Associations between UK tap water and gut microbiota composition suggest the gut microbiome as a potential mediator of health differences linked to water quality
Graphical abstract
Introduction
Improvements in household drinking water quality have been a global public health success (WHO, 2017). Clean water is important for drinking, food preparation and cleaning, and supplying soluble minerals essential for human health. Many studies have drawn links between drinking (tap) water composition and human health (Ayoob and Gupta, 2006; Bouchard et al., 2011; Payment et al., 1997; Schuster et al., 2005). Negative health effects linked to poor water quality are particularly acute in urban areas (e.g. Marsalek and Rochfort, 2004) and also where synthetic products such as insecticides (Klarich et al., 2017) or industrial emissions (Whelton et al., 2015) enter local watercourses that feed water treatment works. Most research seeking to pinpoint sources of drinking water-induced ill-health focuses on environmental factors such as point-source contamination (Hu et al., 2016; Whelton et al., 2015), deficiencies in drinking water distribution systems (Hull and Zodrow, 2017) or variations in aquatic microbiology (Su et al., 2018). Physiological controls are rarely considered. Human gut microbiota represent the transmission pathway of minerals, nutrients and, in individuals lacking colonisation resistance (Litvak and Bäumler, 2019), a reservoir of potentially deleterious microbes from ingested water. The potential for human gut microbiota to act as mediators, or the biological intermediaries, between drinking water and health impacts has been surprisingly overlooked.
Tap water, here used to refer to drinking water from mains water supplies, has the potential to influence microbiota composition in two ways, either as a carrier of bacteria leading to novel exposures or by impacting existing microbiota based on variable solute composition. Exposure to different sources of tap water has been observed to differentially influence microbiota composition in mice, potentially via exposure to water-borne microbial species (Dias et al., 2018). A similar mechanism could also occur in a human population setting given recent evidence of bacterial shedding from biofilms in water distribution systems (Chan et al., 2019; Makris et al., 2014). The solute composition of water may also influence the human microbiota directly. For example, fluoridation of drinking water has been observed to have a selective impact on the composition of the oral, but not gut, microbiome in mice (Yasuda et al., 2017). Similarly, several enteric bacteria are thought to be involved with the metabolic conversion of nitrate to nitrite, and subsequently to ammonia (Tiso and Schechter, 2015). Lower tap water pH has been associated with faster development of insulitis and hyperglycaemia in non-obese diabetic mice with concurrent changes in gut microbiota composition (Sofi et al., 2014). Conversely, in a cross-over study assessing association between gut microbiota and host glucose regulation, a change in tap water pH did not confer associated alterations to gut microbiota composition (Hansen et al., 2018). Water hardness (obtained from national composition studies) has also been associated with several bacterial genera of the oral microbiota (Willis et al., 2018).
We conducted the first preliminary assessment of gut microbiota as a potential mediator between tap water and human health. We used a novel experimental approach that compares solute concentration measurements of domestic tap water with microbiome and health data from the TwinsUK dataset. The use of identical twins allows genetic and early life factors to be controlled for each participant, increasing the power to detect environmental effects. Solutes in domestic tap water were therefore measured and compared with the microbial composition of the human gut measured by 16S rRNA gene amplicon sequencing in 85 mono-zygotic twins from across the UK. This work is important as it further the under-studied hypothesis that the gut microbiota could mediate the effects of tap water composition on host health.
Section snippets
Participant data
Data for the study was provided by TwinsUK, a cohort administered by the Department of Twin Research and Genetic Epidemology at King's College London, UK. TwinsUK is the UK's largest registry of mono and di-zygotic twins. Created in 1992, the registry was originated to assess the heritability of osteoarthritis and osteoporosis and has grown to be one of the most clinically detailed twin cohorts worldwide, with ~14,000 adult twin volunteers from across the UK. Data relating to genetic structure,
Results
85 participants provided at least one water sample (n = 81 providing 2 samples) and completed a water habits questionnaire (see materials & methods); 36 twin pairs are included in this analysis (Fig. 1). Where individuals had provided two samples from the same location there was high correlation of solutes (Supplementary material S7). The first 3 principle components (PC's) of a multiple factor analysis (MFA) of solute levels in water samples suggested the 3 primary solutes contributing to the
Discussion
In this analysis, we observe significant associations between tap water solute and gut microbiota composition, although adjustment for biological variation between participants masked some of these linkages. Key findings were that sodium ADD associated with species diversity, overall microbial community composition differed in association with sulphate ADD and chloride ADD (although not in adjusted models), and there were multiple signatures where the abundance of taxa associated with aspects
Ethics approval and consent to participate
Favourable ethical opinion was granted by the formerly known St. Thomas' Hospital Research Ethics Committee (REC). Following restructure and merging of REC, subsequent amendments were approved by the NRES Committee London—Westminster (TwinsUK, REC ref: EC04/015, 1 November 2011); use of microbiota samples was granted NRES Committee London—Westminster (The Flora Twin Study, REC ref.: 12/LO/0227, 1 November 2011).
Availability of data and material
The European Bioinformatics Institute (EBI) accession numbers for the sequences reported in this paper is ERP015317.
The processed ASV data, along with phenotypic data that can be used to recreate this analysis is available following reasonable request to the TwinsUK data access committee. Information on data access and how to apply is available at http://www.twinsuk.ac.uk/data-access/submission-procedure-2/. Please contact the corresponding author for further detail.
Funding
Twins UK receives funding from the Wellcome Trust (WT081878MA), the National Institute for Health Research (NIHR) Clinical Research Facility at Guy's & St Thomas' NHS Foundation Trust and NIHR Biomedical Research Centre based at Guy's and St Thomas' NHS Foundation Trust and King's College London. This work was also supported by the Chronic Disease Research Foundation.
CRediT authorship contribution statement
Ruth C.E. Bowyer: Methodology, Project administration, Formal analysis, Writing - original draft, Writing - review & editing. Daniel N. Schillereff: Formal analysis, Data curation, Writing - original draft, Writing - review & editing. Matthew A. Jackson: Resources, Writing - review & editing. Caroline Le Roy: Writing - review & editing. Philippa M. Wells: Writing - review & editing. Tim D. Spector: Methodology, Project administration, Writing - review & editing. Claire J. Steves: Methodology,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors of this paper wish to express our appreciation to all study participants of the TwinsUK cohort for donating their samples and time. TwinsUK is funded by the Wellcome Trust, Medical Research Council, European Union, the National Institute for Health Research (NIHR)-funded BioResource, Clinical Research Facility and Biomedical Research Centre based at Guy's and St Thomas' NHS Foundation Trust in partnership with King's College London.
We thank Dr. Julia K Goodrich, Dr. Ruth E Ley and
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