Salinity-Linked Denitrification Potential in Endorheic Lake Bosten (China) and Its Sensitivity to Climate Change

Abstract

Endorheic lakes in arid regions of Northwest China are generally vulnerable and sensitive to accelerated climate change and extensive human activities. Therefore, a better understanding of the self-purification capacity of ecosystems, such as denitrification, is necessary to effectively protect these water resources. In the present study, we measured unamended and amended denitrification rates of Lake Bosten by adding the ambient and extra nitrate isotopes in slurry incubations. Meanwhile, we investigated the abundances and community structure of nitrous oxide-reducing microorganisms using qPCR and high-throughput sequencing, respectively, in the surface sediments of Lake Bosten to study denitrification potential in endorheic lakes of arid regions as well as the response of those denitrifiers to climatically induced changes in lake environments. Amended denitrification rates increased by one order of magnitude compared to unamended rates in Lake Bosten. The great discrepancy between unamended and amended rates was attributed to low nitrate availability, indicating that Lake Bosten is not operating at maximum capacity of denitrification. Salinity shaped the spatial heterogeneity of denitrification potential through changes in the abundances and species diversity of denitrifiers. Climate change had a positive effect on the water quality of Lake Bosten so far, through increased runoff, decreased salinity, and enhanced denitrification. But the long-term trajectories of water quality are difficult to predict alongside future glacier shrinkage and decreased snow cover.

Full text

ORIGINAL RESEARCH
published: 14 July 2022
doi: 10.3389/fmicb.2022.922546
Frontiers in Microbiology | www.frontiersin.org 1July 2022 | Volume 13 | Article 922546
Edited by:
Antonio Castellano-Hinojosa,
University of Florida, United States
Reviewed by:
Jordi Catalan,
Spanish National Research Council
(CSIC), Spain
Maria Cavaco,
University of Alberta, Canada
*Correspondence:
Guang Gao
guanggao@niglas.ac.cn
Specialty section:
This article was submitted to
Aquatic Microbiology,
a section of the journal
Frontiers in Microbiology
Received: 18 April 2022
Accepted: 13 June 2022
Published: 14 July 2022
Citation:
Jiang X, Liu C, Hu Y, Shao K, Tang X,
Gao G and Qin B (2022)
Salinity-Linked Denitrification Potential
in Endorheic Lake Bosten (China) and
Its Sensitivity to Climate Change.
Front. Microbiol. 13:922546.
doi: 10.3389/fmicb.2022.922546
Salinity-Linked Denitrification
Potential in Endorheic Lake Bosten
(China) and Its Sensitivity to Climate
Change
Xingyu Jiang 1, Changqing Liu 1,2 , Yang Hu 1, Keqiang Shao 1, Xiangming Tang 1,
Guang Gao 1
*and Boqiang Qin 1
1State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy
of Science, Nanjing, China, 2University of Chinese Academy of Sciences, Beijing, China
Endorheic lakes in arid regions of Northwest China are generally vulnerable and sensitive
to accelerated climate change and extensive human activities. Therefore, a better
understanding of the self-purification capacity of ecosystems, such as denitrification, is
necessary to effectively protect these water resources. In the present study, we measured
unamended and amended denitrification rates of Lake Bosten by adding the ambient and
extra nitrate isotopes in slurry incubations. Meanwhile, we investigated the abundances
and community structure of nitrous oxide-reducing microorganisms using qPCR and
high-throughput sequencing, respectively, in the surface sediments of Lake Bosten to
study denitrification potential in endorheic lakes of arid regions as well as the response
of those denitrifiers to climatically induced changes in lake environments. Amended
denitrification rates increased by one order of magnitude compared to unamended
rates in Lake Bosten. The great discrepancy between unamended and amended rates
was attributed to low nitrate availability, indicating that Lake Bosten is not operating
at maximum capacity of denitrification. Salinity shaped the spatial heterogeneity of
denitrification potential through changes in the abundances and species diversity of
denitrifiers. Climate change had a positive effect on the water quality of Lake Bosten
so far, through increased runoff, decreased salinity, and enhanced denitrification. But
the long-term trajectories of water quality are difficult to predict alongside future glacier
shrinkage and decreased snow cover.
