Changes in the gut microbiota of mice orally exposed to methylimidazolium ionic liquids

Gregory R Young; Tarek M Abdelghany; Alistair C Leitch; Michael P Dunn; Peter G Blain; Clare Lanyon; Matthew C Wright

doi:10.1371/journal.pone.0229745

Changes in the gut microbiota of mice orally exposed to methylimidazolium ionic liquids

Gregory R Young, Tarek M Abdelghany, Alistair C Leitch, Michael P Dunn, Peter G Blain, Clare Lanyon, Matthew C Wright

Research output: Contribution to journal › Article › peer-review

25 Citations (Scopus)

38 Downloads (Pure)

Abstract

Ionic liquids are salts used in a variety of industrial processes, and being relatively non-volatile, are proposed as environmentally-friendly replacements for existing volatile liquids. Methylimidazolium ionic liquids resist complete degradation in the environment, likely because the imidazolium moiety does not exist naturally in biological systems. However, there is limited data available regarding their mammalian effects in vivo. This study aimed to examine the effects of exposing mice separately to 2 different methylimidazolium ionic liquids (BMI and M8OI) through their addition to drinking water. Potential effects on key target organs-the liver and kidney-were examined, as well as the gut microbiome. Adult male mice were exposed to drinking water containing ionic liquids at a concentration of 440 mg/L for 18 weeks prior to examination of tissues, serum, urine and the gut microbiome. Histopathology was performed on tissues and clinical chemistry on serum for biomarkers of hepatic and renal injury. Bacterial DNA was isolated from the gut contents and subjected to targeted 16S rRNA sequencing. Mild hepatic and renal effects were limited to glycogen depletion and mild degenerative changes respectively. No hepatic or renal adverse effects were observed. In contrast, ionic liquid exposure altered gut microbial composition but not overall alpha diversity. Proportional abundance of Lachnospiraceae, Clostridia and Coriobacteriaceae spp. were significantly greater in ionic liquid-exposed mice, as were predicted KEGG functional pathways associated with xenobiotic and amino acid metabolism. Exposure to ionic liquids via drinking water therefore resulted in marked changes in the gut microbiome in mice prior to any overt pathological effects in target organs. Ionic liquids may be an emerging risk to health through their potential effects on the gut microbiome, which is implicated in the causes and/or severity of an array of chronic disease in humans.

Original language	English
Article number	e0229745
Journal	PLoS One
Volume	15
Issue number	3
DOIs	https://doi.org/10.1371/journal.pone.0229745
Publication status	Published - 12 Mar 2020

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being
SDG 6 Clean Water and Sanitation

Access to Document

10.1371/journal.pone.0229745Licence: CC BY

journal.pone.0229745Final published version, 2.91 MBLicence: CC BY

Cite this

@article{a8993a16296a4250afb82c861b6ca90e,

title = "Changes in the gut microbiota of mice orally exposed to methylimidazolium ionic liquids",

abstract = "Ionic liquids are salts used in a variety of industrial processes, and being relatively non-volatile, are proposed as environmentally-friendly replacements for existing volatile liquids. Methylimidazolium ionic liquids resist complete degradation in the environment, likely because the imidazolium moiety does not exist naturally in biological systems. However, there is limited data available regarding their mammalian effects in vivo. This study aimed to examine the effects of exposing mice separately to 2 different methylimidazolium ionic liquids (BMI and M8OI) through their addition to drinking water. Potential effects on key target organs-the liver and kidney-were examined, as well as the gut microbiome. Adult male mice were exposed to drinking water containing ionic liquids at a concentration of 440 mg/L for 18 weeks prior to examination of tissues, serum, urine and the gut microbiome. Histopathology was performed on tissues and clinical chemistry on serum for biomarkers of hepatic and renal injury. Bacterial DNA was isolated from the gut contents and subjected to targeted 16S rRNA sequencing. Mild hepatic and renal effects were limited to glycogen depletion and mild degenerative changes respectively. No hepatic or renal adverse effects were observed. In contrast, ionic liquid exposure altered gut microbial composition but not overall alpha diversity. Proportional abundance of Lachnospiraceae, Clostridia and Coriobacteriaceae spp. were significantly greater in ionic liquid-exposed mice, as were predicted KEGG functional pathways associated with xenobiotic and amino acid metabolism. Exposure to ionic liquids via drinking water therefore resulted in marked changes in the gut microbiome in mice prior to any overt pathological effects in target organs. Ionic liquids may be an emerging risk to health through their potential effects on the gut microbiome, which is implicated in the causes and/or severity of an array of chronic disease in humans.",

author = "Young, \{Gregory R\} and Abdelghany, \{Tarek M\} and Leitch, \{Alistair C\} and Dunn, \{Michael P\} and Blain, \{Peter G\} and Clare Lanyon and Wright, \{Matthew C\}",

note = "Funding Information: This work was funded by grants from the Medical Research Council (in the form of a DTP Supplement to A.C.L.) [https://mrc.ukri.org/] and the Newton-Mosharafa Fund (in the form of a studentship supporting T.M.A) [https://www. britishcouncil.org.eg/en/programmes/education/ newton-mosharafa-fund]. The work was in part, also supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) [https://www.nihr.ac.uk/] in Chemical and Radiation Threats and Hazards in partnership with Public Health England (M.C.W. and P. G. B), Grant \# HPRU-2012-10076. NIHR HPRU funding was used for the part of the research that did not involve any live animals. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, the Department of Health or Public Health England. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors acknowledge Dr Darren Smith and Dr Andrew Nelson of NUOmics for performing targeted sequencing and providing raw .fastq sequencing files. This paper is dedicated to the memory of Dr Michael Dunn. Publisher Copyright: {\textcopyright} 2020 Young et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",

year = "2020",

month = mar,

day = "12",

doi = "10.1371/journal.pone.0229745",

language = "English",

volume = "15",

journal = "PLoS One",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "3",

}

TY - JOUR

T1 - Changes in the gut microbiota of mice orally exposed to methylimidazolium ionic liquids

