Research papersUnraveling influences of nitrogen cycling on arsenic enrichment in groundwater from the Hetao Basin using geochemical and multi-isotopic approaches
Introduction
Co-occurrence of nitrogen species (e.g., organic nitrogen, NH4+, NO2–, and NO3–) and arsenic (As) has been increasingly commonly observed in aquifers worldwide (Norrman et al., 2015, Smith et al., 2017, Weng et al., 2017, Du et al., 2020). In groundwater systems, NO3– may be artificially sourced from manure and fertilizers or naturally from atmospheric deposition and nitrification processes (Zhang et al., 2012). However, NH4+ contamination generally occurs artificially due to organic waste disposal and naturally from organic matter degradation (Böhlke et al., 2006). Naturally occurring high-As (>10 μg/L) groundwater has become increasingly of great concern posing severe public health consequences to hundreds of millions of people worldwide (Podgorski and Berg, 2020). Under reducing conditions, the reductive dissolution of As-bearing Fe(III) oxides stimulated by organic matter (including organic nitrogen) mineralization has been accepted as the primary mechanism of As mobilization (Glodowska et al., 2020). Under redox-changing environments, As levels are generally regulated by microbially-mediated Fe(III) oxide reduction and Fe(II) oxidation in groundwater systems (Schaefer et al., 2016). Transformations between Fe(III) oxides and dissolved Fe(II) species may be mediated by nitrogen cycling (Senn and Hemond, 2002, Smith et al., 2017), which thus influences As mobility in groundwater.
Co-cycling of nitrogen species are important biogeochemical processes in aquifers (Rivett et al., 2008, Canfield et al., 2010). Under oxic conditions, NH4+ is naturally sourced from progressive organic nitrogen mineralization, which is further oxidized into NO3– via nitrification processes (Kelley et al., 2013). In suboxic to anoxic environments, NO3– is reduced via denitrification (Lutz et al., 2020). Dissimilatory NO3– reduction to NH4+ (DNRA) may also occur under favorable conditions (Rütting et al., 2011). Nitrate denitrification typically occurs in groundwater with limited dissolved organic carbon (DOC), while DNRA is favored when NO3– concentrations are limited (Rivett et al., 2008, Kraft et al., 2014). Nitrite produced from NO3– denitrification may facilitate anaerobic NH4+ oxidation coupled to NO2– reduction (termed anammox) in the presence of anammox bacteria (Zhu et al., 2013). However, anaerobic NH4+ oxidation coupled to Fe(III) oxide reduction (termed Feammox) can be mediated by Fe(III)-reducing bacteria (Yang et al., 2012). Ammonium adsorption is a ubiquitous NH4+ retardation process in aquifers (Böhlke et al., 2006, Nikolenko et al., 2018).
Characterizing sources and natural cycling processes with respect to NO3– and NH4+ in groundwater has been of increasing concern (Rivett et al., 2008, Nikolenko et al., 2018, Xin et al., 2019) and typically utilize stable isotope measurements (e.g., δ15NNO3, δ18ONO3, and δ15NNH4). The 15NNO3 is enriched by fractionation effects via denitrification and DNRA but is depleted via partial nitrification (Böhlke et al., 2006). The 15NNH4 could be enriched by nitrification, Feammox, and anammox, and depleted by DNRA and NH4+ adsorption processes, but organic nitrogen mineralization does not typically show nitrogen isotope fractionation (Nikolenko et al., 2018). In addition to 15N tracer experiments (e.g., 15NO3- and 15NH4+), anammox, Feammox, and DNRA processes were validated through microbiological techniques (Engström et al., 2005, Yang et al., 2012, Ding et al., 2014, Hardison et al., 2015). However, to the best of our knowledge, few have provided direct field evidence of anammox (Böhlke et al., 2006, Clark et al., 2008, Kroeger and Charette, 2008), Feammox, and DNRA (Rütting et al., 2011, Liang et al., 2020) by utilizing NO3– and NH4+ isotopic signatures in groundwater systems.
