Exposure to environmental pollutants selects for xenobiotic-degrading functions in the human gut microbiome

Francesca De Filippis, Vincenzo Valentino, Giuseppina Sequino, Giorgia Borriello, Marita Georgia Riccardi, Biancamaria Pierri, Pellegrino Cerino, Antonio Pizzolante, Edoardo Pasolli, Mauro Esposito, Antonio Limone and Danilo Ercolini ()
Additional contact information
Francesca De Filippis: University of Naples Federico II, Via Università, 100
Vincenzo Valentino: University of Naples Federico II, Via Università, 100
Giuseppina Sequino: University of Naples Federico II, Via Università, 100
Giorgia Borriello: 2
Marita Georgia Riccardi: 2
Biancamaria Pierri: Animal and Human, Via Salute, 2
Pellegrino Cerino: Animal and Human, Via Salute, 2
Antonio Pizzolante: Animal and Human, Via Salute, 2
Edoardo Pasolli: University of Naples Federico II, Via Università, 100
Mauro Esposito: Animal and Human, Via Salute, 2
Antonio Limone: 2
Danilo Ercolini: University of Naples Federico II, Via Università, 100

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract Environmental pollutants from different chemical families may reach the gut microbiome, where they can be metabolized and transformed. However, how our gut symbionts respond to the exposure to environmental pollution is still underexplored. In this observational, cohort study, we aim to investigate the influence of environmental pollution on the gut microbiome composition and potential activity by shotgun metagenomics. We select as a case study a population living in a highly polluted area in Campania region (Southern Italy), proposed as an ideal field for exposomic studies and we compare the fecal microbiome of 359 subjects living in areas with high, medium and low environmental pollution. We highlight changes in gut microbiome composition and functionality that were driven by pollution exposure. Subjects from highly polluted areas show higher blood concentrations of dioxin and heavy metals, as well as an increase in microbial genes related to degradation and/or resistance to these molecules. Here we demonstrate the dramatic effect that environmental xenobiotics have on gut microbial communities, shaping their composition and boosting the selection of strains with degrading capacity. The gut microbiome can be considered as a pivotal player in the environment-health interaction that may contribute to detoxifying toxic compounds and should be taken into account when developing risk assessment models. The study was registered at ClinicalTrials.gov with the identifier NCT05976126.

Date: 2024
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DOI: 10.1038/s41467-024-48739-7

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