Biogeochemical processes of arsenic transformation and redistribution in contaminated soils: Combined effects of iron, sulfur, and organic matter
Graphical abstract
Introduction
Arsenic (As) is a highly toxic element that is widely distributed in soil and groundwater environments. The International Agency for Research on Cancer (IARC) has identified As as carcinogenic to humans (Group 1) because of its high exposure frequency and risk (WHO, 2012). Currently, millions of people in various countries, including Bangladesh and eastern India, are suffering from As poisoning (Fendorf et al., 2010, Smith et al., 2000). Human exposure to As is mainly related to consumption of As-contaminated groundwater (Chowdhury et al., 2000). Studies have shown that the microbial reduction of soil arsenate (As(V)) by As(V)-reducing bacteria in anaerobic environment is one of the most important factors causing soil As release and groundwater arsenite (As(III)) contamination (Guo et al., 2015, Osborne et al., 2015, Tufano et al., 2008).
In the soil environment, Fe(III)-(oxyhydr)oxides are considered to be the main As(V) adsorbents (Bowell, 1994, Sowers et al., 2017); therefore, the As biogeochemical transformations that occur during interactions between As-bearing Fe-minerals and As(V)-reducing bacteria have been widely studied in recent years (Cai et al., 2020, Ohtsuka et al., 2013, Zobrist et al., 2000). Dissimilatory As(V)-reducing bacteria can reduce Fe(III)-(oxyhydr)oxide-associated As(V) in the solid phase, which may result in As(III) release, owing to the generally lower affinity of As(III) for Fe-(oxyhydr)oxides compared to As(V) (Guo et al., 2015). Additionally, some As(V)-reducing bacteria have strong Fe(III)-reducing ability and can cause the reductive dissolution of Fe(III)-(oxyhydr)oxides, releasing solid-associated As(V) to the aqueous phase, where As(V) is subsequently reduced to As(III) (Cui and Jing, 2019, Han et al., 2019, Osborne et al., 2015). On the other hand, Fe(II) can trigger the formation of secondary minerals such as goethite, vivianite, magnetite, and lepidocrocite (Notini et al., 2019, ThomasArrigo et al., 2018). The released As may be re-immobilized due to the re-adsorption and/or incorporation of As by these secondary Fe-minerals. (Muehe et al., 2016, Pedersen et al., 2006).
In addition to Fe-(oxyhydr)oxides, other soil components such as sulfides may affect the biogeochemical transformation of soil As (Wang et al., 2017, Zhang et al., 2017). Phan et al. (2019) added varied sulfate concentrations to sediment in redox cycling bioreactors, and documented decreased As mobility under reducing conditions. Results showed that pyrite (FeS2) was the dominant Fe sulfide formed, and the strong affinity of thioarsenate for FeS2 likely contributed to the As-sequestration. In contrast, ThomasArrigo et al. (2016) showed that, although sulfate addition to As-contaminated flocs may result in abundant mackinawite (FeS) precipitation, the mobilization of As in floc was enhanced. In addition, As may be retained in the solid phase as an orpiment (As2S3)-like species, and the formed As2S3 tends to associate with Fe sulfide (Burton et al., 2014). In the nature, the composition of soil elements (including Fe and S contents) in different soil environments is significantly different, and As mobilization may be attributed to multiple geochemical pathways dominated by different elements (Xu et al., 2017). To date, however, the causal mechanisms of As mobilization and redistribution in soils with contrasting Fe and S contents remain unclear.
Soil properties such as the organic matter (OM) content may also significantly impact As mobilization and speciation transformation (Hu et al., 2018, Muehe et al., 2013). In nature, OM is often adsorbed onto or coprecipitates with Fe minerals, resulting in the formation of organic–mineral associations (Chan et al., 2004, Kaiser and Guggenberger, 2007). The presence of OM can alter the structures and physical properties of minerals, e.g., by occupying the adsorption sites and inducing Fe(III)-(oxyhydr)oxide aggregation (Mikutta et al., 2008), and may consequently decelerate microbial Fe reduction and As mobilization (Amstaetter et al., 2012, Shimizu et al., 2013). In contrast, quinones can promote Fe(III) reduction through an electron-shuttle mechanism (Cooper et al., 2017, Kappler et al., 2004), thereby promoting As mobilization (Wu et al., 2020, Yamamura et al., 2018). Qiao et al. recently demonstrated that the addition of humic substances can facilitate As(V) reduction in paddy soils, mainly by acting as electron shuttles and increasing the As(V)-respiration-related arrA gene abundance (Qiao et al., 2019). However, whether the difference in the initial OM content in soils will affect microbially-mediated As speciation transformation is still unclear, and deserves further investigation.
