production and consumption of methane in the sediments

4.1. Spatiotemporal variations of pore-water profile patterns
The depth of the redox zone in sediments is affected by water tem­
perature, oxygen, salinity, and/or the composition and rate of input of
organic matter (Wallenius et al., 2021). Furthermore, it has been shown
that the concentration gradients of the oxidants for organic carbon
mineralization do not remain constant over time (Crill and Martens,
1987; Dale et al., 2008; Glud et al., 2003). Rather, seasonal variations
affect the rates of reduction processes in sediments. In summer, the
linear and sharp decay of sulfate concentration and the relatively
shallow SMTZ in pore-water (Fig. 2) suggest that the surface sediments
are anoxic (Antler et al., 2014; Hu et al., 2015; Wu et al., 2015) and DO
may be rapidly depleted below the sediment-water interface. A previous
study found that DO is depleted within 6 mm below the sediment-water
interface in salt marsh ponds in summer (Koop-Jakobsen and Gutbrod,
2019). The sulfate reduction zone was immediately adjacent to the
sediment-water interface and the methanogenesis zone was located
below the sulfate reduction zone. The upwards decrease of methane
concentrations in surface sediments suggests the presence of a methane
oxidation zone that overlaps with the sulfate reduction zone. Hypoxia in
sediments is a common phenomenon in summer (e.g. Egger et al., 2016).
In addition to the effects of temperature, blooms of phytoplankton in
spring and summer lead to high organic carbon input and oxygen de­
mand (Middelburg and Levin, 2009; Sawicka and Brüchert, 2017),
resulting in lower DO concentrations in bottom waters (Table 1).
Enhanced hypoxia alters biogeochemical processes and shoals the redox
zone in sediments (Middelburg and Levin, 2009), stressing anaerobic
pathways of organic matter degradation (Hartnett and Devol, 2003;
Middelburg and Levin, 2009), including methanogenesis (Maltby et al.,
2018; Myllykangas et al., 2020), resulting in increased methane flux and
water column methane concentrations in summer (Fig. 2 and Table S2)
(e.g. Egger et al., 2016; Gelesh et al., 2016; Kleint et al., 2021). More­
over, larger sulfate concentration gradients were observed at high bot­
tom water sulfate concentrations (Fig. 2c), suggesting that the level of
The stable carbon isotopic composition of methane in sediments is
less susceptible to anthropogenic influences and thus provides more
reliable constraints on methane production and oxidation (Regnier
et al., 2011). Geochemical profiles of methane in the Beidagang wetland
sediments in summer and winter (Figs. 2 and 3) clearly demonstrate the
deep source of methane and the consumption of methane in surface
sediments. In this section, we identify methane sources and consumption
pathways through concentration and isotope evidence.
4.2.1. Sources of methane in the sediments
Although methane in wetlands is generally considered to be
biogenic, the sources of methane in the sediments of Beidagang wetland
still require careful consideration given the presence and potential in­
fluence of adjacent oil fields. Methanogenesis strongly fractionates
carbon isotopes with the methane produced being significantly depleted
in 13C relative to the substrate (Conrad, 2005; Whiticar, 1999). The
carbon isotopic composition (δ13C-CH4) of biogenic methane typically
ranges from − 110‰ to − 50‰ (Whiticar, 1999; Whiticar and Faber,
1986), while that of thermogenic methane is usually typically enriched
in 13C, ranging from − 50‰ to − 20‰ (Schoell, 1988; Whiticar, 1999). In
the Beidagang wetland, the carbon isotope values (δ13C-CH4) of
methane below the SMTZ ranged from − 50.4 ‰ to − 83.2 ‰ (Figs. 2 and
3), indicating a biogenic source. Therefore, the increase of δ13C-CH4
with depth below the SMTZ most likely reflects in-situ microbial
methane production rather than the addition of heavy methane from
deep sources (Burdige et al., 2016; Sauer et al., 2015). In addition, we
obtained kinetic isotope fractionation factors for carbon (εC = − 1.0‰)
(Fig. 4c) from the Rayleigh distillation function below the SMTZ
(Alperin et al., 1988; Crowe et al., 2011; Egger et al., 2015; Rayleigh,
1896), in contrast to the kinetic isotopic fractionation factors within and
above the SMTZ, which may be relevant to microbial methanogenesis
(Chanton et al., 2005; Egger et al., 2015; Hornibrook et al., 2000;
Acima do SMTZ sempre rico em 13C, CH4 não oxidado (~2%o)

sulfate concentration also has an important effect on the sulfate reduc­

tion rate.