Identifying electron donors for NO3– denitrification (or DNRA) is another important issue. Both organic matter (Eq. (1): termed as heterotrophic denitrification or DNRA) and FeS2 or Fe(II) (Eqs. (2), (3): termed as autotrophic denitrification or DNRA) may be utilized as electron donors in NO3– reduction (Robertson et al., 1996, Pauwels et al., 2000, Rivett et al., 2008, Roberts et al., 2014). In heterotrophic denitrification or DNRA, 12C-labeled organic matter is preferentially degraded to yield 13C-depleted HCO3– (Widory et al., 2005). The 34S-depleted SO42- is produced in groundwater in autotrophic denitrification or DNRA utilizing FeS2 as the electron donor (Böhlke et al., 2002, Otero et al., 2009). Based on multi-isotopic signatures (e.g., δ15NNO3, δ18ONO3, δ34SSO4, and δ13CDIC), potential electron donors for NO3– denitrification have been previously evaluated (Böhlke et al., 2002, Hosono et al., 2014, Hosono et al., 2015, Zhang et al., 2012, Puig et al., 2017). High DOC, FeS2, and Fe(II) concentrations were reported as enhancing NO3– denitrification or DNRA processes (Sayama et al., 2005, Roberts et al., 2014, Robertson and Thamdrup, 2017, Rahman et al., 2019). However, whether heterotrophic or autotrophic denitrification/DNRA dominates in FeS2-containing anoxic aquifers has not been well understood.
Increasing evidence has indicated that As concentration is closely related to different nitrogen species in groundwater (Senn and Hemond, 2002, Norrman et al., 2015, Smith et al., 2017, Weng et al., 2017, Xiu et al., 2020). Low dissolved As concentrations generally occur in oxic-suboxic aquifers with elevated NO3– concentrations due to strong As adsorption on Fe(III) oxides (Senn and Hemond, 2002, Smith et al., 2017). Ammonium is believed to be primarily sourced from microbially-mediated organic matter degradation, which facilitates Fe(III) oxide reduction and thereby releases Fe(II) and As (Harvey et al., 2002). Elevated NH4+ concentrations have been regarded as a proxy of high organic matter degradation rates and As concentrations (Dowling et al., 2002, Postma et al., 2007, Gao et al., 2020). Feammox, anammox, and DNRA processes may take place in groundwater and influence NH4+ concentrations. A microbial study indicated that Feammox may occur under favorable conditions in aquifers (Xiu et al., 2020). However, the distributions of Feammox, anammox, and DNRA in high As-containing groundwater and their effects on dissolved Fe(II) and As concentrations remain unclear. Therefore, knowledge of nitrogen-species cycling is crucial in revealing the mechanisms of As enrichment in aquifer systems.
By using multi nitrogen isotopes, most studies focused on delineating nitrogen behavior and fate (Nikolenko et al., 2018 and references therein; Liang et al., 2020), but few studies explained the relationship between nitrogen cycling and As enrichment processes (Smith et al., 2017, Weng et al., 2017). This study aims to (1) evaluate primary sources and cycling processes of NO3– and NH4+ in groundwater, and (2) provide a detailed picture of As enrichment processes in nitrogen cycling systems. Spatial distributions of geochemical compositions (e.g., NO3–, NH4+, Fe(II), and As concentrations) and multi-isotopic signatures (e.g., δ15NNO3, δ18ONO3, δ15NNH4, δ13CDIC, and δ13CDOC) of groundwater in different redox zones from alluvial-pluvial aquifers in the Hetao Basin of China were investigated.
Section snippets
Study area
The Hetao Basin is a typical alluvial-pluvial basin and is located north of the Yellow River and south of the Langshan Mountains in the northwest of Inner Mongolia, China (Fig. 1). Our previous studies have shown that aquifers in the study area can be divided into three redox zones: the alluvial fan, transition area, and flat plain (Guo et al., 2016a, Gao et al., 2020). The alluvial fan is located in the recharge area under oxic conditions; the transition area is situated between the alluvial
Water chemistry, arsenic, and nitrogen species
The physicochemical parameters of water samples are summarized in Table S1 and Fig. 2. The groundwater pH spread over a wide range of 7.04–8.66, which generally increased from Zones I to II and slightly decreased in Zone III in deep groundwater. The shallow groundwater in Zone IV had relatively higher pH values compared with deep groundwater. The total dissolved solids (TDS) concentration varied by a factor of approximately 20 from 122 to 2,840 mg/L in groundwater samples, 40% of which had TDS
Nitrification in Zone I
Extremely high dissolved NO3– concentrations (up to 172 mg/L) being associated with low δ15NNO3 (6.3‰ to 10.7‰) and δ18ONO3 (-2.5‰ to 3.0‰) were obtained in deep groundwater from Zone I (Fig. 5). This suggests the occurrence of NH4+ nitrification in Zone I. Previous studies have shown that δ15NNO3 and δ18ONO3 of newly formed NO3– from in-situ NH4+ nitrification should theoretically be in the ranges of 2‰ to 10‰ and −10‰ to 10‰, respectively (Kendall, 1998, Lohse et al., 2013, Kelley et al., 2013
Conclusions
A detailed picture of the nitrogen cycling processes and their impacts on As mobility were presented based on multi-isotopic signatures and cross correlations among dissolved nitrogen species, Fe(II), and As concentrations. In the study area, groundwater NH4+ was primarily sourced from organic nitrogen mineralization in the four considered zones. Negative δ15NNH4 (low to −13.2‰) being associated with extremely high DOC:NO3– molar ratios (up to 406 mol/mol) supports DNRA as an important NH4+
CRediT authorship contribution statement
Zhipeng Gao: Writing - original draft, Visualization, Conceptualization, Software. Haicheng Weng: Methodology, Data curation, Investigation. Huaming Guo: Writing - review & editing, Project administration, Resources, Supervision, Validation, Funding acquisition.
