The role of soil arsenic fractionation in the bioaccessibility, transformation, and fate of arsenic in the presence of human gut microbiota

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Highlights

  • Amorphous and crystalline Fe/Al (hydr)oxides contributed to colon As bioaccessibility.

  • High degree of transformation was found as soluble As at higher bioaccessibility.

  • As transformation occurred mainly in the solid phase at lower bioaccessibility (< 5%).

  • Gut microbiota could transform As(V) associated with crystalline and sulfide minerals.

Abstract

Soil arsenic (As) fractionation and its bioaccessibility are two important factors in human health risk assessment. However, data related to the impact of As minerals on the bioaccessibility with human gut microbiota involvement are scarce. In this study, speciation analysis was determined using HPLC-ICP-MS and XANES after incubation with colon microbiota from human origin, in combination with sequential extraction. Significant increase of colon As bioaccessibility was contributed primarily from As associated with amorphous and crystalline Fe/Al (hydr)oxides. We found a high degree of transformation at higher bioaccessibility (ave. 40 % of total As), which was predominantly present as liquid-phase As. In contrast, As transformation occurred mainly in the solid phase at lower bioaccessibility (< 5%), especially for soils containing As-S species. XANES spectroscopy revealed that As(III) increased by about 20 % in soil residues. Finally, the excreted As may be predominantly in association with (alumino)silicate minerals by SEM-EDX. It inferred that the priority sequence in As transformation by human gut microbiota was dissolved As(V), As(V) sorbed to mineral surfaces, crystalline As(V)-bearing minerals and As sulfides. This study will shed new light on the role of As-bearing minerals in evaluating health risks from soil As exposure.

Introduction

Arsenic (As), a human carcinogen, is widely distributed in the natural environment (Carlin et al., 2016). In regions of mining and smelting activities, oral ingestion of contaminated soil and dust has become the main exposure route, especially for children with typical hand-to-mouth behavior (Glorennec et al., 2016). Human health risks from soil As exposure could be adequately represented by evaluating its bioavailability (fraction of the ingested soil As reaches the systemic circulation) using in vivo models, such as swine and mice (Li et al., 2019). In considerations of cost performance and ethics, in vitro methodologies as an appropriate surrogate have been developed and validated for predicting As bioavailability (Bradham et al., 2018; Juhasz et al., 2015).

A number of in vitro methods, varying in the composition and operational parameters, have been applied to the assessment of As bioaccessibility in contaminated soil, as the fraction of soluble As in the human gastrointestinal tract and available for absorption (Ruby et al., 1996; Wragg et al., 2011). Most of the current in vitro studies simulated the stomach and small intestine conditions, where the impact of the colon microorganisms is not taken into account. The colon composed of at least 1014 bacteria, harbors a diverse microbial community of more than 1000 species, which can induce chemical transformation of xenobiotics through a variety of enzymes (Koppel et al., 2017). Previous work has demonstrated the metabolic potency of colon microbiota from human origin toward inorganic As, dietary-bound and/or soil-bound As through a series of As biotransformation, including reduction, methylation, and thiolation (Calatayud et al., 2018; DC. Rubin et al., 2014; van de Wiele et al., 2010). Earlier studies on As associated with Fe oxides and soils, showed that human colon microbiota promoted As release for most samples, and As bioaccessibility was consistently higher than the corresponding value of the small intestinal phase (Laird et al., 2007, 2010; Yin et al., 2020). Thus, the involvement of human gut microbiota must be considered when evaluating health risks from soil As exposure.

It is acknowledged that several factors control As bioavailability in contaminated soil, such as particle sizes and chemical speciation of As (Ruby et al., 1999). The mobility and bioaccessibility of As was influenced by the solubility of the primary and secondary As-bearing minerals (Walker et al., 2009). Meunier et al. (2010) found that the elevated bioaccessibility of As was in the following order: i) Ca-Fe arsenate, ii) amorphous Fe arsenates and As-bearing Fe (hydr)oxides, and iii) arsenopyrite or scorodite. Soils containing arsenopyrite significantly decreased As bioavailability (Bradham et al., 2011). The bioaccessibility of As was strongly dependent on the mineralogical composition of Fe(III)-As(V) coprecipitates (Ehlert et al., 2018). A new analytical protocol of quantitative mineralogy showed that low bioaccessibility may be due to As associated primarily with Fe (hydr)oxides in fine intergrowth with phyllosilicates (Ciminelli et al., 2018). The bioaccessible As extracted by the IVG method was the As present in the non-specifically and specifically sorbed fractions (Whitacre et al., 2013). Higher As bioaccessibility was observed in the following order; i) As bound to amorphous Fe oxides, ii) As associated with crystalline Fe oxides and As sulfide minerals, and iii) As associated with the weathering products of As sulfide minerals (Kim et al., 2014). The importance of chemical binding type between As and Fe oxide will result in more accurately assessing As bioaccessibility in soil (Jeong et al., 2017). Our previous work found that the release of As associated with amorphous Fe/Al minerals by human gut microbiota may result in an increase of colon bioaccessibility (Yin et al., 2017). Thus, there is a lack of knowledge about the release of As associated with mineral phase and the extent of solid-phase As transformation in presence of human gut microbiota.

The desire to further understand the interaction between human gut microbiota and As-bearing minerals motivates the present study. The objective of this study was to explore the role of soil fractionation in assessing As bioaccessibility in simulated gastrointestinal tract. Therefore, in combination with sequential extraction, the release, transformation, and partitioning of As were determined upon incubation with human gut microbiota. The speciation and distribution of As in the solid and liquid phase were investigated using techniques such as XAS, HPLC-ICP-MS, SED-EDX.

Section snippets

Soil sample preparation

Soil samples (n = 8) were collected from contaminated sites in different provinces of China. All soil samples were taken from the 0−20 cm layer and air-dried; subsequently, the physicochemical properties were determined on triplicate samples, including soil pH, soil organic matter (OM), soil texture and total concentrations of iron, manganese, and aluminum (Yin et al., 2017). Arsenic fractionation in soils was determined using a five-step sequential extraction procedure (Wenzel et al., 2001),

Contribution of each fraction to As bioaccessibility

Soil properties were shown in Table 1, and total As concentrations ranged from 111 to 3226 mg/kg. The majority of As in the 8 soils in Fig. S1 was associated with amorphous Fe and Al oxides (ave. 28.0 %, 5.4–58.1 %, fraction 3), and residual phases such as sulfide and aluminosilicate minerals (ave. 45.9 %, 12.2–93.8 %, fraction 5). In contrast, only 9.4 % of total As was presented in non-specifically/specifically sorbed As (fraction 1 and 2). The in vitro experiments consisting of PBET and

CRediT authorship contribution statement

Naiyi Yin: Conceptualization, Methodology, Investigation, Writing - original draft, Funding acquisition. Yunpeng Li: Methodology, Data curation. Xiaolin Cai: Conceptualization, Resources, Formal analysis. Huili Du: Validation. Pengfei Wang: Visualization. Zeliang Han: Investigation. Guoxin Sun: Supervision, Software. Yanshan Cui: Supervision, Project administration, 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

We acknowledge Beijing Synchrotron Radiation Facility (BSRF) for the valuable beamtime, operated by Institute of High Energy Physics, Chinese Academy of Sciences. This work was supported by the National Natural Science Foundation of China [grant number 41877501], the University of Chinese Academy of Sciences, and the project of National Postdoctoral Program for Innovative Talents funded by China Postdoctoral Science Foundation [grant number BX20180299].

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