The opposite was true in winter. The sulfate reduction zone, methane
oxidation zone, methanogenesis zone and sulfate-methane transition
zone all shifted downwards compared to summer, and the associated
biogeochemical rates decreased, exhibiting reduced concentration gra­
dients. In addition, the sulfate concentrations at the sediment surface
remained constant over some depth in winter, which is consistent with
the observation of Sawicka and Brüchert (2017). DO concentrations in
water column were higher in winter than in summer (Table 1) (e.g.
Sawicka and Brüchert, 2017). Increased DO concentration in the water
column and decreased organic carbon input and reduced microbial ac­
tivity lead to deeper sulfate penetration and broader oxidation zones
(Pimenov et al., 2013). Bioturbation may also be an important influence
that can facilitate oxygen penetration to greater depths (Antler et al.,
2019; Myllykangas et al., 2020), leading to kink-type sulfate profiles
(Fig. 3) (Hensen et al., 2003). It is important to note that the pore-water
profile pattern in the littoral site (BTES) (Fig. 2d) also differs from the
other sites in summer, possibly due to loose sediments and plant roots
supporting oxygen transport to the surface sediments (Chowdhury and
Dick, 2013; Hanson and Hanson, 1996; Whalen, 2005), making the
surface sediments low-oxygen zones (Bastviken et al., 2004). A previous
study suggested that oxygen dynamics in pond swamp habitats differ
from those of surrounding vegetated marshes (Koop-Jakobsen and
Gutbrod, 2019). In the littoral zone, oxygen penetration can reach a
Fig. 4. Rayleigh fractionation plots for δ13C-CH4. CH4(z)/CH4(max) represents
depth of 6 cm in summer, which is 10 times deeper than in pond swamp
the fraction of residual methane (CH4(z)) relative to the initial methane con­
habitats (Koop-Jakobsen and Gutbrod, 2019). centration (CH4(max)). Data from the August 2019 (summer) are shown in solid
circles, and those from the February 2021 (winter) are shown in hollow circle.
Different slopes across the SMTZ reveal two to three distinct sets of kinetic
isotope fractionation factors for carbon (εC) that are spatially separated.

7
 W. La et al.
Whiticar, 1999). In the methanogenesis zones below the SMTZ, carbon
dioxide and acetate are used as substrates for methanogenesis in the
absence of sulfate (Claypool and Kaplan, 1974; Martens and Berner,
1974). The nearly parallel profiles of δ13C-CH4 and δ13C-DIC with
increasing depth (Heuer et al., 2009) below the SMTZ suggest that
methane is likely produced through CO2 reduction (Whiticar, 1999). The
exact process requires more evidence and needs to be studied in the
future. It should be noted that fluctuations in deep methane concen­
tration profiles may be caused by uneven distribution of gas pockets or
degassing during sub-sampling (Dickens et al., 1997; Paull and Ussler
III, 2001). However, in the mixing and net-reaction plots of CH4 (Fig.
S6), all points below the SMTZ were linearly correlated (R2 = 0.99),
indicating that methane is not affected by degassing during sampling
(Komada et al., 2016).