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.
Acknowledgements
The study was financially supported by the National Natural Science Foundation of China (grant Nos. 41825017 and 41672225), 111 project (No. B20010), the Fundamental Research Funds for the Central Universities (grant Nos. 2652018189 and 2652017165).
References (103)
- et al.
Isotopic fractionation of oxygen and nitrogen in coastal marine sediments
Geochim. Cosmochim. Acta
(1997) - et al.
Using isotope fractionation of nitrate-nitrogen and nitrate-oxygen for evaluation of microbial denitrification in a sandy aquifer
J. Hydrol.
(1990) - et al.
Nitrogen loss from anaerobic ammonium oxidation coupled to Iron(III) reduction in a riparian zone
Environ. Pollut.
(2017) - et al.
Anaerobic ammonium oxidation by nitrite (anammox): Implications for N2 production in coastal marine sediments
Geochim. Cosmochim. Acta
(2005) - et al.
A dual isotope approach to identify denitrification in groundwater at a river-bank infiltration site
Water Res.
(2003) - et al.
A review of high arsenic groundwater in Mainland and Taiwan, China: Distribution, characteristics and geochemical processes
Appl. Geochem.
(2014) - et al.
Incompatible distributions of groundwater arsenic and uranium in the Hetao basin, Inner Mongolia: Implication for origins and fate controls
Sci. Total Environ.
(2016) - et al.
Controls of organic matter bioreactivity on arsenic mobility in shallow aquifers of the Hetao Basin, P.R China
J. Hydrol.
(2019) - et al.
Influence of organic carbon and nitrate loading on partitioning between dissimilatory nitrate reduction to ammonium (DNRA) and N2 production
Geochim. Cosmochim. Acta
(2015) - et al.
An isotope study of the sources of nitrate in Malta’s groundwater
J. Hydrol.
(2012)
Nitrogen, carbon, and sulfur isotopic change during heterotrophic (Pseudomonas aureofaciens) and autotrophic (Thiobacillus denitrificans) denitrification reactions
J. Contam. Hydrol.
Combined use of δ13C, δ15N, and δ34S tracers to study anaerobic bacterial processes in groundwater flow systems
Water Res.
Hydrogeochemical zonation and its implication for arsenic mobilization in deep groundwaters near alluvial fans in the Hetao Basin, Inner Mongolia
J. Hydrol.
Tracing nitrogen sources and cycling in catchments
Nitrate nitrogen and oxygen isotope ratios for identification of nitrate sources and dominant nitrogen cycle processes in a tile-drained dryland agricultural field
Soil Biol. Biochem.
Hydrogeological controls on ammonium enrichment in shallow groundwater in the central Yangtze River Basin
Sci. Total Environ.
Nitrogen reduction processes in paddy soils across climatic gradients: Key controlling factors and environmental implications
Geoderma
Modelling nitrogen and oxygen isotope fractionation during denitrification in a lacustrine redox-transition zone
Geochim. Cosmochim. Acta
15N isotope biogeochemistry and natural denitrification process in groundwater: Application to the chalk aquifer of northern France
Geochim. Cosmochim. Acta
Natural organic matter in sedimentary basins and its relation to arsenic in anaerobic ground water: the example of West Bengal and its worldwide implications
Appl. Geochem.
Isotopic composition of nitrogen species in groundwater under agricultural areas: A review
Sci. Total Environ.
