Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract

Gut microbiota provides protection against arsenic (As) induced toxicity, and As metabolism is considered an important part of risk assessment associated with soil As exposures. However, little is known about microbial iron(III) reduction and its role in metabolism of soil-bound As in the human gut....

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Main Authors: Naiyi Yin, Xuhui Chang, Peng Xiao, Yi Zhou, Xiaotong Liu, Shimao Xiong, Pengfei Wang, Xiaolin Cai, Guoxin Sun, Yanshan Cui, Zhengyi Hu
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412023001848
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author Naiyi Yin
Xuhui Chang
Peng Xiao
Yi Zhou
Xiaotong Liu
Shimao Xiong
Pengfei Wang
Xiaolin Cai
Guoxin Sun
Yanshan Cui
Zhengyi Hu
author_facet Naiyi Yin
Xuhui Chang
Peng Xiao
Yi Zhou
Xiaotong Liu
Shimao Xiong
Pengfei Wang
Xiaolin Cai
Guoxin Sun
Yanshan Cui
Zhengyi Hu
author_sort Naiyi Yin
collection DOAJ
description Gut microbiota provides protection against arsenic (As) induced toxicity, and As metabolism is considered an important part of risk assessment associated with soil As exposures. However, little is known about microbial iron(III) reduction and its role in metabolism of soil-bound As in the human gut. Here, we determined the dissolution and transformation of As and Fe from incidental ingestion of contaminated soils as a function of particle size (<250 μm, 100–250 μm, 50–100 μm and < 50 μm). Colon incubation with human gut microbiota yielded a high degree of As reduction and methylation of up to 53.4 and 0.074 μg/(log CFU/mL)/hr, respectively; methylation percentage increased with increasing soil organic matter and decreasing soil pore size. We also found significant microbial Fe(III) reduction and high levels of Fe(II) (48 %−100 % of total soluble Fe) may promote the capacity of As methylation. Although no statistical change in Fe phases was observed with low Fe dissolution and high molar Fe/As ratios, higher As bioaccessibility of colon phase (avg. 29.4 %) was mainly contributed from reductive dissolution of As(V)-bearing Fe(III) (oxy)hydroxides. Our results suggest that As mobility and biotransformation by human gut microbiota (carrying arrA and arsC genes) are strongly controlled by microbial Fe(III) reduction coupled with soil particle size. This will expand our knowledge on oral bioavailability of soil As and health risks from exposure to contaminated soils.
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spelling doaj.art-9bb048f7f5b84f778b6c599c2658715a2023-04-25T04:07:45ZengElsevierEnvironment International0160-41202023-04-01174107911Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tractNaiyi Yin0Xuhui Chang1Peng Xiao2Yi Zhou3Xiaotong Liu4Shimao Xiong5Pengfei Wang6Xiaolin Cai7Guoxin Sun8Yanshan Cui9Zhengyi Hu10College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaCollege of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of ChinaResearch Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of China; Corresponding author at: Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of China.College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of China; Corresponding authors at: College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China.College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China; Sino-Danish Centre for Education and Research, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of ChinaGut microbiota provides protection against arsenic (As) induced toxicity, and As metabolism is considered an important part of risk assessment associated with soil As exposures. However, little is known about microbial iron(III) reduction and its role in metabolism of soil-bound As in the human gut. Here, we determined the dissolution and transformation of As and Fe from incidental ingestion of contaminated soils as a function of particle size (<250 μm, 100–250 μm, 50–100 μm and < 50 μm). Colon incubation with human gut microbiota yielded a high degree of As reduction and methylation of up to 53.4 and 0.074 μg/(log CFU/mL)/hr, respectively; methylation percentage increased with increasing soil organic matter and decreasing soil pore size. We also found significant microbial Fe(III) reduction and high levels of Fe(II) (48 %−100 % of total soluble Fe) may promote the capacity of As methylation. Although no statistical change in Fe phases was observed with low Fe dissolution and high molar Fe/As ratios, higher As bioaccessibility of colon phase (avg. 29.4 %) was mainly contributed from reductive dissolution of As(V)-bearing Fe(III) (oxy)hydroxides. Our results suggest that As mobility and biotransformation by human gut microbiota (carrying arrA and arsC genes) are strongly controlled by microbial Fe(III) reduction coupled with soil particle size. This will expand our knowledge on oral bioavailability of soil As and health risks from exposure to contaminated soils.http://www.sciencedirect.com/science/article/pii/S0160412023001848ArsenicIronGut microbiomtaMetabolismSpeciation analysisSimulator of the Human Intestinal Microbial Ecosystem
spellingShingle Naiyi Yin
Xuhui Chang
Peng Xiao
Yi Zhou
Xiaotong Liu
Shimao Xiong
Pengfei Wang
Xiaolin Cai
Guoxin Sun
Yanshan Cui
Zhengyi Hu
Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
Environment International
Arsenic
Iron
Gut microbiomta
Metabolism
Speciation analysis
Simulator of the Human Intestinal Microbial Ecosystem
title Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
title_full Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
title_fullStr Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
title_full_unstemmed Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
title_short Role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
title_sort role of microbial iron reduction in arsenic metabolism from soil particle size fractions in simulated human gastrointestinal tract
topic Arsenic
Iron
Gut microbiomta
Metabolism
Speciation analysis
Simulator of the Human Intestinal Microbial Ecosystem
url http://www.sciencedirect.com/science/article/pii/S0160412023001848
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