4.2.2. The oxidation of methane in the sediments
The δ13C-CH4 values within and above the SMTZ showed an upwards
increase (Figs. 2 and 3), which is consistent with methane carbon
isotope fractionation related to methane oxidation (Alperin et al., 1988;
Conrad, 2005; Whiticar, 1999). Light isotopes are preferentially
oxidized during methane oxidation (Alperin et al., 1988; Martens et al.,
1999; Whiticar, 1999), resulting in a gradual enrichment of the residual
CH4 in 13C-CH4 toward cores surface (Egger et al., 2015). The Rayleigh
distillation function plots (Fig. 4) show two or three distinct sets of
carbon isotope fractionation factors (εC). Above the SMTZ in summer
(BTES) and winter (all sites), the isotope fractionation factors (εC)
ranged from 2.0‰ to 2.7‰, which are comparable to the fractionation
factor (εC = 2 ‰) derived from the high cell density methane aerobic
oxidation experiments reported by Templeton et al. (2006). Considering
that the sulfate concentrations remained constant over those depths and
that the slightly sustained decrease in methane concentrations was
accompanied by a gradual increase in δ13C-CH4 in surface sediments, the
aerobic oxidation of methane (MOx) may have occurred above the SMTZ
at these sites. Aerobic methane oxidizing bacteria (MOB) are expected to
dominate the surface sediment (Rasigraf et al., 2017). Studies from
lacustrine and terrestrial environments suggest that MOB may be less
sensitive to temperature (King, 1992; Wik et al., 2014) and more
adaptable to cold environments. This explains our observation that
δ13C-CH4 could increase to − 29.5‰ in winter (Fig. 3b), which is
consistent with the findings in Lake Willersinnweiher that MOx causes
an increase in δ13C-CH4 from − 75‰ in the bottom water to − 24‰ in the
middle water (Einzmann, 2020). In brackish coastal sediments, aerobic
methanotrophs at the surface of the sediment have also been found to
consume a large fraction of methane not oxidized by the AOM process
(McDonald et al., 2005; Moussard et al., 2009; Steinle et al., 2017).
The depleted δ13C-DIC hotspots (Treude et al., 2014) within the
SMTZ (Fig. 2) are likely the result of carbon isotope fractionation during
AOM (Hinrichs et al., 1999), adding light carbon from methane to the
DIC pool (Chen et al., 2010; Haese et al., 2003; Yoshinaga et al., 2014).
The minimum values of δ13C-DIC ranged from − 18.49‰ to − 11.82‰,
larger than those observed in marine sediments (cf. Komada et al., 2016;
Wehrmann et al., 2011; Wurgaft et al., 2019), but consistent with coastal
environments (cf. − 19‰ and − 12‰, Sauer et al., 2015), where they are
thought to be the result of S-AOM. The Rayleigh distillation function
plots (Fig. 4) reveal a common range of carbon isotope fractionation
factors (εC) (8.9‰ to 12.5‰), which corresponds with the reported
uma boundary (7.3‰ ~13‰) of carbon isotope fractionation factors associ­
hipóteseated with S-AOM in marine Sediment (Alperin et al., 1988; Egger et al.,
das
s deste 2015; Holler et al., 2009; Martens et al., 1999). This result is consistent
trabalho
era with the sharp decrease in sulfate concentration within the SMTZ
provar (Figs. 2 and 3), indicating that S-AOM is the main methane anaerobic
que
[SO4] oxidation process within the SMTZ and may even dominate the methane
regulava
a sua
consumption process in the Beidagang Wetland, both in high and low
importâ sulfate environments.
The carbon isotope fractionation factors below the SMTZ at the BGS
ncia no
S-AOM.
and BRS sites remain in the same sense as within the SMTZ (Fig. 4),
8
Water Research 217 (2022) 118441
suggesting that AOM still exists below the SMTZ at the BGS and BRS
sites. AOM may also be present below the SMTZ at the BTS site, affecting
the carbon isotope fractionation process and disturbing the carbon
isotope fractionation factor during methanogenesis. At the BGS site,
AOM tends to couple sulfate reduction at low sulfate concentration.
Previous studies have shown that S-AOM can occur at low sulfate con­
centration (much less than 1 mmol L− 1) (e.g. Beal et al., 2011; Segarra
et al., 2015; Weber et al., 2017, 2016) perhaps supported by a cryptic
sulfur cycle (Holmkvist et al., 2011). However, at the BRS site, the
carbon isotope fractionation factors below the SMTZ in summer and
winter are as low as 4.3‰, which may be a result of the carbon isotope
partitioning behavior during methanogenesis blurring the kinetic iso­
topic effects of carbon during the cryptic sulfur cycle. Another possi­
bility is that this value is related to Fe-AOM, which has been found to
play an important role in methane removal in freshwater (Crowe et al.,
2011; Norði et al., 2013; Sivan et al., 2011; Wersin et al., 1991) and
brackish water (Egger et al., 2015; Segarra et al., 2013; Slomp et al.,
2013) environments. The high active iron contents in BR (~3 mg/g, Sun
et al., unpublished) may support this hypothesis, but requires more
conclusive evidence. In addition, the downward increase in sulfate
concentration at the bottom of the sediment may be an inheritance from
earlier saltwater relics (Koebsch et al., 2019) or a conseqence upwelling
of deeper groundwater, which further promotes anaerobic oxidation of
methane in the deep sediment (Mogollón et al., 2012). The nitrate
concentrations (< 8 μmol L− 1) of the bottom water in this study are
much lower than the values (minimum value is 71.4 μmol L− 1) reported
by He et al. (2019), suggesting that N-AOM may not be important in the
Beidagang wetland.
