Bioaccessibility of arsenic from contaminated soils and alteration of the gut microbiome in an in vitro gastrointestinal model

Abstract

Arsenic exposure has been reported to alter the gut microbiome in mice. Activity of the gut microbiome derived from fecal microbiota has been found to affect arsenic bioaccessibility in an in vitro gastrointestinal (GI) model. Only a few studies have explored the relation between arsenic exposure and changes in the composition of the gut microbiome and in arsenic bioaccessibility. Here, we used simulated GI model system (GIMS) containing a stomach, small intestine, colon phases and microorganisms obtained from mouse feces (GIMS-F) and cecal contents (GIMS-C) to assess whether exposure to arsenic-contaminated soils affect the gut microbiome and whether composition of the gut microbiome affects arsenic bioaccessibility. Soils contaminated with arsenic did not alter gut microbiome composition in GIMS-F colon phase. In contrast, arsenic exposure resulted in the decline of bacteria in GIMS-C, including members of Clostridiaceae, Rikenellaceae, and Parabacteroides due to greater diversity and variability in microbial sensitivity to arsenic exposure. Arsenic bioaccessibility was greatest in the acidic stomach phase of GIMS (pH 1.5-1.7); except for GIMS-C colon phase exposed to mining-impacted soil in which greater levels of arsenic solubilized likely due to microbiome effects. Physicochemical properties of different test soils likely influenced variability in arsenic bioaccessibility (GIMS-F bioaccessibility range: 8-37%, GIMS-C bioaccessibility range: 2-18%) observed in this study.

Fig. 1.

Experiment Setup.

Fig. 2.. Alpha and Beta diversity at weeks 3–4 in GIMS-F (A–C) and GIMS-C (D–F)

A.) Alpha diversity (observed OTU) rarefaction curve at week 3 B) Alpha diversity at week 4 C) PCoA based on weighted UniFrac distances of no exposure (inoculum: blue, 2 h post-inoculation: red, week 1: yellow, week 2: gray, week 3: black, week 4: magenta) and arsenic-exposed groups (week 1: green, week 2: pink, week 3: teal, week 4: purple). Weeks 2–4 no exposure groups are circled in black. Weeks 2–4 arsenic-exposed groups are circled in red. D.) Alpha diversity rarefaction curve at week 3. E.) Alpha diversity at week 4 F) PCoA based on weighted UniFrac distances of no exposure (inoculum: blue, 2 h post-inoculation: red, week 1: green, week 2: pink, week 3: beige, week 4: purple) and arsenic-exposed groups (week 2: gray, week 3: black, week 4: magenta). Week 1 arsenic-exposed groups are circled in green. A cluster of week 2 arsenic-exposed, no exposure, and 2 h post-inoculation groups are circled in red. A cluster of weeks 3–4 no exposure and arsenic-exposed groups are circled in black.

Fig. 3.. Mean Percent IVBA for weeks 3–4 in each GI phase of GIMS-F and GIMS-C.

A.) NIST 2710 A GIMS-F B) Pesticide-impacted soil GIMS-F C.) Mining-impacted soil GIMS-F D.) NIST 2710 A GIMS-C E.) Pesticide-impacted soil GIMS-C F.) USGS soil GIMS-C. (*p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0001).