AU - Young, Gregory R

AU - Abdelghany, Tarek M

AU - Leitch, Alistair C

AU - Dunn, Michael P

AU - Blain, Peter G

AU - Lanyon, Clare

AU - Wright, Matthew C

N1 - Funding Information: This work was funded by grants from the Medical Research Council (in the form of a DTP Supplement to A.C.L.) [https://mrc.ukri.org/] and the Newton-Mosharafa Fund (in the form of a studentship supporting T.M.A) [https://www. britishcouncil.org.eg/en/programmes/education/ newton-mosharafa-fund]. The work was in part, also supported by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) [https://www.nihr.ac.uk/] in Chemical and Radiation Threats and Hazards in partnership with Public Health England (M.C.W. and P. G. B), Grant # HPRU-2012-10076. NIHR HPRU funding was used for the part of the research that did not involve any live animals. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, the Department of Health or Public Health England. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors acknowledge Dr Darren Smith and Dr Andrew Nelson of NUOmics for performing targeted sequencing and providing raw .fastq sequencing files. This paper is dedicated to the memory of Dr Michael Dunn. Publisher Copyright: © 2020 Young et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/3/12

Y1 - 2020/3/12

N2 - Ionic liquids are salts used in a variety of industrial processes, and being relatively non-volatile, are proposed as environmentally-friendly replacements for existing volatile liquids. Methylimidazolium ionic liquids resist complete degradation in the environment, likely because the imidazolium moiety does not exist naturally in biological systems. However, there is limited data available regarding their mammalian effects in vivo. This study aimed to examine the effects of exposing mice separately to 2 different methylimidazolium ionic liquids (BMI and M8OI) through their addition to drinking water. Potential effects on key target organs-the liver and kidney-were examined, as well as the gut microbiome. Adult male mice were exposed to drinking water containing ionic liquids at a concentration of 440 mg/L for 18 weeks prior to examination of tissues, serum, urine and the gut microbiome. Histopathology was performed on tissues and clinical chemistry on serum for biomarkers of hepatic and renal injury. Bacterial DNA was isolated from the gut contents and subjected to targeted 16S rRNA sequencing. Mild hepatic and renal effects were limited to glycogen depletion and mild degenerative changes respectively. No hepatic or renal adverse effects were observed. In contrast, ionic liquid exposure altered gut microbial composition but not overall alpha diversity. Proportional abundance of Lachnospiraceae, Clostridia and Coriobacteriaceae spp. were significantly greater in ionic liquid-exposed mice, as were predicted KEGG functional pathways associated with xenobiotic and amino acid metabolism. Exposure to ionic liquids via drinking water therefore resulted in marked changes in the gut microbiome in mice prior to any overt pathological effects in target organs. Ionic liquids may be an emerging risk to health through their potential effects on the gut microbiome, which is implicated in the causes and/or severity of an array of chronic disease in humans.

AB - Ionic liquids are salts used in a variety of industrial processes, and being relatively non-volatile, are proposed as environmentally-friendly replacements for existing volatile liquids. Methylimidazolium ionic liquids resist complete degradation in the environment, likely because the imidazolium moiety does not exist naturally in biological systems. However, there is limited data available regarding their mammalian effects in vivo. This study aimed to examine the effects of exposing mice separately to 2 different methylimidazolium ionic liquids (BMI and M8OI) through their addition to drinking water. Potential effects on key target organs-the liver and kidney-were examined, as well as the gut microbiome. Adult male mice were exposed to drinking water containing ionic liquids at a concentration of 440 mg/L for 18 weeks prior to examination of tissues, serum, urine and the gut microbiome. Histopathology was performed on tissues and clinical chemistry on serum for biomarkers of hepatic and renal injury. Bacterial DNA was isolated from the gut contents and subjected to targeted 16S rRNA sequencing. Mild hepatic and renal effects were limited to glycogen depletion and mild degenerative changes respectively. No hepatic or renal adverse effects were observed. In contrast, ionic liquid exposure altered gut microbial composition but not overall alpha diversity. Proportional abundance of Lachnospiraceae, Clostridia and Coriobacteriaceae spp. were significantly greater in ionic liquid-exposed mice, as were predicted KEGG functional pathways associated with xenobiotic and amino acid metabolism. Exposure to ionic liquids via drinking water therefore resulted in marked changes in the gut microbiome in mice prior to any overt pathological effects in target organs. Ionic liquids may be an emerging risk to health through their potential effects on the gut microbiome, which is implicated in the causes and/or severity of an array of chronic disease in humans.

UR - https://www.scopus.com/pages/publications/85081699575

U2 - 10.1371/journal.pone.0229745

DO - 10.1371/journal.pone.0229745

M3 - Article

C2 - 32163446

SN - 1932-6203

VL - 15

JO - PLoS One

JF - PLoS One

IS - 3

M1 - e0229745

ER -

Changes in the gut microbiota of mice orally exposed to methylimidazolium ionic liquids

Abstract

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this