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


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
27 May 2024
Historique:
received: 19 02 2024
accepted: 08 05 2024
medline: 28 5 2024
pubmed: 28 5 2024
entrez: 27 5 2024
Statut: epublish

Résumé

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.

Identifiants

pubmed: 38802370
doi: 10.1038/s41467-024-48739-7
pii: 10.1038/s41467-024-48739-7
doi:

Substances chimiques

Xenobiotics 0
Environmental Pollutants 0
Metals, Heavy 0

Banques de données

ClinicalTrials.gov
['NCT05976126']

Types de publication

Journal Article Observational Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

4482

Subventions

Organisme : Ministero della Salute (Ministry of Health, Italy)
ID : GR-2016-02362975

Informations de copyright

© 2024. The Author(s).

Références

Fan, Y. & Pedersen, O. Gut microbiota in human metabolic health and disease. Nat. Rev. Microbiol. 19, 55–71 (2021).
pubmed: 32887946 doi: 10.1038/s41579-020-0433-9
De Vos, W. M. et al. Gut microbiome and health: mechanistic insights. Gut 71, 1020–1032 (2022).
pubmed: 35105664 doi: 10.1136/gutjnl-2021-326789
Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723–735 (2008).
pubmed: 18549407 doi: 10.1111/j.1574-6976.2008.00123.x
Rosenberg, E. & Zilber-Rosenberg, I. The hologenome concept of evolution after 10 years. Microbiome 6, 78 (2018).
pubmed: 29695294 pmcid: 5922317 doi: 10.1186/s40168-018-0457-9
Henry, L. P. et al. The microbiome extends host evolutionary potential. Nat. Commun. 12, 5141 (2021).
pubmed: 34446709 pmcid: 8390463 doi: 10.1038/s41467-021-25315-x
Obeng, N. et al. Evolution of Microbiota–Host Associations: The Microbe’s Perspective. Trends Microbiol. 29, 779–787 (2021).
pubmed: 33674142 doi: 10.1016/j.tim.2021.02.005
Suzuki, T. A. et al. Codiversification of gut microbiota with humans. Science 377, 1328–1332 (2022).
pubmed: 36108023 pmcid: 10777373 doi: 10.1126/science.abm7759
Lindell, A. E., Zimmermann-Kogadeeva, M. & Patil, K. R. Multimodal interactions of drugs, natural compounds and pollutants with the gut microbiota. Nat. Rev. Microbiol. 20, 431–443 (2022).
pubmed: 35102308 pmcid: 7615390 doi: 10.1038/s41579-022-00681-5
Zimmermann, M. et al. Mapping human microbiome drug metabolism by gut bacteria and their genes. Nature 570, 462–467 (2019).
pubmed: 31158845 pmcid: 6597290 doi: 10.1038/s41586-019-1291-3
Javdan, B. et al. Personalized mapping of drug metabolism by the human gut microbiome. Cell 181, 1661–1679 (2019).
doi: 10.1016/j.cell.2020.05.001
Chiu, K. et al. The impact of environmental chemicals on the gut microbiome. Toxicol. Sci. 176, 253–284 (2020).
pubmed: 32392306 pmcid: 7416318 doi: 10.1093/toxsci/kfaa065
Claus, S. P., Guillou, H. & Ellero-Simatos, S. The gut microbiota: a major player in the toxicity of environmental pollutants? NPJ Biofilms Microbiomes 2, 16003 (2016).
pubmed: 28721242 pmcid: 5515271 doi: 10.1038/npjbiofilms.2016.3
Haiser, H. J. & Turnbaugh, P. J. Developing a metagenomic view of xenobiotic metabolism. Pharmacol. Res. 69, 21–31 (2016).
doi: 10.1016/j.phrs.2012.07.009
Gao, J., Ellis, L. B. & Wackett, L. P. The University of Minnesota Biocatalysis/Biodegradation Database: improving public access. Nucleic Acids Res. 38, 488–491 (2010).
doi: 10.1093/nar/gkp771
Borchert, E. et al. Enhancing microbial pollutant degradation by integrating eco-evolutionary principles with environmental biotechnology. Trends Microbiol. 29, 908–918 (2021).
pubmed: 33812769 doi: 10.1016/j.tim.2021.03.002
Fuller, R. et al. Pollution and health: a progress update. Lancet Planet Health 6, e535–e547 (2022).
pubmed: 35594895 doi: 10.1016/S2542-5196(22)00090-0