4.2.3. The contribution of S-AOM to sulfate reduction and methane
oxidation OSR - organoclastico Sulfato Redução
Both S-AOM and OSR coexisting within the SMTZ Burdige and
Komada, 2011; Komada et al., 2016) consume sulfate and produce DIC
through sulfate reduction processes. In the Beidagang wetland, linear
sulfate profiles within the SMTZ (Fig. 2) suggest that S-AOM may
dominate the consumption of sulfate within the SMTZ (Borowski et al.,
1996; Chuang et al., 2013; Hensen et al., 2003; Luo et al., 2013;
Mazumdar et al., 2014; Niewöhner et al., 1998; Wallmann et al., 2006).
The ratio of cation-adjusted DIC (ΔDIC+ΔCa2++ΔMg2+) to removed
sulfate (ΔSO42-) is often used to assess the occurrence of OSR and S-AOM
within the SMTZ (Antler et al., 2014; Burdige and Komada, 2011; Chen
et al., 2010; Haese et al., 2003; Hu et al., 2015; Liu et al., 2020; Luo et al.,
2013; Peketi et al., 2015; Wu et al., 2016). We expected a ratio of 1:1 for
AOM and 2:1 for OSR according to the net stoichiometry of Eqs. (1) and
((2), and found that almost all data for BR and BG (summer and winter)
within the SMTZ plotted along the 2:1 ratio line (Fig. 5), which appears
to indicate that OSR is the main sulfate consumption process within the
SMTZ for both BR and BG. The distribution of data for BT was close to
the 1:1 ratio line in summer (BTS) and between the 2:1 and 1:1 lines in
winter (BTW), suggesting that S-AOM removed sulfate within the SMTZ
in summer, while OSR and AOM coexist in winter. This is consistent with
the conclusions of Wu et al. (2015). Data from the BTES site also suggest
that S-AOM and OSR coexist within the SMTZ. It should be noted that
this approach is not always reliable, as DIC from deep sources can cause
data to fall above the 2:1 line (Fig. 5) (Chatterjee et al., 2011; Wu et al.,
2016), while significant authigenic carbonate precipitation in saline
water with high concentrations of Ca2+ can drive data below the 1:1 line
(Fig. 5) (Liu et al., 2020).
To understand better the sulfate reduction pathways within the
SMTZ and to quantify the role of S-AOM in sulfate reduction, diffusion
flux calculations across the SMTZ were performed (see Supporting In­
formation). The calculation results are listed in Table S2. For the BRS,
BGS, BTS and BTES sites, the ratios of net DIC produced by S-AOM and
OSR to total sulfate fluxes were 1.63, 1.38, 1.03 and 1.48, respectively.
The estimates of 1.51, 1.89 and 1.62 for BRW, BGW, BTW sites in winter
were greater than those in summer. This result is consistent with the
W. La et al.
SRB
AOM
Fig. 5. Pore water DIC (cation-adjusted) added versus SO42- removed (relative
to bottom water) within the SMTZ. Dashed line of 1:1 ratio is consistent with S-
AOM and dashed line of 2:1 ratio is consistent with OSR.
