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Title: The role of gut microbiota in fetal methylmercury exposure: Insights from a pilot study

Abstract

The mechanisms by which gut microbiota contribute to methylmercury metabolism remain unclear. Among a cohort of pregnant mothers, the main objectives of our pilot study were to determine 1) associations between gut microbiota and mercury concentrations in biomarkers (stool, hair and cord blood) and 2) the contributions of gut microbial mercury methylation/demethylation to stool methylmercury. Moreover, for pregnant women (36-39 weeks gestation, n=17) donated hair and stool specimens, and cord blood was collected for a subset (n=7). The diversity of gut microbiota was determined using 16S rRNA gene profiling (n=17). For 6 stool samples with highest/lowest methylmercury concentrations, metagenomic whole genome shotgun sequencing was employed to search for one mercury methylation gene (hgcA), and two mer operon genes involved in methylmercury detoxification (merA and merB). There were seventeen bacterial genera that were significantly correlated (increasing or decreasing) with stool methylmercury, stool inorganic mercury, or hair total mercury; however, aside from one genus, there was no overlap between biomarkers. No definitive matches for hgcA or merB, while merA were detected at low concentrations in all six samples. Proportional differences in stool methylmercury were not likely attributed to gut microbiota through methylation/demethylation. Gut microbiota potentially altered methylmercury metabolism using indirect pathways.

Authors:
 [1];  [2]; ORCiD logo [3];  [3];  [3];  [3]; ORCiD logo [4]
  1. Univ. of South Carolina, Columbia, SC (United States)
  2. Greenville Health System, SC (United States)
  3. Baylor College of Medicine, Houston, TX (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1286950
Alternate Identifier(s):
OSTI ID: 1396957
Grant/Contract Number:  
AC05-00OR22725; DE SC0006809
Resource Type:
Accepted Manuscript
Journal Name:
Toxicology Letters
Additional Journal Information:
Journal Volume: 242; Journal Issue: C; Journal ID: ISSN 0378-4274
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; mercury; methylmercury; gut; microbiome; metabolism; human health

Citation Formats

Rothenberg, Sarah E., Keiser, Sharon, Ajami, Nadim J., Wong, Matthew C., Gesell, Jonathan, Petrosino, Joseph F., and Johs, Alexander. The role of gut microbiota in fetal methylmercury exposure: Insights from a pilot study. United States: N. p., 2016. Web. doi:10.1016/j.toxlet.2015.11.022.
Rothenberg, Sarah E., Keiser, Sharon, Ajami, Nadim J., Wong, Matthew C., Gesell, Jonathan, Petrosino, Joseph F., & Johs, Alexander. The role of gut microbiota in fetal methylmercury exposure: Insights from a pilot study. United States. https://doi.org/10.1016/j.toxlet.2015.11.022
Rothenberg, Sarah E., Keiser, Sharon, Ajami, Nadim J., Wong, Matthew C., Gesell, Jonathan, Petrosino, Joseph F., and Johs, Alexander. Mon . "The role of gut microbiota in fetal methylmercury exposure: Insights from a pilot study". United States. https://doi.org/10.1016/j.toxlet.2015.11.022. https://www.osti.gov/servlets/purl/1286950.
@article{osti_1286950,
title = {The role of gut microbiota in fetal methylmercury exposure: Insights from a pilot study},
author = {Rothenberg, Sarah E. and Keiser, Sharon and Ajami, Nadim J. and Wong, Matthew C. and Gesell, Jonathan and Petrosino, Joseph F. and Johs, Alexander},
abstractNote = {The mechanisms by which gut microbiota contribute to methylmercury metabolism remain unclear. Among a cohort of pregnant mothers, the main objectives of our pilot study were to determine 1) associations between gut microbiota and mercury concentrations in biomarkers (stool, hair and cord blood) and 2) the contributions of gut microbial mercury methylation/demethylation to stool methylmercury. Moreover, for pregnant women (36-39 weeks gestation, n=17) donated hair and stool specimens, and cord blood was collected for a subset (n=7). The diversity of gut microbiota was determined using 16S rRNA gene profiling (n=17). For 6 stool samples with highest/lowest methylmercury concentrations, metagenomic whole genome shotgun sequencing was employed to search for one mercury methylation gene (hgcA), and two mer operon genes involved in methylmercury detoxification (merA and merB). There were seventeen bacterial genera that were significantly correlated (increasing or decreasing) with stool methylmercury, stool inorganic mercury, or hair total mercury; however, aside from one genus, there was no overlap between biomarkers. No definitive matches for hgcA or merB, while merA were detected at low concentrations in all six samples. Proportional differences in stool methylmercury were not likely attributed to gut microbiota through methylation/demethylation. Gut microbiota potentially altered methylmercury metabolism using indirect pathways.},
doi = {10.1016/j.toxlet.2015.11.022},
journal = {Toxicology Letters},
number = C,
volume = 242,
place = {United States},
year = {Mon Feb 01 00:00:00 EST 2016},
month = {Mon Feb 01 00:00:00 EST 2016}
}