Liu, F. et al. Associations between long-term exposure to ambient air pollution and risk of type 2 diabetes mellitus: A systematic review and meta-analysis. Environ. Pollut. 252, 1235–1245 (2019).
pubmed: 31252121 doi: 10.1016/j.envpol.2019.06.033
Wolf, K. et al. Long-term exposure to low-level ambient air pollution and incidence of stroke and coronary heart disease: a pooled analysis of six European cohorts within the ELAPSE project. Lancet Planet Health 5, e620–e632 (2021).
pubmed: 34508683 doi: 10.1016/S2542-5196(21)00195-9
Gourd, E. New evidence that air pollution contributes substantially to lung cancer. Lancet Oncol. 23, e448 (2022).
pubmed: 36116453 doi: 10.1016/S1470-2045(22)00569-1
Mazza, A. et al. Heavy environmental pressure in Campania and other Italian regions: A short review of available evidence. Int. J. Environ. Res. Public Health 15, 105 (2018).
pubmed: 29320415 pmcid: 5800204 doi: 10.3390/ijerph15010105
Falcone, P. M. & De Rosa, S. P. Use of fuzzy cognitive maps to develop policy strategies for the optimization of municipal waste management: A case study of the land of fires (Italy). Land Use Policy 96, 104680 (2020).
doi: 10.1016/j.landusepol.2020.104680
Di Lorenzo, G. et al. Increased risk of bladder cancer in critical areas at high pressure of pollution of the Campania region in Italy: A systematic review. Crit. Rev. Oncol. Hematol. 96, 534–541 (2015).
pubmed: 26520458 doi: 10.1016/j.critrevonc.2015.07.004
Nature Editorial. A toxic legacy. Nature 508, 431 (2014).
Senior, K. & Mazza, A. Italian “Triangle of death” linked to waste crisis. Lancet Oncol. 5, 525–527 (2004).
pubmed: 15384216 doi: 10.1016/S1470-2045(04)01561-X
Triassi, M. et al. Environmental pollution from illegal waste disposal and health effects: a review on the “triangle of death”. Int. J. Environ. Res. Public Health 12, 1216–1236 (2015).
pubmed: 25622140 pmcid: 4344663 doi: 10.3390/ijerph120201216
Qu, C. et al. High spatial resolution measurements of passive-sampler derived air concentrations of persistent organic pollutants in the Campania region, Italy: Implications for source identification and risk analysis. Environ. Pollut. 286, 117248 (2021).
pubmed: 33984778 doi: 10.1016/j.envpol.2021.117248
Qu, C. et al. The occurrence of OCPs, PCBs, and PAHs in the soil, air, and bulk deposition of the Naples metropolitan area, southern Italy: Implications for sources and environmental processes. Environ. Int. 124, 89–97 (2019).
pubmed: 30640133 doi: 10.1016/j.envint.2018.12.031
Pierri, B. et al. Exposure study on susceptible people - SPES: An integrative biomonitoring approach. Environ. Int. 158, 106931 (2022).
pubmed: 34653810 doi: 10.1016/j.envint.2021.106931
Pizzolante, A. et al. Development of a municipality index of environmental pressure in Campania, Italy. Future Sci. OA 7, FSO720 (2021).
pubmed: 34258027 pmcid: 8256331 doi: 10.2144/fsoa-2021-0055
Oren, A., Garrity, G. M. Valid publication of the names of forty-two phyla of prokaryotes. Int. J. Syst. Evol. Microbio. 71, https://doi.org/10.1099/ijsem.0.005056 (2021).
Wild, C. P. Complementing the genome with an “exposome”: the outstanding challenge of environmental exposure measurement in molecular epidemiology. Cancer Epidemiol. Biomark. Prev. 14, 1847–1850 (2005).
doi: 10.1158/1055-9965.EPI-05-0456
Giambò, F. et al. Role-playing between environmental pollutants and human gut microbiota: A complex bidirectional interaction. Front. Med. 29, 810397 (2022).
doi: 10.3389/fmed.2022.810397
Wang, Z. et al. Genome characteristics reveal the biocontrol potential of Actinobacteria isolated from sugarcane rhizosphere. Front. Microbiol. 12, 797889 (2021).
pubmed: 35003029 pmcid: 8740303 doi: 10.3389/fmicb.2021.797889
