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Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract

Sergio Cornejo Rubin De Celis, Pradeep Alava, Ivar Zekker, Gijs Du Laing UGent and Tom Van de Wiele UGent (2014) ENVIRONMENTAL HEALTH PERSPECTIVES. 122(8). p.817-822
abstract
BACKGROUND: Arsenic (As) toxicity is primarily based on its chemical speciation. Although inorganic and methylated As species are well characterized in terms of metabolism and formation in the human body, the origin of thiolated methylarsenicals is still unclear. OBJECTIVES: We sought to determine whether sulfate--reducing bacteria (SRB) from the human gut are actively involved in the thiolation of monomethylarsonic acid (MMA(V)). METHODS: We incubated human fecal and colon microbiota in a batch incubator and in a dynamic gut simulator with a dose of 0.5 mg MMA(V) in the absence or presence of sodium molybdate, an SRB inhibitor. We monitored the conversion of MMAV into monomethyl monothioarsonate (MMMTA(V)) and other As species by high-performance liquid chromatography coupled with inductively coupled plasma mass spectrometry analysis. We monitored the sulfate-reducing activity of the SRB by measuring hydrogen sulfide (H2S) production. We used molecular analysis to determine the dominant species of SRB responsible for As thiolation. RESULTS: In the absence of sodium molybdate, the SRB activity-primarily derived from Desulfovibrio desulfuricans (piger)-was specifically and proportionally correlated (p < 0.01) to MMA(V) conversion into MMMTA(V). Inactivating the SRB with molybdate did not result in MMA(V) thiolation; however, we observed that the microbiota from a dynamic gut simulator were capable of demethylating 4% of the incubated MMA(V) into arsenous acid (iAs(III)), the trivalent and more toxic form of arsenic acid (iAs(V)). CONCLUSION: We found that SRB of human gastrointestinal origin, through their ability to produce H2S, were necessary and sufficient to induce As thiolation. The toxicological consequences of this microbial As speciation change are not yet clear. However, given the efficient epithelial absorption of thiolated methylarsenicals, we conclude that the gut microbiome-and SRB activity in particular-should be incorporated into toxicokinetic analysis carried out after As exposure.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
HUMAN GUT MICROBIOTA, HPLC-ICP-MS, IN-VITRO, METABOLISM, ACID, SPECIATION, URINE, DIVERSITY, POPULATIONS
journal title
ENVIRONMENTAL HEALTH PERSPECTIVES
Environ. Health Perspect.
volume
122
issue
8
pages
817 - 822
Web of Science type
Article
Web of Science id
000341713800016
JCR category
ENVIRONMENTAL SCIENCES
JCR impact factor
7.977 (2014)
JCR rank
4/223 (2014)
JCR quartile
1 (2014)
ISSN
0091-6765
DOI
10.1289/ehp.1307759
language
English
UGent publication?
yes
classification
A1
additional info
Reproduced with permission from Environmental Health Perspectives
copyright statement
I have transferred the copyright for this publication to the publisher
id
5737633
handle
http://hdl.handle.net/1854/LU-5737633
date created
2014-10-24 16:14:27
date last changed
2016-12-19 15:47:08
@article{5737633,
  abstract     = {BACKGROUND: Arsenic (As) toxicity is primarily based on its chemical speciation. Although inorganic and methylated As species are well characterized in terms of metabolism and formation in the human body, the origin of thiolated methylarsenicals is still unclear. 
OBJECTIVES: We sought to determine whether sulfate--reducing bacteria (SRB) from the human gut are actively involved in the thiolation of monomethylarsonic acid (MMA(V)). 
METHODS: We incubated human fecal and colon microbiota in a batch incubator and in a dynamic gut simulator with a dose of 0.5 mg MMA(V) in the absence or presence of sodium molybdate, an SRB inhibitor. We monitored the conversion of MMAV into monomethyl monothioarsonate (MMMTA(V)) and other As species by high-performance liquid chromatography coupled with inductively coupled plasma mass spectrometry analysis. We monitored the sulfate-reducing activity of the SRB by measuring hydrogen sulfide (H2S) production. We used molecular analysis to determine the dominant species of SRB responsible for As thiolation. 
RESULTS: In the absence of sodium molybdate, the SRB activity-primarily derived from Desulfovibrio desulfuricans (piger)-was specifically and proportionally correlated (p {\textlangle} 0.01) to MMA(V) conversion into MMMTA(V). Inactivating the SRB with molybdate did not result in MMA(V) thiolation; however, we observed that the microbiota from a dynamic gut simulator were capable of demethylating 4\% of the incubated MMA(V) into arsenous acid (iAs(III)), the trivalent and more toxic form of arsenic acid (iAs(V)). 
CONCLUSION: We found that SRB of human gastrointestinal origin, through their ability to produce H2S, were necessary and sufficient to induce As thiolation. The toxicological consequences of this microbial As speciation change are not yet clear. However, given the efficient epithelial absorption of thiolated methylarsenicals, we conclude that the gut microbiome-and SRB activity in particular-should be incorporated into toxicokinetic analysis carried out after As exposure.},
  author       = {Cornejo Rubin De Celis, Sergio and Alava, Pradeep and Zekker, Ivar and Du Laing, Gijs and Van de Wiele, Tom},
  issn         = {0091-6765},
  journal      = {ENVIRONMENTAL HEALTH PERSPECTIVES},
  keyword      = {HUMAN GUT MICROBIOTA,HPLC-ICP-MS,IN-VITRO,METABOLISM,ACID,SPECIATION,URINE,DIVERSITY,POPULATIONS},
  language     = {eng},
  number       = {8},
  pages        = {817--822},
  title        = {Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract},
  url          = {http://dx.doi.org/10.1289/ehp.1307759},
  volume       = {122},
  year         = {2014},
}

Chicago
Cornejo Rubin De Celis, Sergio, Pradeep Alava, Ivar Zekker, Gijs Du Laing, and Tom Van de Wiele. 2014. “Arsenic Thiolation and the Role of Sulfate-reducing Bacteria from the Human Intestinal Tract.” Environmental Health Perspectives 122 (8): 817–822.
APA
Cornejo Rubin De Celis, S., Alava, P., Zekker, I., Du Laing, G., & Van de Wiele, T. (2014). Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. ENVIRONMENTAL HEALTH PERSPECTIVES, 122(8), 817–822.
Vancouver
1.
Cornejo Rubin De Celis S, Alava P, Zekker I, Du Laing G, Van de Wiele T. Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. ENVIRONMENTAL HEALTH PERSPECTIVES. 2014;122(8):817–22.
MLA
Cornejo Rubin De Celis, Sergio, Pradeep Alava, Ivar Zekker, et al. “Arsenic Thiolation and the Role of Sulfate-reducing Bacteria from the Human Intestinal Tract.” ENVIRONMENTAL HEALTH PERSPECTIVES 122.8 (2014): 817–822. Print.