findings in Fig. 5. The sulfate fluxes diffusing into the SMTZ in the
sediments of the open water area sediments (BR, BG and BT) were 30.75
~ 50.74 mmol m− 2 d− 1 in summer and 0.52 ~ 3.07 mmol m− 2 d− 1 in
winter. For the littoral zone (BTES), the summer flux value was 7.59
mmol m− 2 d− 1. According to the net DIC fluxes, we calculated that
37.03%~96.41% of the sulfate diffusing into the SMTZ was reduced by
S-AOM in summer (Fig. 6), while the contribution of S-AOM to sulfate
consumption (FS-AOM) within the SMTZ decreased in winter, with the
estimated range being 11.53%~47.27%. The variation of DOC con­
centrations within the SMTZ (Fig. S2 and S3) also supported our
calculation results, especially at the BGS site, where DOC consumption
within the SMTZ was much higher than accumulation, indicating that
OSR accounts for the major consumption of sulfate. This is a wide range
compared to the reported values for estuarine sediments (cf. Sawicka
and Brüchert, 2017), continental shelf (cf. Wurgaft et al., 2019),
deep-sea basins (cf. Hong et al., 2016; Komada et al., 2016) and cold
seeps (cf. Feng et al., 2019; Liu et al., 2020; Wehrmann et al., 2011).
Further, the FS-AOM was greater at sites with high sulfate concentrations
Fig. 6. The fraction of total SO42- flux into the SMTZ that accounted for by S-AOM and OSR. (a) Different proportions of sampling sites in summer of this study. The
ring part and number shown in the plot represent the proportion of S-AOM, The remaining blanks not shown is contributed by OSR. (b) Different consumption ratio of
S-AOM and OSR in saltmarsh (this study), estuary (Wu et al., 2015; 2016) and sea (Feng et al., 2019).
9
Water Research 217 (2022) 118441
with almost all of the sulfate (96.41%) being used to consume methane
at the BTS site. However, at the BTES site, the sulfate concentration was
the same as at BTS site, but S-AOM consumed only half of the methane
within the SMTZ. The low oxygen status of the surface sediments may
inhibit strictly S-AOM anaerobic processes, and microorganisms asso­
ciated with AOM were found to be viable at relatively high temperatures
(Zehnder and Brock, 1980), which may also be responsible for the
pathway alteration in winter. On a regional scale, the highest FS-AOM was
observed in the sulfate-rich ocean environment, while the highest FOSR
was observed in an estuarine environment (Fig. 6b), probably due to the
flowing river water facilitating the exchange of dissolved oxygen in the
surface pore water with the overlying water, consistent with the reason
for the lower FS-AOM at BTES site.
The calculated methane fluxes consumed by S-AOM in summer were
18.79 mmol m− 2 d− 1, 19.17 mmol m− 2 d− 1, 44.81 mmol m− 2 d− 1 and
3.89 mmol m− 2 d− 1 at BRS, BGS, BTS and BTES sites, respectively. The
estimated consumption values for BRW, BGW and BTW sites in winter
were 0.26 mmol m− 2 d− 1, 0.06 mmol m− 2 d− 1 and 1.17 mmol m− 2 d− 1.
The contribution of S-AOM to methane oxidation can reach 71.01%,
89.28%, 95.91% and 83.30% at BRS, BGS, BTS and BTES sites in sum­
mer, respectively. Methane oxidation decreases in winter to 22.03%,
46.15% and 85.40% at BRW, BGW and BTW sites, respectively. The
contribution of S-AOM to methane consumption in this study is close to
previous estimates for the marine environment (90%, Knittel and Boe­
tius, 2009). Previous studies have found that S-AOM efficiency in the
marine environment appears to be related to the rate of upward flow of
sulfate-depleted fluids, with increased S-AOM efficiency at lower fluid
velocity (Niemann et al., 2006; Wallmann et al., 2006; Xu et al., 2018,
2021). In some environments with very low fluid flow rates, where
methane rarely escapes to the bottom water (Steeb et al., 2015; Xu et al.,
2018), the contribution of S-AOM to methane consumption can be up to
98%~100% (Knab et al., 2008; Xu et al., 2021). The low porosity (Fig.
S4), high methane flux (Table S2) and sufficient sulfate in the bottom
water can support high S-AOM efficiency at our study sites. Overall, our
results based on the calculation of diffusive fluxes demonstrate that
S-AOM dominates methane oxidation in the Beidagang wetland and
make an important contribution to methane removal in both high and
low sulfate concentration wetlands. However, the higher the sulfate
concentration in the surface water of the wetland, the more efficiently
methane was removed.