Saibu, S., Adebusoye, S. A. & Oyetibo, G. O. Soil microbiome response to 2-chlorodibenzo-p-dioxin during bioremediation of contaminated tropical soil in a microcosm-based study. J. Hazard Mater. 451, 131105 (2023).
pubmed: 36893594 doi: 10.1016/j.jhazmat.2023.131105
Mawang, C. I. et al. Actinobacteria: An eco-friendly and promising technology for the bioaugmentation of contaminants. Biotechnol. Rep. 32, e00679 (2021).
doi: 10.1016/j.btre.2021.e00679
Chen, S. C. et al. Novel clades of soil biphenyl degraders revealed by integrating isotope probing, multi-omics, and single-cell analyses. ISME J. 15, 3508–3521 (2021).
pubmed: 34117322 pmcid: 8630052 doi: 10.1038/s41396-021-01022-9
Abdelsalam, N. A. et al. Toxicomicrobiomics: The human microbiome vs. pharmaceutical, dietary, and environmental xenobiotics. Front. Pharmacol. 11, 390 (2020).
pubmed: 32372951 pmcid: 7179069 doi: 10.3389/fphar.2020.00390
Dickinson, A. W. et al. Heavy metal pollution and co-selection for antibiotic resistance: A microbial palaeontology approach. Environ. Int. 132, 105117 (2019).
pubmed: 31473413 doi: 10.1016/j.envint.2019.105117
Xu, Y. et al. Effect of the selective pressure of sub-lethal level of heavy metals on the fate and distribution of ARGs in the catchment scale. Environ. Pollut. 220, 900–908 (2017).
pubmed: 27876226 doi: 10.1016/j.envpol.2016.10.074
Seiler, C. & Berendonk, T. U. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol. 3, 399 (2012).
pubmed: 23248620 pmcid: 3522115 doi: 10.3389/fmicb.2012.00399
Baker-Austin, C. et al. Co-selection of antibiotic and metal resistance. Trends Microbiol 14, 176–182 (2006).
pubmed: 16537105 doi: 10.1016/j.tim.2006.02.006
Ng, E. L. et al. Microplastic pollution alters forest soil microbiome. J. Hazard Mater. 409, 124606 (2021).
pubmed: 33246819 doi: 10.1016/j.jhazmat.2020.124606
Dell’Anno, F. et al. Microbiome enrichment from contaminated marine sediments unveils novel bacterial strains for petroleum hydrocarbon and heavy metal bioremediation. Environ. Pollut. 317, 120772 (2023).
pubmed: 36455775 doi: 10.1016/j.envpol.2022.120772
Zrimec, J. et al. Plastic-degrading potential across the global microbiome correlates with recent pollution trends. mBio 12, e0215521 (2021).
pubmed: 34700384 doi: 10.1128/mBio.02155-21
Thriene, K. & Michels, K. B. Human gut microbiota plasticity throughout the life course. Int. J. Environ. Res. Public Health 20, 1463 (2023).
pubmed: 36674218 pmcid: 9860808 doi: 10.3390/ijerph20021463
Gomez, A. et al. Plasticity in the human gut microbiome defies evolutionary constraints. mSphere 4, e00271–19 (2019).
pubmed: 31366708 pmcid: 6669335 doi: 10.1128/mSphere.00271-19
Weersma, R. K., Zhernakova, A. & Fu, J. Interaction between drugs and the gut microbiome. Gut 69, 1510–1519 (2020).
pubmed: 32409589 doi: 10.1136/gutjnl-2019-320204
Riboli, E. et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 5, 1113–1124 (2002).
pubmed: 12639222 doi: 10.1079/PHN2002394
Brasseur, C. et al. Levels of dechloranes and polybrominated diphenyl ethers (PBDEs) in human serum from France. Environ. Int. 65, 33–40 (2014).
pubmed: 24440800 doi: 10.1016/j.envint.2013.12.014
Van den Berg, M. et al. The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 93, 223–241 (2006).
pubmed: 16829543 doi: 10.1093/toxsci/kfl055
Morton, J. T. et al. Learning representations of microbe–metabolite interactions. Nat. Methods 16, 1306–1314 (2019).
pubmed: 31686038 pmcid: 6884698 doi: 10.1038/s41592-019-0616-3
Pasolli, E. et al. Machine learning meta-analysis of large metagenomic datasets: tools and biological insights. PLoS Comput. Biol. 12, e1004977 (2016).
pubmed: 27400279 pmcid: 4939962 doi: 10.1371/journal.pcbi.1004977