Keywords: nitrate availability, salinity, arid region, Northwest China, species diversity, endorheic lake
INTRODUCTION
Endorheic lakes, as one of the major components of endorheic water systems, are the
primary available water sources in arid regions and play significant roles in the social
and economic development of those regions (Tao et al., 2015; Xu et al., 2020). High
degrees of continentality and isolation make endorheic lakes particularly susceptible
and vulnerable to climate and environmental change (Yapiyev et al., 2017; Huang
et al., 2020). Due to the discharge of agricultural, industrial, and urban wastewaters,
endorheic waters have been increasingly threatened by eutrophication in recent decades
(Arce et al., 2013; Menberu et al., 2021; Sun et al., 2021; Diaz-Torres et al., 2022).

Jiang et al. Denitrification in Lake Bosten
More importantly, endorheic lakes are land-locked drainage
networks where water does not drain into other water bodies
(Yapiyev et al., 2017). Due to the lack of outlets, the removal
of inflowing pollutants depend primarily on the self-purification
capacity of ecosystems (Arce et al., 2013; Valiente et al., 2018).
Therefore, a better understanding of the self-purification capacity
and ecological resilience of endorheic lakes is necessary to
effectively protect the water resources in arid regions.
Denitrification, the process of reducing nitrate to dinitrogen
(N2), is considered the primary pathway for permanent nitrogen
(N) removal in aquatic ecosystems (Seitzinger, 1988). It plays an
important role in alleviating N pollution and maintaining the
self-purification capacity of ecosystems (Roland et al., 2018). The
availability of both nitrate and organic carbon are considered the
most important factors limiting denitrification rates (Seitzinger,
1988; Seitzinger et al., 2006; Xia et al., 2017; Jiang et al., 2020).
Salinity also has an important influence on denitrification (Koop-
Jakobsen and Giblin, 2010; Arce et al., 2013; Zhou et al., 2016).
Many endorheic lakes are naturally saline, as the evaporative
concentration process leads to salt accumulation (Yapiyev et al.,
2017), which comprises a diverse array of salts such as calcium,
sodium, potassium, sulfate, carbonate, and chloride (Heinrichs
and Walker, 2006). The change in salinity can cause decrease
or increase in cytoplasmic volume by imposing considerable
osmotic stress on the relevant microbes such as nitrifiers and
denitrifiers, resulting in the loss of metabolic activity (Ardon
et al., 2013; Zhao et al., 2013b; Neubauer et al., 2019). In
addition, salt water containing sulfate may have inhibitory or
promoting effects on nitrate reduction due to sulfide toxicity or
by providing electron donors for chemoautotrophic processes
from the reduction of sulfate (Aelion and Warttinger, 2010;
Zhu et al., 2018; Murphy et al., 2020). A consensus on these
mechanisms remains elusive, probably due to the differences in
microbial community structure involved in N cycling, which
is sensitive to salinity variation (Herbert et al., 2015; Zhou
et al., 2016). Lakes are hotspots of denitrification with high
N removal efficiency due to the long residence times of water
(Wollheim et al., 2008; Finlay et al., 2013). Previous research
about denitrification has mainly focused on out-flowing lakes.
We lack a direct understanding of the denitrification potential of
endorheic lakes in arid regions.
Climate change introduces a new challenge for endorheic
lakes (Tao et al., 2015; Zhang et al., 2017). In Northwest China,
temperatures have risen markedly in recent decades and faster
than in the surrounding regions (Shi et al., 2007; Yang et al.,
2020). Climate change can influence lakes either through higher
temperatures or by changes in salinity (Mosley, 2015; Greaver
et al., 2016), the latter is particularly influential in arid and
semiarid lakes (Brucet et al., 2012; Lin et al., 2017). Climate
change is affecting the hydrological cycle with more frequent
and intense precipitation, altered snow accumulation and melt,
and changes in evaporation (Sorg et al., 2012; Zhou et al., 2015),
leading to large-scale changes in lake salinity (Jeppesen et al.,
2015; Rusuli et al., 2015). Thus, how denitrification in endorheic
lakes will respond to climatically induced changes in lake salinity
is a key question.
Lake Bosten used to be the largest freshwater lake in the
endorheic basins of China and is of great importance as a water
supply for local domestic use and industrial and agricultural
production (Zhou et al., 2015; Wang et al., 2018b). Since the
1960s, Lake Bosten suffers from salinization and eutrophication
mainly caused by accelerated climate change and extensive
human activities (Guo et al., 2015b; Fontana et al., 2019). It has
changed from an oligotrophic freshwater lake to a mesotrophic
oligosaline lake (Tang et al., 2012; Dai et al., 2013). Lake Bosten
represents an interesting feature, which has a natural salinity
gradient (Tang et al., 2012; Dai et al., 2013). It provides an
ideal ecosystem in which to study the denitrification capacity
of endorheic lakes in arid regions as well as its response to
climatically induced changes in lake salinity.