4.3. Possible sources of pore-water DIC
The concentration and stable carbon isotopic composition of pore-
water DIC are sensitive indicators to characterize carbon cycle pro­
cesses (Wu et al., 2016). The increase of DIC concentration and decrease
of δ13C-DIC in sediment surface (Fig. 2) are correlated with OSR and
W. La et al.
S-AOM (Burdige et al., 2016; Komada et al., 2016; Wehrmann et al.,
2011), while the increase of δ13C-DIC with depth below the SMTZ
(Fig. 2) is related to methanogenesis by either CO2 reduction or acetate
fermentation (Conrad, 2005; Whiticar, 1999). Therefore, the high con­
centration of DIC within the SMTZ is a mixture of in situ light DIC
produced by OSR and AOM within the SMTZ and heavy DIC produced by
methanogenesis below the SMTZ (Chatterjee et al., 2011).
To estimate the relative contributions of OSR, S-AOM, and meth­
anogenesis to the DIC pool in summer, we applied a simple three-end-
member mixing model (Komada et al., 2016; Wu et al., 2016):
δ13 Cadded = fOSR *δ13 COM + fS− AOM *δ
13
CS− + fmethanogenesis *δ13 CDIC*
AOM
fOSR + fS− + fmethanogenesis = 1
AOM
where f is the fraction of DIC produced from OSR, S-AOM and meth­
anogenesis. The meaning of the different δ and the details of the
calculation process can be found in the Supporting Information. The
final calculation results are presented in Table S3. Methanogenesis is the
largest source of the pore-water DIC pool, ranging from 82.56% to
88.7%, while OSR (0.64%~8.68%) and S-AOM (2.55%~8.58%)
contribute relatively little to the pore-water DIC pool. The high contri­
bution of methanogenesis to the DIC pool may influence the DIC con­
centration within the SMTZ, resulting in a ratio of cation-adjusted DIC to
removed sulfate higher than 2: 1 (Fig. 5). Furthermore, the role of AOM
and methanogenesis is more important in areas of high sulfate concen­
tration in the Beidagang wetland (BTS and BTES). On a regional scale,
the contribution of S-AOM to pore-water DIC pool increases, and the
contribution of methanogenesis decreases from coastal wetlands to
marine sediments (Fig. 7). The increasing trend of methane contribution
to the DIC pool from marine sediments to coastal wetlands is consistent
with the trend from the abyss to the inner shelf (Akam et al., 2020), and
this trend may be related to the increasing organic carbon burial rate per
unit area from ocean to coastal wetlands (2.62 g C m− 2 yr− 1 for shelf
waters, 13.10 g C m− 2 yr− 1 for estuarine waters and 98.72 g C m− 2 yr− 1
for tidal wetlands) (Najjar et al., 2018). Coastal wetlands have high
carbon storage, accounting for ~50% of ocean carbon sequestration
(Duarte et al., 2013, 2005). High organic carbon burial rates and high
organic carbon sequestration can provide methanogens with sufficient
substrate for methanogenesis (Egger et al., 2018), which may explain
such a high contribution of methanogenesis to pore-water DIC pool in
coastal wetlands (Fig. 7). In addition, we found that the contribution of
S-AOM to pore water DIC is higher at sites with high sulfate concen­
trations, both in the Beidagang wetland and on a regional scale.
alta Corg
alta [SO4]
Fig. 7. Fractions of DIC from different sources contributed to the pore water
total DIC pool in saltmarsh (this study), estuary (Wu et al., 2015; 2016) and sea
(Feng et al., 2019).