Tracing sources of ammonium in reducing groundwater in a well field in Hanoi (Vietnam) by means of stable nitrogen isotope (δ15N) values
Appl. Geochem.
Monitoring groundwater nitrate attenuation in a regional system coupling hydrogeology with multi-isotopic methods: The case of Plana de Vic (Osona, Spain)
Agr. Ecosyst Environ.
Denitrification and mixing in a schist aquifer: influence on water chemistry and isotopes
Chem. Geol.
Benthic metabolism and the fate of dissolved inorganic nitrogen in intertidal sediments
Estuar. Coast. Shelf Sci.
Arsenic in groundwater of the Red River floodplain, Vietnam: controlling geochemical processes and reactive transport modeling
Geochim. Cosmochim. Acta
Characterizing sources and natural attenuation of nitrate contamination in the Baix Ter aquifer system (NE Spain) using a multi-isotope approach
Sci. Total Environ.
Role of organic carbon, nitrate and ferrous iron on the partitioning between denitrification and DNRA in constructed stormwater urban wetlands
Sci. Total Environ.
Nitrate attenuation in groundwater: A review of biogeochemical controlling processes
Water Res.
Attenuation of nitrate in aquitard sediments of southern Ontario
J. Hydrol.
The fate of nitrogen is linked to iron(II) availability in a freshwater lake sediment
Geochim. Cosmochim. Acta
Unexpectedly high degree of anammox and DNRA in seagrass sediments: Description and application of a revised isotope pairing technique
Geochim. Cosmochim. Acta
Origin of high ammonium, arsenic and boron concentrations in the proximity of a mine: Natural vs. anthropogenic processes
Sci. Total Environ.
Nitrogen and carbon isotopic composition of marineand terrestrial organic matter in Arctic Ocean sediments:implications for nutrient utilization and organicmatter composition
Deep-Sea Res. I
Anoxic nitrate reduction coupled with iron oxidation and attenuation of dissolved arsenic and phosphate in a sand and gravel aquifer
Geochim. Cosmochim. Acta
Influence of temperature and pH on the anammox process: A review and meta-analysis
Chemosphere
Anammox and denitrification separately dominate microbial N-loss in water saturated and unsaturated soils horizons of riparian zones
Water Res.
Isotopic evidence of nitrogen sources and nitrogen transformation in arsenic-contaminated groundwater
Sci. Total Environ.
Community N and O isotope fractionation by sulfide-dependent denitrification and anammox in a stratified lacustrine water column
Geochim. Cosmochim. Acta
Microbial and hydrological influences on nitrate isotopic composition in an agricultural lowland catchment
J. Hydrol.
The missing nitrogen pieces: A critical review on the distribution, transformation, and budget of nitrogen in the vadose zone-groundwater system
Water Res.
Linking microbial community composition to hydrogeochemistry in the western Hetao Basin: Potential importance of ammonium as an electron donor during arsenic mobilization
Environ. Int.
Mechanisms of nitrate accumulation in highly urbanized rivers: Evidence from multi-isotopes in the Pearl River Delta
China. J. Hydrol.
Tracking nitrogen pollution sources in plain watersheds by combining high-frequency water quality monitoring with tracing dual nitrate isotopes
J. Hydrol.
Analysis of δ15N and δ18O to identify nitrate sources and transformations in Songhua River, Northeast China
J. Hydrol.
Use of multiple isotope tracers to evaluate denitrification in ground water: study of nitrate from a large-flux septic system plume
Ground Water
Controls on Nitrogen Loss Processes in Chesapeake Bay Sediments
Environ. Sci. Technol.
Groundwater residence time and aquifer recharge in multilayered, semi-confined and faulted aquifer systems using environmental tracers
J. Hydrol.
Nitrogen isotope effects induced by anammox bacteria
Proc. Natl. Acad. Sci. USA
Denitrification in the recharge area and discharge area of a transient agricultural nitrate plume in a glacial outwash sand aquifer
Minnesota. Water Resour. Res.
Cited by (54)
Predicting geogenic groundwater arsenic contamination risk in floodplains using interpretable machine-learning model
2024, Environmental PollutionSources and hydrogeochemical processes of groundwater under multiple water source recharge condition
2023, Science of the Total EnvironmentDeterministic factors modulating assembly of groundwater microbial community in a nitrogen-contaminated and hydraulically-connected river-lake-floodplain ecosystem
2023, Journal of Environmental Management
- 1
The authors contribute equally to the manuscript