Slurry incubations incorporating the 15N isotope-tracing
technique have been used as a powerful tool for estimating
potential denitrification rates in the field (Song et al., 2013; Yin
et al., 2014; Jiang et al., 2020) and simulation experiments (Salk
et al., 2017; Wang et al., 2018a; Murphy et al., 2020). Although
denitrification rates in slurries are usually significantly higher
than under in situ conditions due to the disruption of natural
profiles of sediments (Laverman et al., 2006), slurry incubation
is highly repeatable and flexible (Yin et al., 2014; Salk et al.,
2017). It is suitable for exploring the relative differences in
denitrification potential and estimating nitrate limitations by
adding extra nitrate (amended) and not adding extra nitrate
(unamended) to the slurries. During denitrification, nitrite and
nitrous oxide reductase enzymes can catalyze the reduction of
nitrite and nitrous oxide, which are encoded by the nirS/nirK and
nosZI/nosZII genes, respectively (Franklin et al., 2017; Neubauer
et al., 2019; Murphy et al., 2020). These genes commonly
used as an amplicon for quantifying or sequencing denitrifiers
(Throback et al., 2004). Quantifying the potential denitrification
rates, combined with the abundance of key genes, can provide
a comprehensive understanding of lake denitrification potential
(Murphy et al., 2020; Broman et al., 2021; Yang et al., 2022).
Here, we examine unamended and amended denitrification
rates at 17 sampling sites in Lake Bosten through the addition
of extra nitrate (100 µmol L−1) or otherwise to slurries, in
order to estimate potential denitrification rates. We determine
the abundance of nirS and nosZI genes in surface sediments
through qPCR to estimate the genetic potential of denitrification.
In addition, high throughput sequencing using nosZI gene
as an amplicon was conducted to estimate the microbial
community structure mediating denitrification. We test the
following hypotheses: (1) low nitrate concentration may be
a proximate control of denitrification rates in Lake Bosten;
(2) the sediment of different areas in Lake Bosten varies in
denitrification potential due to the difference in nitrate and
salinity levels; and (3) based on earlier studies about the
influence of salinity on denitrification, we hypothesize that
climate change can influence lake denitrification via changes in
salinity. Our study provides insights into the influence of changes
in salinity on N cycling in endorheic lakes and can be used to
predict future response of water quality to climate change in
arid regions.
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Jiang et al. Denitrification in Lake Bosten
MATERIALS AND METHODS
Study Area
Lake Bosten is located in the lowest area of the intermontane
Yanqi Basin between the Taklimakan Desert and Tien Shan,
Northwestern China. Winds come mainly from the southwest,
indicating dominant influences of westerlies throughout the
summer season (Ma et al., 2020; Yao et al., 2022). The mean
annual temperature was ∼9.1◦C, and the annual precipitation
was 76.3 mm. Lake Bosten has a surface area of ∼1,005 km2, a
maximum depth of 16 m, and an average depth of 8 m. Water
temperature and pH ranged from 23.5 to 24.9◦C and from 8.8 to
9.5, respectively (Supplementary Table S1).
The Kaidu River is the most important tributary in the area
and accounts for about 83% of the lake’s annual water inflow
runoff, which is supplied by melting ice, precipitation, and
groundwater (Chen et al., 2008; Rusuli et al., 2016). Other rivers
are small seasonal rivers, such as the Huangshui River, which
contributes to almost all the remaining 17% of inflow runoff
(Chen et al., 2008; Rusuli et al., 2016). A pumping station was
constructed in the southwestern part of Lake Bosten, which
pumps lake water into the Peacock River to adjust the outflow
of the lake (Yu et al., 2015; Zhou et al., 2017).
The freshwater inflow from the Kaidu River is removed
by the pumping station at the southwestern margin of Lake
Bosten, shaping a freshwater region in the southwest of Lake
Bosten (Kaidu River Estuary: KRE). The drainage channels of
agricultural production are mainly located in the northwestern
coastal area (NCA), making this area the most heavily polluted
in Lake Bosten. The rest of the area is the main lake area (MLA)
(Figure 1).