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Works referenced in this record:

Bacterial mercury resistance from atoms to ecosystems
journal, June 2003


Microbes inside—from diversity to function: the case of Akkermansia
journal, March 2012


Gut microbiota limits heavy metals burden caused by chronic oral exposure
journal, October 2013


QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

The Toxicology of Mercury and Its Chemical Compounds
journal, January 2006


Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium
journal, September 2004

  • Derrien, M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5
  • DOI: 10.1099/ijs.0.02873-0

Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces
journal, August 2012

  • Dridi, B.; Fardeau, M. -L.; Ollivier, B.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 8
  • DOI: 10.1099/ijs.0.033712-0

Diversity of the Human Intestinal Microbial Flora
journal, June 2005


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Mercury Methylation by Novel Microorganisms from New Environments
journal, September 2013

  • Gilmour, Cynthia C.; Podar, Mircea; Bullock, Allyson L.
  • Environmental Science & Technology, Vol. 47, Issue 20
  • DOI: 10.1021/es403075t

Excretion of Methyl Mercury in Human Feces
journal, January 2000

  • Ishihara, Nobuo
  • Archives of Environmental Health: An International Journal, Vol. 55, Issue 1
  • DOI: 10.1080/00039890009603384

Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding: Mother-neonate bacterial transfer
journal, September 2013

  • Jost, Ted; Lacroix, Christophe; Braegger, Christian P.
  • Environmental Microbiology, Vol. 16, Issue 9
  • DOI: 10.1111/1462-2920.12238

Data, information, knowledge and principle: back to metabolism in KEGG
journal, November 2013

  • Kanehisa, Minoru; Goto, Susumu; Sato, Yoko
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1076

Host Remodeling of the Gut Microbiome and Metabolic Changes during Pregnancy
journal, August 2012


Determination of Methyl Mercury in Whole Blood by Ethylation-GC-CVAFS after Alkaline Digestion-Solvent Extraction
journal, July 2000

  • Liang, L.; Evens, C.; Lazoff, S.
  • Journal of Analytical Toxicology, Vol. 24, Issue 5
  • DOI: 10.1093/jat/24.5.328

Re-evaluation of distillation and comparison with HNO3 leaching/solvent extraction for isolation of methylmercury compounds from sediment/soil samples
journal, May 2004

  • Liang, Lian; Horvat, Milena; Feng, Xinbin
  • Applied Organometallic Chemistry, Vol. 18, Issue 6
  • DOI: 10.1002/aoc.617

Phylogeny of mercury resistance (mer) operons of gram-negative bacteria isolated from the fecal flora of primates
journal, March 1997


Diversity of hair growth profiles
journal, October 2005


UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


The commensal microflora of human milk: new perspectives for food bacteriotherapy and probiotics
journal, March 2004

  • Martı́n, Rocı́o; Langa, Susana; Reviriego, Carlota
  • Trends in Food Science & Technology, Vol. 15, Issue 3-4
  • DOI: 10.1016/j.tifs.2003.09.010

Seafood consumption and blood mercury concentrations in adults aged ≥20 y, 2007–2010
journal, February 2014

  • Nielsen, Samara Joy; Kit, Brian K.; Aoki, Yutaka
  • The American Journal of Clinical Nutrition, Vol. 99, Issue 5
  • DOI: 10.3945/ajcn.113.077081

Maternal Fish Consumption, Hair Mercury, and Infant Cognition in a U.S. Cohort
journal, October 2005

  • Oken, Emily; Wright, Robert O.; Kleinman, Ken P.
  • Environmental Health Perspectives, Vol. 113, Issue 10
  • DOI: 10.1289/ehp.8041

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


Epidemiologic confirmation that fruit consumption influences mercury exposure in riparian communities in the Brazilian Amazon
journal, October 2007


Mucolytic Bacteria With Increased Prevalence in IBD Mucosa Augment In Vitro Utilization of Mucin by Other Bacteria
journal, January 2010

  • Png, Chin Wen; Lindén, Sara K.; Gilshenan, Kristen S.
  • American Journal of Gastroenterology, Vol. 105, Issue 11
  • DOI: 10.1038/ajg.2010.281