Auteurs

Francesca De Filippis (F)

Department of Agricultural Sciences, University of Naples Federico II, Via Università, 100, Portici, Italy.
Task Force on Microbiome Studies, University of Naples Federico II, Corso Umberto I, 40, Napoli, Italy.
Istituto Zooprofilattico Sperimentale del Mezzogiorno, Via Salute, 2, Portici, Italy.

Vincenzo Valentino (V)

Department of Agricultural Sciences, University of Naples Federico II, Via Università, 100, Portici, Italy.

Giuseppina Sequino (G)

Department of Agricultural Sciences, University of Naples Federico II, Via Università, 100, Portici, Italy.

Giorgia Borriello (G)

Istituto Zooprofilattico Sperimentale del Mezzogiorno, Via Salute, 2, Portici, Italy.

Marita Georgia Riccardi (MG)

Istituto Zooprofilattico Sperimentale del Mezzogiorno, Via Salute, 2, Portici, Italy.

Biancamaria Pierri (B)

National Reference Centre for the Analysis and Study of the Correlation between Environment, Animal and Human, Via Salute, 2, Portici, Italy.

Pellegrino Cerino (P)

National Reference Centre for the Analysis and Study of the Correlation between Environment, Animal and Human, Via Salute, 2, Portici, Italy.

Antonio Pizzolante (A)

National Reference Centre for the Analysis and Study of the Correlation between Environment, Animal and Human, Via Salute, 2, Portici, Italy.

Edoardo Pasolli (E)

Department of Agricultural Sciences, University of Naples Federico II, Via Università, 100, Portici, Italy.
Task Force on Microbiome Studies, University of Naples Federico II, Corso Umberto I, 40, Napoli, Italy.

Mauro Esposito (M)

National Reference Centre for the Analysis and Study of the Correlation between Environment, Animal and Human, Via Salute, 2, Portici, Italy.

Antonio Limone (A)

Istituto Zooprofilattico Sperimentale del Mezzogiorno, Via Salute, 2, Portici, Italy.

Danilo Ercolini (D)

Department of Agricultural Sciences, University of Naples Federico II, Via Università, 100, Portici, Italy. ercolini@unina.it.
Task Force on Microbiome Studies, University of Naples Federico II, Corso Umberto I, 40, Napoli, Italy. ercolini@unina.it.

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