Collection and Pre-Treatment of Samples
Water and sediment samples, from 17 sites at Lake Bosten,
were collected in September 2019. Water samples from the top
(50 cm below the surface), middle, and bottom (50 cm above the
sediment) were collected using a polymethyl methacrylate water
sampler (UWITEC, Austria) and then mixed. Water samples
for dissolved nutrient analyses were filtered using 0.2 µm nylon
syringe filters immediately following the mixture in the field. The
surface sediments (about 3 cm depth) were collected with a 60 cm
long gravity corer (UWITEC, Austria), and then placed in clean
airtight plastic bags. Water temperature (WT), pH, dissolved
oxygen (DO), and salinity were measured at each sampling site
in situ, with a multiparameter water quality sonde (YSI 6600V2,
USA). All collected sediment and water samples were kept in a
cool and shaded place, and subsequently delivered to the Institute
of Lake Bosten.
Measurements of Unamended and
Amended Denitrification Rates
Unamended and amended denitrification rates were measured
using slurry incubations incorporating the 15N isotope-tracing
technique (Yin et al., 2014; Jiang et al., 2020). Sediment
samples were mixed with lake water at a ratio of 1:10 to
make homogenized slurries. The slurry was stirred continuously
and purged with helium for 40 min. The purged slurries were
distributed into 12 ml vials (Labco Exetainer, UK), and then
immediately sealed. Subsequently, preincubation was conducted
at the in situ temperature on a shaker table (200 rpm) for 24 h, to
eliminate residual nitrate and DO. After preincubation, a certain
amount of 15N-nitrate (99 atom%) solution was injected into a
group of vials to determine the unamended denitrification rates
according to the nitrate concentrations of the water column in
Lake Bosten. Simultaneously, a high 15N-nitrate level (a final
concentration of 100 µmol L−1) was injected into another group
of vials to estimate the amended potential rates. Subsequently,
three of the vials were randomly selected from each group and
immediately preserved with the addition of 200 µL ZnCl2as the
initial samples for the measurement of denitrification rates. The
remaining vials were incubated under the same conditions for
2, 4, and 8 h, and then used to measure the production of 29N2
and 30N2.
Dissolved 29N2and 30 N2were determined using membrane
inlet mass spectrometry (MIMS) analysis (Kana et al., 1998). The
unamended and amended denitrification rates were calculated
according to the following equation:
R=K×V
W(1)
where R(µmol N kg−1h−1) indicates the measured
15N-based unamended or amended denitrification rates, Kis
the slope calculated from the concentration of 15N-N2vs.
incubation time (Supplementary Figure S1), V(L) is the volume
of the incubation vial, and W(kg) denotes the dry weight of
the sediment.
DNA Extraction and Real-Time
Quantitative PCR (qPCR)
Genomic DNA was extracted from the sediment samples using
the FastDNATM Spin kit for soil (MP Biomedicals) according
to the manufacturer’s instructions. The quality and quantity
of DNA were checked using agarose gel electrophoresis and
using a NanoDrop ND-1000 UV/Vis spectral photometer. The
quality of DNA extracted in each sampling site was exhibited in
Supplementary Table S2. Extracts were stored at −80◦C prior to
gene quantification. The sampling site of BST06 and BST13 were
removed from the following molecular biological analysis due to
low DNA quality.
qPCR was used to quantify functional genes for enzymes
of nitrification (AOB and AOA) (Rotthauwe et al., 1997;
Francis et al., 2005) and denitrification (nirS and nosZI)
(Throback et al., 2004). Triplicate qPCR reactions were set
up for each sample. The primers, thermocycling conditions,
and relevant references are included in the supplemental
information (Supplementary Table S3). The total qPCR
reaction volume of 20 µl contained 10 µl of SYBR green qPCR
Master Mix, 1 µl of forward primer, 1 µl of reverse primer,
7µl of ddH2O, and 1 µl of the template (DNA). Reactions
were performed using an EcoTM Real-Time PCR System.
Melting curves were checked for each reaction to confirm
the purity of the amplified products. Standard curves were
obtained using 10-fold serial gradient dilutions of standard
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Jiang et al. Denitrification in Lake Bosten
FIGURE 1 | Map of Lake Bosten, showing study area, sampling sites and electrical conductivity (EC) in water column. Electrical conductivity was the average value
from 2010 to 2019, which derived from the long-term monitoring of the institute of Lake Bosten. The lake area was divided into three subregions according to the EC
gradient: Kaidu River Estuary (KRE), Main Lake Area (MLA) and Northwestern Coastal Area (NCA).
plasmids containing targeted genes with known copy numbers.
The qPCR amplification efficiencies and other calibration
curve parameters are listed in Supplementary Table S4.
Gene abundance was calculated based on the constructed
standard curve and then converted into copies per gram of
dry sediment.
