Unraveling influences of nitrogen cycling on arsenic enrichment in groundwater from the Hetao Basin using geochemical and multi-isotopic approaches

Highlights

• Organic nitrogen mineralization and DNRA contributed primarily to NH₄⁺ release.

• Feammox and anammox were major NH₄⁺ sinks under anoxic conditions.

• DNRA was favored over denitrification under much higher DOC:NO₃^– molar ratios.

• Feammox and heterotrophic DNRA increased Fe(II) and arsenic concentrations.

• Anammox and Fe(II)-fueled autotrophic DNRA reduced Fe(II) and arsenic mobilization.

Abstract

Sources and co-cycling of nitrogen species in arsenic-prone groundwater remain poorly understood, which could affect arsenic behavior. Here, geochemical and multi-isotopic characteristics of groundwater from various redox environments were investigated to reveal the effects of nitrogen cycling on arsenic mobility in groundwater systems from the Hetao Basin in China. In deep groundwater along an approximate flow path from the alluvial fan (Zone I) through the transition area (Zone II) and to the flat plain (Zone III), a progressive NO₃^– depletion with gradually increased δ¹⁵N_NO3 and δ¹⁸O_NO3 occurred, accompanied by increases in dissolved NH₄⁺, Fe(II), and arsenic concentrations and a decrease in δ¹⁵N_NH4. Shallow groundwater in the flat plain (Zone IV) covered wider ranges of δ¹⁵N_NO3 and δ¹⁸O_NO3 and relatively lower δ¹⁵N_NH4. Organic nitrogen mineralization contributed primarily to NH₄⁺ release in all zones, and dissimilatory NO₃^– reduction to NH₄⁺ (DNRA) was an important NH₄⁺ source in Zone IV. While NH₄⁺ loss mainly occurred via nitrification in Zone I, anaerobic NH₄⁺ oxidation was coupled to Fe(III) oxide reduction (Feammox) in Zones II and III and to NO₂^– reduction (anammox) in Zones II, III, and IV. Groundwater NO₃^– was reduced via heterotrophic denitrification in Zones II and III, while the DNRA was favored over denitrification in Zone IV with much higher DOC:NO₃^– molar ratios. Feammox and heterotrophic DNRA increased the dissolved Fe(II) and arsenic concentrations via the enhanced Fe(III) oxide reduction. However, anammox and Fe(II)-fueled autotrophic DNRA decreased their concentrations due to limited Fe(III) oxide reduction and/or enhanced Fe(II) oxidation. The influences of nitrogen cycling on arsenic behavior are mainly mediated by transformations between Fe(III) oxides and dissolved Fe(II). This study provides the first detailed multi-isotopic picture of nitrogen cycling and the relevant effects on arsenic enrichment processes.

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., δ¹⁵N_NO3, δ¹⁸O_NO3, and δ¹⁵N_NH4). The ¹⁵N_NO3 is enriched by fractionation effects via denitrification and DNRA but is depleted via partial nitrification (Böhlke et al., 2006). The ¹⁵N_NH4 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 SO₄^2- 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., δ¹⁵N_NO3, δ¹⁸O_NO3, δ³⁴S_SO4, and δ¹³C_DIC), 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.

$${\left({\mathrm{C}\mathrm{H}}_2\mathrm{O}\right)}_m{\left({\mathrm{N}\mathrm{H}}_3\right)}_n+\frac{4m}{5}{\mathrm{N}\mathrm{O}}_3^{-}+\frac{5\mathrm{n}-m}{5}{\mathrm{H}}^{+}={\frac{2m}{5}\mathrm{N}}_2+m{\mathrm{H}\mathrm{C}\mathrm{O}}_3^{-}+{\frac{2m}{5}\mathrm{H}}_2\mathrm{O}+{n\mathrm{N}\mathrm{H}}_4^{+}$$

$$14{\text{NO}}_3^{-}+5{\text{FeS}}_2+4{\text{H}}^{+}=7{\text{N}}_2+10{\text{SO}}_4^{2-}+5{\text{Fe}}^{2+}+2{\text{H}}_2\text{O}$$

$$2{\text{NO}}_3^{-}+10{\text{Fe}}^{2+}+24{\text{H}}_2\text{O}=10\text{Fe}{\left(\text{OH}\right)}_3+18{\text{H}}^{+}+{\text{N}}_2$$

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., δ¹⁵N_NO3, δ¹⁸O_NO3, δ¹⁵N_NH4, δ¹³C_DIC, and δ¹³C_DOC) of groundwater in different redox zones from alluvial-pluvial aquifers in the Hetao Basin of China were investigated.