Arsenic (As) speciation and distribution are two important factors in assessing human health risk from As-contaminated soil. In this study, we used the combination of physiologically based extraction test (PBET) and Simulator of Human Intestinal Microbial Ecosystem (SHIME) to determine soil As metabolism by human gut microbiota. The results showed that the percentage of soil arsenate [As(V)] transformation reached 22.1−38.2%, while that of arsenite [As(III)] attained 66.5−92.0%; 30.1−56.4% of As(V) transformed was attached to the soil solid phase. In comparison to sequential extraction results, almost all amorphous Fe/Al-oxide-bound As was liberated in the colon phase. An X-ray absorption nearedge structure (XANES) showed that the As(III) percentage in the soil solid phase reached 16.6−26.9% and reached 73.4% (soil 1) in the colon phase. Additionally, plenty of As(III) and different extents of methylation were also observed in colon extraction solution. As bioaccessibility in the colon phase was 1.8−2.8 times that in the small intestinal phase. Our results indicated that human gut microbiota increased As bioaccessibility, and large amounts of As(III) were adsorbed onto the soil solid phase as a result of microbial reduction. Determining As speciation and distribution in extraction solution and soil solid phases will allow for an accurate assessment of the risk to human health upon soil As exposure. ■ INTRODUCTIONArsenic (As) is a common toxic contaminant that is extensively distributed in the environment. 1 Human exposure to As in soils is a major public concern and is associated with serious risks to human health because As species are known carcinogens. 2,3 In most cases, human exposure to soil As occurs via inhalation, inadvertent oral ingestion, and dermal contact. 4,5 Inadvertent oral ingestion has been considered an important exposure route for soil As, especially ingestion through outdoor hand-to-mouth activities by children. 6 The estimation of As bioaccessibility (gastric and small intestinal phases) in contaminated soils through in vitro methods has been used for human health risk assessment. On the basis of previous studies, 7−9 simple, fast, and inexpensive in vitro methods can effectively estimate in vivo relative As bioavailability. Generally, bioaccessibility is defined as the fraction of As that is soluble in the gastrointestinal environment of humans and available for absorption, whereas bioavailability is determined by the fraction of As that is absorbed into the systemic circulation. 7,8 Currently, As bioaccessibility in the gastric and small intestinal phases may underestimate its harm to human health. 10 Studies have clearly illustrated that gut microbiota significantly affect As metabolism by, for example, reduction, methylation, and thiolation. 11 As metabolism in contaminated soil by human gut microbiota can affect As bioaccessibility and speciation. 10,12 Therefore, As biotransformation must be considered an essential part of the risk assessment of oral soil As exposure using i...
• Five in vitro gastrointestinal methods combined with SHIME (colon phase) were used.• As bioaccessibility varied in the colon phase among these methods.• Plenty of As(III) and methylated arsenicals by microbial transformation were observed.• As bioaccessibility in PBET/SBRC-SHIME colon phase were closer to in vivo results for NIST 2710a. Arsenic (As) speciation analysis is essential when evaluating the risks upon oral exposure to As-contaminated soils. In this study, we first investigated the variability in the As bioaccessibility and speciation using a combination of five common in vitro methods (SBRC, PBET, DIN, UBM and IVG) (gastric and small intestinal phases) and the SHIME model (colon phase). Our results indicate that the As bioaccessibility varies in the colon phase. An increase in the As bioaccessibility for SBRC and PBET, and a decrease for UBM and IVG were observed in the colon phase. In addition, we found different extents of methylation and large amounts of arsenite [As(III)] due to microbial reduction in the colon digests. The UBM-SHIME method displayed a higher methylation percentage of 13.5-82.1%, but a lower methylation percentage of 0.2-21.8% was observed in the SBRC-SHIME method. Besides, The MMA V levels in the colon digests were positively correlated with those of As(III) and DMA V , so DMA V can be considered an indicator to evaluate the As metabolic speed of in vitro cultured human gut microbiota. Based on the standard reference soil of NIST 2710a, the As bioaccessibility in the colon phase of PBET-SHIME and SBRC-SHIME were the closest to the in vivo results. Combining in vitro methods and SHIME will remarkably affect the accurate assessment of potential risks to human health associated with oral exposure to soil As.
The influence of the human gut microbiota on the bioaccessibility and bioavailability of trace elements in vegetables has barely been studied. An in vitro digestion model combining the physiologically based extraction test (PBET) and the Simulator of Human Intestinal Microbial Ecosystem (SHIME) was applied. Results showed that the gut microbiota increased the bioaccessibility of iron (Fe) in ten test vegetables by 1.3-1.8 times, but reduced the bioaccessibility of manganese (Mn), copper (Cu), and zinc (Zn) in vegetables in the colon phase by 3.7% to 89.6%, 24.8% to 100.0%, and 59.9% to 100.0%, respectively. Using the Caco-2 cell model to simulate the human absorption process, the bioavailable contents and the bioavailability of the trace elements were further determined. Swamp cabbage was the best source of Fe and Cu; spinach and lettuce provided the highest amounts of bioavailable Mn and Zn, respectively. Referring to the daily reference intakes of trace elements, the obtained data provide a scientific basis for both reasonable ingestion of vegetables in diets and diversification of diets.