High-throughput Sequencing
The microbial reduction of nitrous oxide to N2is catalyzed
by nitrous oxide reductase. The nosZI gene was sequenced
to explore the microbial community structure performing
complete denitrification across the lake using the primer pairs
nosZ-F/nosZ1622R (Throback et al., 2004). The purified DNA
products were sent to Shanghai Personal Biotechnology Co.,
Ltd for high-throughput sequencing using the Illumina MiSeq
platform. Paired-end sequencing reads were merged using
FLASH (Fast Length Adjustment of Short reads, v1.2.11) (Magoc
and Salzberg, 2011). Adapters and primers were trimmed off
all the reads using Cutadapt (v1.9.1). Sequences shorter than
400 bp, lower than 25 quality scores, and suspected to be
chimeras were discarded using USEARCH (v10.0.240) (Edgar
and Flyvbjerg, 2015). The sequences were initially grouped at
97% of the sequence similarities, and representative sequences
were translated and compared to the nosZ reference sequence
in GenBank using BLASTx. Frameshift errors were removed.
Subsequently, the high-quality sequences were aligned based
on the amino acid residues and grouped based on 85% of the
nucleotide sequence similarities to form a new OTU table for the
subsequent analysis.
Chemical Analysis of Water and Sediment
Physicochemical Parameters
Dissolved organic carbon (DOC) was determined using a
TOC analyzer (Teledyne Tekmar, Torch, USA). Acid volatile
sulfides (AVS) in sediments were determined with the following
methods. Sulfide in sediment samples was converted into H2S
by HCl extraction for 1 h. Subsequently, released H2S was
captured in a NaOH solution with a continuous N2flow.
The dissolved sulfide concentration in the NaOH solution
was measured spectrophotometrically by the methylene blue
method. The other physicochemical parameters, including total
nitrogen (TN), nitrate, ammonium, sulfate, sediment total
organic carbon (STOC), and sediment total nitrogen (STN)
were determined following standard methods detailed in Jiang
et al. (2020).
Statistical Analyses
The statistical analyses were performed using R 3.5.3 and
the RStudio 1.1.462 interface. Kruskal–Wallis rank tests and
one-way ANOVA were used to evaluate the differences in
environmental factors, gene abundances, species diversity,
and denitrification rates among areas, determining statistically
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Jiang et al. Denitrification in Lake Bosten
FIGURE 2 | Spatial distribution of the physicochemical parameters in the overlying water [Salinity, Dissolved Oxygen (DO), Nitrate, Ammonium, Total Nitrogen (TN),
Sulfate and Dissolved Organic Carbon (DOC)] and sediments [Sediment Total Organic Carbon (STOC), Sediment Total Nitrogen (STN) and Acid volatile sulfides (AVS)]
in Lake Bosten.
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Jiang et al. Denitrification in Lake Bosten
FIGURE 3 | Spatial distribution of the unamended (A) and amended (B) denitrification rates in Lake Bosten.
significant differences when p<0.05. Alpha diversity indices,
unconstrained PCoA analysis, and redundancy analysis (RDA)
were constructed with the “vegan” package in R. Pearson
correlations were used to examine the relationships between
parameters of denitrification and environmental properties.
Data visualization was performed using the package “ggplot2”
in R.
RESULTS
The Physicochemical Parameters of the
Water and Sediment in Lake Bosten
In Lake Bosten, dissolved oxygen and salinity ranged from 6.9 to
10.8 mg L−1and from 0.51‰ to 0.81‰, respectively. Dissolved
oxygen in NCA was significantly higher than that in KRE and
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Jiang et al. Denitrification in Lake Bosten
MLA, while salinity in KRE was significantly lower than that in
MLA and NCA. The concentrations of nitrate and TN exhibited
a decreasing trend from KRE to NCA. Especially for nitrate,
the values in KRE were 3–4 times higher than the values in
MLA and NCA, which ranged from 0.1 to 0.4 mg L−1. The
concentrations of TN ranged from 0.7 to 1.3 mg L−1, and the
values in KRE were significantly higher than that in NCA. In
contrast, the opposite trend was found for sulfate, DOC, STOC,
STN, and AVS, which ranged from 140 to 413 mg L−1, from 5.3
to 12.0 mg L−1, from 10.0 to 58.3 mg g−1, from 2.2 to 6.1 mg
g−1and from 3.9 to 26.1 µmol g−1, respectively. Ammonium
concentrations ranged from 0.1 to 0.4 mg L−1, and there was
no significant variation among the three areas in Lake Bosten
(Figure 2).
