Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins

Abstract

Background: Dietary habits have a profound influence on the metabolic activity of gut microorganisms and their influence on health. Concerns have been raised as to whether the consumption of foodstuffs contaminated with pesticides can contribute to the development of chronic disease by affecting the gut microbiome. We performed the first pesticide biomonitoring survey of the British population, and subsequently used the results to perform the first pesticide association study on gut microbiome composition and function from the TwinsUK registry.

Methods: Dietary exposure of 186 common insecticide, herbicide, or fungicide residues and the faecal microbiome in 65 twin pairs in the UK was investigated. We evaluated if dietary habits, geographic location, or the rural/urban environment, are associated with the excretion of pesticide residues. The composition and metabolic activity of faecal microbiota was evaluated using shotgun metagenomics and metabolomics respectively. We performed a targeted urine metabolomics analysis in order to evaluate whether pesticide urinary excretion was also associated with physiological changes.

Results: Pyrethroid and/or organophosphorus insecticide residues were found in all urine samples, while the herbicide glyphosate was found in 53% of individuals. Food frequency questionnaires showed that residues from organophosphates were higher with increased consumption of fruit and vegetables. A total of 34 associations between pesticide residue concentrations and faecal metabolite concentrations were detected. Glyphosate excretion was positively associated with an overall increased bacterial species richness, as well as to fatty acid metabolites and phosphate levels. The insecticide metabolite Br2CA, reflecting deltamethrin exposure, was positively associated with the phytoestrogens enterodiol and enterolactone, and negatively associated with some N-methyl amino acids. Urine metabolomics performed on a subset of samples did not reveal associations with the excretion of pesticide residues.

Conclusions: The consumption of conventionally grown fruit and vegetables leads to higher ingestion of pesticides with unknown long-term health consequences. Our results highlight the need for future dietary intervention studies to understand effects of pesticide exposure on the gut microbiome and possible health consequences.

Keywords: Biomonitoring; Dietary habits; Food intake; Gut microbiota; Pesticides.

Fig. 1

Association between urinary concentrations of glyphosate and faecal microbiota metabolism in 124 individuals. A Detection of glyphosate in a urine sample spiked with 0.1 μg/L of glyphosate. B MRM transition spectrum for the same sample. C Urinary glyphosate levels as a boxplot with the highest censoring threshold (LOQ) shown as a horizontal line. D Glyphosate levels according to living areas. E Faecal metabolites, which have the largest difference in abundance as box plots. F Beta diversity using Bray-Curtis dissimilarity. G Alpha diversity as the number of observed species. H. Relative abundance (as copies per million, cpm) for the bacteria contributing to the abundance (white to red: relative abundance; grey: undetected) of the shikimate pathway (as MetaCyc: chorismate biosynthesis I)

Fig. 2

Deep phenotyping of the faecal microbiome in 130 individuals (65 twin pairs). A Faecal metabolomics allow the detection of a large number of metabolites from different classes, including xenobiotics. B Correlations between the abundance of gut microorganisms and metabolites (positive, red; negative, blue) inform on the interaction between environmental exposures and the metabolism of the gut microbiome