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

The influence of obesity on blood mercury levels for U.S. non-pregnant adults and children: NHANES 2007–2010
journal, April 2015


The methylation of mercuric chloride by human intestinal bacteria
journal, September 1975

  • Rowland, I. R.; Grasso, P.; Davies, M. J.
  • Experientia, Vol. 31, Issue 9
  • DOI: 10.1007/BF02326961

Effects of Diet on Mercury Metabolism and Excretion in Mice Given Methylmercury: Role of Gut Flora
journal, November 1984

  • Rowland, I. R.; Robinson, R. D.; Doherty, R. A.
  • Archives of Environmental Health: An International Journal, Vol. 39, Issue 6
  • DOI: 10.1080/00039896.1984.10545872

The effect of various dietary fibres on tissue concentration and chemical form of mercury after methylmercury exposure in mice
journal, July 1986

  • Rowland, Ian R.; Mallett, Anthony K.; Flynn, John
  • Archives of Toxicology, Vol. 59, Issue 2
  • DOI: 10.1007/BF00286730

Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women
journal, March 2010

  • Santacruz, A.; Collado, M. C.; García-Valdés, L.
  • British Journal of Nutrition, Vol. 104, Issue 1
  • DOI: 10.1017/S0007114510000176

Methyl Mercury Decomposition in Mice Treated with Antibiotics
journal, October 1981


Site-Directed Mutagenesis of HgcA and HgcB Reveals Amino Acid Residues Important for Mercury Methylation
journal, February 2015

  • Smith, Steven D.; Bridou, Romain; Johs, Alexander
  • Applied and Environmental Microbiology, Vol. 81, Issue 9
  • DOI: 10.1128/AEM.00217-15

Degradation of methyl and ethyl mercury into inorganic mercury by various phagocytic cells
journal, January 1992

  • Suda, Ikuo; Totoki, Shinji; Uchida, Tetsuya
  • Archives of Toxicology, Vol. 66, Issue 1
  • DOI: 10.1007/BF02307268

Intestinal transport of methylmercury and inorganic mercury in various models of Caco-2 and HT29-MTX cells
journal, September 2013


Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes
journal, September 2011


Maternal Fish Consumption, Mercury Levels, and Risk of Preterm Delivery
journal, January 2007

  • Xue, Fei; Holzman, Claudia; Rahbar, Mohammad Hossein
  • Environmental Health Perspectives, Vol. 115, Issue 1
  • DOI: 10.1289/ehp.9329

Resampling-based false discovery rate controlling multiple test procedures for correlated test statistics
journal, December 1999


Cinnabar is not converted into methylmercury by human intestinal bacteria
journal, April 2011


Works referencing / citing this record:

Comparison of Bacterial Community Structure and Diversity in Traditional Gold Mining Waste Disposal Site and Rice Field by Using a Metabarcoding Approach
journal, January 2020

  • Fatimawali, ; Kepel, Billy Johnson; Gani, Maria Apriliani
  • International Journal of Microbiology, Vol. 2020, p. 1-8
  • DOI: 10.1155/2020/1858732

Intestinal Methylation and Demethylation of Mercury
journal, December 2018

  • Li, Hong; Lin, Xiaoying; Zhao, Jiating
  • Bulletin of Environmental Contamination and Toxicology, Vol. 102, Issue 5
  • DOI: 10.1007/s00128-018-2512-4

Blood total mercury and methylmercury among pregnant mothers in Charleston, South Carolina, USA
journal, April 2018

  • Donohue, Alexis; Wagner, Carol L.; Burch, James B.
  • Journal of Exposure Science & Environmental Epidemiology, Vol. 28, Issue 5
  • DOI: 10.1038/s41370-018-0033-1

Modulators of mercury risk to wildlife and humans in the context of rapid global change
journal, January 2018


Toward Sustainable Environmental Quality: Priority Research Questions for North America
journal, July 2019

  • Fairbrother, Anne; Muir, Derek; Solomon, Keith R.
  • Environmental Toxicology and Chemistry, Vol. 38, Issue 8
  • DOI: 10.1002/etc.4502

Chemical transformation of xenobiotics by the human gut microbiota
journal, June 2017


Toward Sustainable Environmental Quality: Priority Research Questions for North America
journal, July 2019

  • Fairbrother, Anne; Muir, Derek; Solomon, Keith R.
  • Environmental Toxicology and Chemistry, Vol. 38, Issue 8
  • DOI: 10.1002/etc.4502

Modulators of mercury risk to wildlife and humans in the context of rapid global change
journal, January 2018


Chemical transformation of xenobiotics by the human gut microbiota
journal, June 2017