Unamended and Amended Denitrification
Rates
Unamended and amended denitrification rates ranged from
2.24 to 6.08 µmol N kg−1h−1and from 12.87 to 77.63
µmol N kg−1h−1, respectively, in Lake Bosten, and the
amended rates were about 8.9 times those of the unamended
rates (Figures 3A,B). These sampling sites showed considerable
variation in amended denitrification rates. Generally, the
amended rates were highest in KRE, intermediate in MLA,
and lowest in NCA. In contrast, in unamended denitrification
rates, the differences were small among sampling sites in
Lake Bosten.
The Abundance of Functional Genes for
Nitrification and Denitrification
The bacterial amoA gene copy numbers ranged from 9.45 ×
102copies g−1of sediment at site BST13 to 8.30 ×104copies
g−1of sediment at site BST4 (Figure 4A). The archaeal amoA
gene copy numbers ranged from undetected values to 1.15 ×
104copies g−1of sediment, and there was a decreasing trend
from KRE to NCA (Figure 4B). The abundance of the AOB gene
was higher than the abundance of the AOA gene in most of the
sampling sites.
Copy numbers of the nirS gene and nosZI genes ranged from
1.89 ×107to 1.49 ×108copies g−1of sediment and from
4.84 ×107to 4.85 ×108copies g−1of sediment, respectively
(Figures 4C,D). The abundance of the nosZI gene exceeded the
abundance of the nirS gene at most sites. There was a decreasing
trend in the abundance of the nirS gene and nosZI gene from
KRE to NCA.
The Community Structure of Denitrifying
Microorganisms
Alpha-diversity analysis revealed a decreasing trend in the
diversity indexes of Richness, Shannon, and Simpson from KRE
to NCA (Supplementary Figure S2). Unconstrained principal
coordinates analysis (PCoA) with Bray–Curtis distance showed
the community variation of nitrous oxide reducers among
different sampling sites (Supplementary Figure S3). The results
showed that the first two axes explained 87.3% of the microbial
FIGURE 4 | Spatial distribution of the abundances of AOB (A),AOA (B),nirS
(C), and nosZI (D) genes in Lake Bosten.
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Jiang et al. Denitrification in Lake Bosten
FIGURE 5 | Redundancy analyses (RDA) ordination plots showing the significant environmental factors in structuring variations in the community composition of
nitrous oxide reducer in Lake Bosten. Significance levels: *corrected p-value <0.05. KRE, Kaidu River Estuary; MLA, Main Lake Area; NCA, Northwestern Coastal
Area.
community variation. The microbial community of nitrous oxide
reducers was significant differences among the three areas in
Lake Bosten (p<0.05). The forward selection procedure in
RDA revealed that the variation in the microbial community
of nitrous oxide reducer was significantly explained by salinity
and ammonium, which described 21.3 and 21.5% of the total
variation, respectively (Figure 5).
DISCUSSION
Nitrate Availability Limited Unamended
Denitrification Rates
The main objective of this study was to explore the denitrification
potential of Lake Bosten and its response to increasing inputs of
nutrients and changes in salinity. Amended denitrification rates
increased by one order of magnitude compared to unamended
rates in response to additional nitrate at most of the sites,
indicating the high potential of denitrification in Lake Bosten.
The availability of nitrate is considered one of the most important
limiting factors for denitrification in lakes and other aquatic
ecosystems (Pina-Ochoa and Alvarez-Cobelas, 2006; Seitzinger
et al., 2006). In Lake Bosten, nitrate concentrations in the
water positively correlated with unamended denitrification rates
(Table 1), indicating that low nitrate concentrations may limit
unamended denitrification rates. Nitrate can be supplied as
an external input or by in situ nitrification. The coupled
nitrification-denitrification process usually dominates N removal
in ecosystems of nitrate limitation (Koop-Jakobsen and Giblin,
2010; Xia et al., 2017). In Lake Bosten, the abundance of either
the AOB or AOA gene was low compared to the equivalent
values in most freshwater lakes by at least one order of
magnitude (Wu et al., 2010; Hou et al., 2013; Zhao et al.,
2013a; Bollmann et al., 2014; Liu et al., 2014). Meanwhile,
the concentrations of ammonium were significantly higher
than those of nitrate, perhaps indicating that nitrification
was inhibited. Therefore, both the low nitrate concentrations
and abundances of nitrifiers may limit denitrification rates in
Lake Bosten.
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Jiang et al. Denitrification in Lake Bosten
TABLE 1 | Pearson’s correlation analysis between denitrification rates (amended and unamended) and environmental variables (n=17) and between functional gene
abundance (nirS, nosZI,AOB, and AOA) and environmental variables (n=15).