Water Research 217 (2022) 118441
4.4. The variation of the SMTZ depth and its controlling factors
The depth of the SMTZ in the Beidagang Wetland (10 cm on average)
is similar to other wetlands (~10 cm, Ng et al., 2017; Segarra et al.,
2015, 2013) but shallower than that of estuarine sediments (cf. Sawicka
and Brüchert, 2017; Wu et al., 2015) and Marine sediments (cf. Egger
et al., 2018 and reference therein). In addition, significant seasonal
fluctuations in the depth of the SMTZ were found, with shallower depths
near the sediment-water interface in summer and moving down to
deeper depths in winter. Similar observations were found in other
studies, with the SMTZ deeper in winter than in summer (e.g. Kleint
(5)
et al., 2021; Maltby et al., 2018; Myllykangas et al., 2020; Sawicka and
Brüchert, 2017; Wu et al., 2015). In summer, elevated temperatures and
(6)
high organic matter input and hypoxia due to biomass blooms (Mid­
delburg and Levin, 2009) increase SO42- reduction and methanogenesis
rates, which may lead to vertical upwards migration of SMTZ in sedi­
ments (Egger et al., 2016, 2015; Slomp et al., 2013). Spatially, the depth
of the SMTZ was significantly deeper than that of open water in the
littoral areas of reeds growth, which may be the result of oxygen influ­
ence (Wehrmann et al., 2011). In addition, there was little variation in
SMTZ depths in open water areas, and the SMTZ was deeper in areas
with higher bottom water sulfate concentrations, which is consistent
with studies in coastal marine sediments (cf. Cao et al., 2021; Mylly­
kangas et al., 2020; Wu et al., 2015). Wu et al. (2015) suggested that
high sulfate concentration increases the sulfate flux into the sediments
and affects the depth of the SMTZ. However, a strong correlation be­
tween the depth of the SMTZ and bottom water sulfate concentration
was not observed on a regional scale (Fig. 8a), implying that sulfate
concentration may not be a direct cause of SMTZ depth variation
(Myllykangas et al., 2020).
A strong negative correlation between the SMTZ depth, downward
sulfate flux and upward methane flux was observed on a regional scale
(Fig. 8b, c), which is consistent with the global ocean sediment data of
Egger et al. (2018). Many studies have suggested that the depth of the
SMTZ is related to the upward methane flux (e.g. Burdige and Komada,
2011; Myllykangas et al., 2020; Sauer et al., 2015), and that high up­
ward methane flux will shoal the SMTZ (Borowski et al., 1996; Hong
et al., 2016; Liu et al., 2020; Sauer et al., 2015; Zhang et al., 2020). For
example, the SMTZ depth is typically greater than 100 cm in marine
sediments, while the depth of SMTZ in cold seeps is only a few centi­
meters (e.g. Fischer et al., 2012; Gieskes et al., 2005), which may be due
to the high upward methane flux in cold seeps. Activated methano­
genesis directly affects the sulfate kinetics through AOM (Mogollón
et al., 2012). As the upward diffusion flux of methane increases, the
activity of AOM is enhanced (Hong et al., 2016; Liu et al., 2020; Regnier
et al., 2011), leading to an increased demand for sulfate, which explains
the strong positive correlation between downward sulfate flux and up­
ward methane flux (Fig. 7d). High methane concentrations and high
upward methane fluxes were observed in organic matter-rich regions
(Mogollón et al., 2012; Sawicka and Brüchert, 2017; Zhang et al., 2020),
suggesting that organic matter input may be a key factor influencing the
relationship between methane fluxes and SMTZ depth (Borowski et al.,
1996; Myllykangas et al., 2020). High organic matter input rates and
sedimentation rates will shorten the residence time of organic matter in
the sulfate reduction zone, increase the methanogenic substrate below
the SMTZ (Dale et al., 2019; Sundby, 2006), promote methane pro­
duction, increase the upward methane flux (Egger et al., 2016, 2018),
and further shoal the SMTZ depth, weaken the filtering function of the
SMTZ, and result in more methane entering the water column and even
escaping to the atmosphere (Gelesh et al., 2016).
On a regional scale, the upward methane fluxes increase from marine
sediments to estuarine sediments and yet further to coastal wetlands
sediments by every 2 to 3 orders of magnitude (Fig. 8). Egger et al.
(2018) also found methane diffusive fluxes to the SMTZ from coastal
systems up to three orders of magnitude higher compared to methano­
genic deep-sea sediments, and suggested that this flux increase
10
W. La et al. Water Research 217 (2022) 118441

Fig. 8. The SMTZ depths versus bottom water SO42- concentration (a), versus diffusive flux of SO42- into the SMTZ (b) and diffusive flux of CH4 into the SMTZ (c),
and the relationship between diffusive flux of SO42− and CH4 into the SMTZ (d). The dark areas are the 95% confidence interval, and the light areas are the 95%
prediction interval.

correlates with changes in sediment age at the SMTZ. The high upward
methane flux in coastal wetlands may be associated with the high carbon
burial rate (Chmura et al., 2003; Duarte et al., 2005; Houghton, 2007).