Arsenic (As) speciation is essential in assessing health risks from As-contaminated soil. Release of soil-bound arsenic, As transformation by human gut microbiota, and the subsequent intestinal absorption of soil As metabolites were evaluated. A colon microbial community in a dynamic human gut model and the intestinal epithelial cell line Caco-2 were cultured. Arsenic speciation analysis and absorption of different As species were undertaken. In this study, soil As release (3.7-581.2 mg kg) was observed in the colon. Arsenic in the colon digests was transformed more quickly than that in the soil solid phase. X-ray absorption near-edge spectroscopy (XANES) analysis showed that 44.2-97.6% of arsenite [As(III)] generated due to arsenate [As(V)] reduction was in the soil solid phase after the colon phase. We observed a high degree of cellular absorption of soil As metabolites, exhibiting that the intestinal absorption of monomethylarsonic acid and As(III) (33.6% and 30.2% resp.) was slightly higher than that of dimethylarsinic acid and As(V) (25.1% and 21.7% resp.). Our findings demonstrate that human gut microbiota can directly release soil-bound arsenic, particularly As-bearing amorphous Fe/Al-oxides. Determining As transformation and intestinal absorption simultaneously will result in an accurate risk assessment of human health with soil As exposures.
h i g h l i g h t sWe isolated three anaerobic As(Ⅴ)-reducing bacterium from soil with high ratio of As(Ⅲ). Strains JQ, DJ-3 and DJ-4 could transform very high concentration of As(Ⅴ) to As(Ⅲ). All the three strains could release goethite-adsorbed As(Ⅴ) into solution. We compared the three strains with other previously isolated strains. The existence of the strains will cause the mobilization and transformation of As in soil. Handling Editor: X. Cao Keywords:As(Ⅴ)-reducing bacteria Arsenate reduction As release Goethite a b s t r a c t Arsenic (As) contamination has become a worldwide environmental problem: arsenite (As(Ⅲ)) especially has posed a major threat to human health. Here, we report the first three isolates of anaerobic As(Ⅴ)-reducing bacterial strains (strains JQ, DJ-3 and DJ-4) from a soil sample containing 48.7% of total As in the form of As(III) collected in Chifeng, Inner Mongolia, China. Strains JQ, DJ-3 and DJ-4 were phylogenetically closely related to Bacillus, Desulfitobacterium and Exiguobacterium, respectively. Among these strains, JQ and DJ-3 have the arsC gene, DJ-4 possesses the arrA gene. The three strains could all resist and reduce high concentrations of As(Ⅴ) under anoxic conditions. The order of resistance to As(Ⅴ) was DJ-3 > JQ > DJ-4. Strain DJ-3 not only possesses the strongest resistance to As(Ⅴ) but could also reduce 53% of the As(Ⅴ) to As(III) in the treatment of 60 mM As(Ⅴ) in 5 d. All three strains could release As from goethite; strain DJ-4 has the highest ability to promote the release of As (90.5%) from goethite. These results suggested that strains JQ, DJ-3 and DJ-4 may play an important role in the mobilization and transformation of As in soil.
The in vitro bioaccessibility of trace metals associated with oral ingestion of market vegetables (lettuce, pak choi, cole, and leaf lettuce) of Beijing, China was studied. The physiologically based extraction test (PBET) combined with the Simulator of Human Intestinal Microbial Ecosystem (SHIME) was applied to simulate stomach, small intestine, and colon of human. In the gastro-intestinal phases, the bioaccessibility of Cu, Fe, Mn, and Zn varied within 5.7–75.5%, 17.3–50.4%, 13.3–49.1%, and 19.9–63.7%, respectively. There was no significant difference in the metal bioaccessibility between the gastric and small intestinal phases, except for higher Cu bioaccessibility in the small intestine. Besides, the bioaccessibility of the four trace metals in the colon phase was first ever reported. A significant decline in Cu bioaccessibility (1.8–63.7%) and slight increases in the bioaccessibility of Fe (16.7–56.4%), Mn (21.2–71.6%), and Zn (15.7–69.7%) were revealed, which could mainly be attributed to the effect of colon microbiota. In addition, the estimated daily intakes (EDIs) of Cu, Fe, Mn, and Zn were worked out to be 0.7, 8.8, 2.7, and 4.5 μg kg−1 body weight d−1, based on which the potential influences of these trace metals in vegetables on the health of the local consumers was demonstrated.
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