Denitrification rates Functional gene abundance
Amended Unamended nirS nosZI AOB AOA
Nitrate 0.41 0.51* 0.37 0.66** 0.02 −0.01
Ammonium 0.10 0.10 0.13 0.24 −0.07 0.20
TN 0.28 0.51* 0.39 0.49 0.08 −0.09
Sulfate −0.59* −0.44 −0.69** −0.81** −0.11 −0.17
DOC −0.14 −0.21 −0.54* −0.36 0.06 −0.07
STOC −0.62** −0.26 −0.40 −0.53* −0.31 −0.22
STN −0.61** −0.25 −0.34 −0.47 −0.31 −0.13
AVS −0.53* 0.04 −0.45 −0.24 −0.36 −0.26
WT 0.25 0.03 0.20 −0.03 0.15 0.41
pH 0.12 −0.22 −0.12 −0.25 0.51* −0.01
DO −0.56* −0.13 −0.57* −0.32 −0.24 −0.39
Salinity −0.50* −0.48 −0.49 −0.62** 0.01 −0.08
The coefficients (r) are shown. Significance levels: *p-value <0.05, **p-value <0.01. Environmental variables include nitrate, ammonium, total nitrogen (TN), sulfate, dissolved organic
carbon (DOC), sediment total organic carbon (STOC), sediment total nitrogen (STN), acid volatile sulfides (AVS), water temperature (WT), pH, dissolved oxygen (DO) and salinity.
The Influence of Changes in Salinity on
Denitrification
In Lake Bosten, there is heterogeneity in denitrification potential.
The sediments in KRE had the highest amended denitrification
rates. Nitrate loads mainly derive from the transportation of the
Kaidu River in Lake Bosten (Yu et al., 2015; Zhou et al., 2017),
which exhibited an obvious decline in nitrate from the estuary
to the east section (Figure 2). This phenomenon indirectly
reflects a high potential of N removal in KRE. In contrast,
the denitrification potential in NCA was low, suggesting that
other environmental factors constrained denitrification except
for nitrate availability.
Amended denitrification rates were negatively correlated with
salinity and sulfate concentrations in Lake Bosten (Table 1),
perhaps indicating that salinity is a key regulating factor of
denitrification. Climate change is affecting the hydrological cycle
of Lake Bosten and consequent effects on concentration or
dilution will alter lake salinity (Rusuli et al., 2015; Liu and Bao,
2020). In addition, there is a continuous input of salinity from
salt leaching associated with the agricultural irrigation of the
northwestern basin (Tang et al., 2012; Guo et al., 2015b). In the
past 60 years, Lake Bosten has evolved from freshwater to an
oligosaline lake. Salinity has become a dominant factor shaping
the bacterial community in the water and sediment of Lake
Bosten (Tang et al., 2012; Dai et al., 2013).
Salinity can affect denitrification in many respects.
Considerable studies have reported that salinity directly inhibits
the metabolic activity of denitrification, through osmotic stress
and sulfide toxicity (Ruiz-Romero et al., 2009; Ardon et al., 2013;
Zhao et al., 2013b; Neubauer et al., 2019). Sulfate is the main
component of salt anions in Lake Bosten, which is consistent
with the changes in salinity (r=0.83, p<0.01). High sulfate
can enhance the accumulation of toxic sulfide in sediments
(Aelion and Warttinger, 2010; Zhu et al., 2018; Murphy et al.,
2020) and then inhibit denitrification rates. Furthermore, the
influence of salinity on denitrification depends on the long-term
salinity adaptation of denitrifying microorganisms (Franklin
et al., 2017; Wang et al., 2018a; Murphy et al., 2020). Many
studies have shown that salinity is the most important factor in
structuring communities of denitrifying microorganisms, such
as nosZ-denitrifiers (Cai et al., 2019; Wang et al., 2019; Han et al.,
2021), and that salinity can affect denitrification rates by altering
the abundance and diversity of denitrifying microorganism. In
Lake Bosten, there was a significant correlation between the
abundance of the nirS and nosZI genes (r=0.79, p<0.01).
Salinity or sulfate was negatively correlated with the abundance
of nirS and nosZI, respectively, and the latter was the stronger.
The nitrous oxide reducers are more sensitive to osmotic stress
and ionic toxicity than the nitrite reducers (Laverman et al.,
2007; Zhou et al., 2016). In addition, the species diversity of
nitrous oxide reducers significantly decreased with the increase
of salinity or sulfate in Lake Bosten (p<0.01). Elevated salinity
appears to decrease the abundance and diversity of nitrous oxide
reducers, resulting in incomplete denitrification.