This would imply that the relative contribution of methanogenesis to
organic matter degradation becomes more important (Mogollón et al.,
2012), which is consistent with the relative contribution of methano­
genesis to pore water DIC increasing from marine environments to
coastal wetlands (Fig. 7). Although we have no direct evidence that
methane consumption by S-AOM decreased from ocean to coastal wet­
lands, as methane within the SMTZ is usually assumed to be completely
consumed by sulfate in flux calculations (e.g. Wu et al., 2016), The
contribution of S-AOM to the pore water DIC pool decreased from ocean
to coastal wetlands (Fig. 7), which indirectly suggests a decrease in the
contribution of S-AOM to methane consumption. Therefore, the shoaled
SMTZ impairs S-AOM and increases the potential for methane emission
(Myllykangas et al., 2020; Wallenius et al., 2021). The contribution of Fig. 9. Conceptual diagram illustrating the spatial variations of the SMTZ and
S-AOM to methane consumption is greater in areas with high bottom the contribution of S-AOM to methane and sulfate depletion and DIC produc­
water sulfate concentrations (Fig. 9), suggesting that bottom water tion in coastal wetland sediments.
sulfate concentration also has an important effect on S-AOM. High
bottom water sulfate concentrations mean that there is enough sulfate in 5. Conclusions
the SMTZ to support methane oxidation and that sulfate can be
replenished quickly and adequately. The reaction of sulfate with easily Geochemical profiles patterns of sediments in the Beidagang
available methane can support thriving microbial growth. However, in Wetland, Tianjin, China, show significant temporal and spatial vari­
the areas with low sulfate concentrations, there is little sulfate remain­ ability. Our results show that despite aerobic oxidation of methane,
ing to support methane oxidation after the OSR process. Thus, sulfate is methane consumption is mainly dominated by S-AOM in the Beidagang
not available to penetrate deeper to react with methane, and microor­ Wetland. It consumes 71.01%− 95.91% of methane within the SMTZ,
ganisms may have adapted to using organic matter rather than methane and 37.03%− 96.41% of sulfate is consumed meanwhile within the
as a substrate for growth during their long-term evolution. SMTZ. In winter, this contribution become lower due to changes in

11
W. La et al.
dissolved oxygen and temperature. In particular, S-AOM consumes more
sulfate within the SMTZ in areas with high bottom water sulfate con­
centrations, while more sulfate is used for OSR within the SMTZ in areas
with low bottom water sulfate concentrations. In addition, methano­
genesis is the largest source of the pore-water DIC pool with a range of
82.56%− 88.7%, while OSR (0.64%− 8.68%) and S-AOM (2.55%−
8.58%) contribute less to the pore-water DIC pool. Similarly, meth­
anogenesis and S-AOM contribute more to the pore-water DIC pool in
areas with high sulfate concentrations in the bottom water. In addition,
the SMTZ depths in the Beidagang wetland sediments were shallower
than those in estuarine and marine sediments, and there were significant
seasonal variations, which may be caused by changes in temperature,
oxygen and organic matter inputs. The depth of the SMTZ is strongly
negatively correlated with the upward methane flux and the downward
sulfate flux. The large amount of organic carbon buried in the coastal
wetlands triggers active methanogenesis, leading to high upward
methane fluxes that shoal the SMTZ, resulting in high methane emis­
sions from the coastal wetlands. Desalinization of coastal wetland waters
caused by human intervention will reduce the supply of sulfate from the
water column to the sediment, weakening the S-AOM and impairing the
barrier function of the SMTZ, further inducing high methane emissions
in coastal wetlands.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
We thank A.Z. Xu, P. Sun and W.Y. Li for their assistance during
sampling, X.L. Fu, L. Lu and Z.Y. Pang for methane concentration and
carbon isotopic composition determination. We thank prof. Rob M.
Ellam for his contribution to the editing of the language. This work was
supported by the National Natural Science Foundation of China (Grant
Numbers: 41971123 and 42103052) and the National Science & Tech­
nology Fundamental Resources Investigation Program of China (Grant
Number: 2021FY101000).
Supplementary materials
Supplementary material associated with this article can be found, in
the online version, at doi:10.1016/j.watres.2022.118441.
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