As mentioned above, anaerobic microorganisms with As(V)- and Fe(III)-reducing capabilities play an important role in the biogeochemical cycling of As (Jiang et al., 2013, Qiao et al., 2018, Schaefer et al., 2017). Recently, two typical bacterial strains, Desulfitobacterium sp. DJ-3 and Exiguobacterium sp. DJ-4, were isolated from As-contaminated soil in Inner Mongolia, China (Cai et al., 2016). Desulfitobacterium is a typical As(V)-reducing bacterial genus that has been isolated in a variety of soil environments. It can use a wide variety of electron acceptors, including several metals (e.g., As(V), Fe(III), Mn(IV)), nitrate, sulfate, and humic acids (Niggemyer et al., 2001, Villemur et al., 2006). Strain DJ-4 is the first Exiguobacterium strain isolated from soil that can reduce As(V). Both strains carry arrA genes and can reduce high As(V) concentrations under anoxic conditions (Cai et al., 2019, Cai et al., 2016). Additionally, strains DJ-3 and DJ-4 can cause solid-phase As release through both dissimilatory As(V)-reduction and reductive Fe(III)-dissolution pathways (Cai et al., 2020). The strains can utilize humic acids as electron shuttles to facilitate ferrihydrite-associated As(V) reduction (Cai et al., 2021). Collectively, these two strains may significantly impact the speciation and partitioning of soil As, and were therefore used in this study.
Overall, it is clear that the biogeochemical cycling of soil As is greatly influenced by the soil properties. However, in soils with contrasting Fe, S, and OM contents, the causal mechanisms of As transformation and distribution remain unclear. Relying on the combination utilization of sequential soil As extraction, synchrotron X-ray techniques and wet-chemical analyses, our study aims to (i) analyze the dominant geochemical pathways of As redistribution in soils with contrasting Fe and S contents; and to (ii) elucidate the influence of soil OM content on microbially-mediated speciation transformation of As in soil. This study serves to assess the impact of soil Fe, S, and OM contents on As transformation and redistribution under microbial reduction in strongly anoxic environment.
Section snippets
Soil samples
Soil samples were collected from the surface layers (0–20 cm) of one mining and four agricultural fields in Dalian, Shimen, Shangyu, Chenzhou, and Jincheng, China. The soils are hereafter referred to as Soil ‘1’, ‘2’, ‘3’, ‘4’, and ‘5’, respectively. All five soils contain elevated levels of As (greater than 15 mg/kg) owing to industrial metal mining, geogenic weathering and/or agricultural activities. The soils have different physicochemical properties, especially OM content,
Characterization of initial soil samples
The physicochemical properties and elemental compositions of the initial soil samples are listed in Table 1 and S2. The total As, Fe, S, Al, and Mn contents of the soil samples varied within the ranges of 17.2–802.5 mg/kg, 25.9–191.1 g/kg, 0.6–10.3 g/kg, 6.3–53.8 g/kg, and 0.1–0.8 g/kg, respectively. The oxalate-extractable Fe and available sulfate contents of Soil 1 (28.2 g/kg and 342.9 mg/kg, respectively) were much higher than those of the other soils. The oxalate-extractable Fe contents of
Conclusions
Our study demonstrates that microbial reduction of As(V)-contaminated soil may result in significant As(III) release. As(V)-reducing bacteria can release specifically sorbed As, amorphous oxide-bound As, and crystalline oxide-bound As. Thereafter, the As redistribution geochemical pathways are strongly impacted by the soil Fe and S contents. In Fe-rich soils, such as mining-derived mineral substrates and mining area soils, released As is preferentially adsorbed onto and/or incorporated into
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 authors acknowledge the Beijing Synchrotron Radiation Facility (BSRF) and the Shanghai Synchrotron Radiation Facility (SSRF) for providing valuable beamtime. This work was funded by the National Natural Science Foundation of China (No. 42107432, No. 41877501), the project of China National Postdoctoral Program for Innovative Talents (No. BX2021297), and supported by the Fundamental Research Funds for the Central Universities (E1E40512).
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