Salinity also indirectly affects denitrification by inhibiting
nitrification rates or altering the physicochemical environment
(Herbert et al., 2015; Zhou et al., 2016; Franklin et al., 2017).
Previous research also suggests that toxic sulfide can inhibit
microbial activity related to nitrification (Herbert et al., 2015;
Wang et al., 2020), while some investigations conducted in other
habitats showed moderate salinity in favor of nitrification (Zhou
et al., 2016; Wang et al., 2018a). In this study, the abundances of
AOB and AOA genes were not correlated with salinity, sulfate,
and AVS, indicating that the differences in gene abundances
were not attributed to the changes in salinity. Further research
is needed to reveal the underlying mechanisms of low gene
abundance mediated nitrification in Lake Bosten. In addition,
amended denitrification rates were negatively correlated with
Frontiers in Microbiology | www.frontiersin.org 9July 2022 | Volume 13 | Article 922546

Jiang et al. Denitrification in Lake Bosten
STOC and DO in Lake Bosten. Elevated salinity might constrain
the activities of microbes and reduce the deposition of organic
carbon and the consumption of DO, thus inhibiting the
anaerobic denitrifying process. Neubauer et al. (2019) also
reported that denitrification rates were reduced due to the
decrease in oxygen demand induced by salinization.
The Response of Endorheic Lakes to
Climate Change in Northwest China
The arid region of Northwest China has been getting warmer
and wetter in recent decades because of the enhancement of the
westerly circulation (Yang et al., 2021; Yao et al., 2022). Glacial
melt leads to increased runoff, which carries a large amount
of silt as well as plant and animal residues (Sorg et al., 2012;
Guo et al., 2015b). Meanwhile, the decomposition of organic
matter and the release of nutrients may be enhanced by the
increasing temperature (Wik et al., 2016; Jane et al., 2021).
Thus, climate warming may lead to an increase in nutrient
input into lakes from the watershed. For example, climate
warming and consequent glacial melt led to the increasing
inflow of the Kaidu River into Lake Bosten in 2013 (Guo
et al., 2015a). Meanwhile, nitrate concentration in the Kaidu
River estuary has been fluctuating but increasing in recent
years (Supplementary Figure S4). However, a decreasing trend
in nitrate concentration was observed in Lake Bosten. This may
be because the increase in water level led to the decrease in
salinity and nitrate concentrations through dilution. In addition,
the estuary area of the Kaidu River has excess capacity to remove
additional nitrate, which plays an important role in regulating
and alleviating external nitrate loads, especially with the decrease
of salinity.
In Northwest China, the influence of climate change on the
water quality of endorheic lakes is complicated. On the one hand,
the external nutrient inputs may increase, accompanied by an
increase in the quantity of runoff and climate warming, but on
the other hand, the pollution will be alleviated due to dilution and
the decrease of salinity. Although climate change had a positive
effect on the water quality of Lake Bosten so far, long-term
trajectories of water quality are difficult to predict. Accelerated
climate warming will cause glacier shrinkage and decreased snow
cover in the future (Sorg et al., 2012; Zhou et al., 2015). This
brings large uncertainties into predictions of the changes in
runoff, water level, and salinity. Effective management decisions
are essential for maintaining the water quantity, salinity, and
denitrification capacity of lakes in the face of accelerated climate
change and extensive human activities.
DATA AVAILABILITY STATEMENT
The data presented in the study are deposited in the
China National Center for Bioinformation, accession number
CRA006560 (https://www.cncb.ac.cn/).
AUTHOR CONTRIBUTIONS
XJ: conceptualization, methodology, investigation, writing—
original draft, visualization, and funding acquisition. CL and
YH: investigation and data curation. KS: formal analysis and
project administration. XT: writing—review and editing. GG and
BQ: conceptualization, writing—review andediting, and funding
acquisition. All authors contributed to the article and approved
the submitted version.
FUNDING
This study was financially supported by the National Natural
Science Foundation of China (grant numbers: 41790423 and
U2003205) and National Key R&D Program of China (grant
numbers: 2019YFA0607100).
ACKNOWLEDGMENTS
We thank the Institute of Lake Bosten, Environmental
Protection Bureau of Bayingolin Mongolia Autonomous
Prefecture, Korle, China for providing the data, instruments
and labs.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fmicb.
2022.922546/full#supplementary-material
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Frontiers in Microbiology | www.frontiersin.org 12 July 2022 | Volume 13 | Article 922546