IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48739-7.html
   My bibliography  Save this article

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

Author

Listed:
  • Francesca De Filippis

    (University of Naples Federico II, Via Università, 100
    University of Naples Federico II, Corso Umberto I, 40)

  • Vincenzo Valentino

    (University of Naples Federico II, Via Università, 100)

  • Giuseppina Sequino

    (University of Naples Federico II, Via Università, 100)

  • Giorgia Borriello
  • Marita Georgia Riccardi
  • 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
    University of Naples Federico II, Corso Umberto I, 40)

  • Mauro Esposito

    (Animal and Human, Via Salute, 2)

  • Antonio Limone
  • Danilo Ercolini

    (University of Naples Federico II, Via Università, 100
    University of Naples Federico II, Corso Umberto I, 40)

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.

Suggested Citation

  • Francesca De Filippis & Vincenzo Valentino & Giuseppina Sequino & Giorgia Borriello & Marita Georgia Riccardi & Biancamaria Pierri & Pellegrino Cerino & Antonio Pizzolante & Edoardo Pasolli & Mauro Es, 2024. "Exposure to environmental pollutants selects for xenobiotic-degrading functions in the human gut microbiome," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48739-7
    DOI: 10.1038/s41467-024-48739-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48739-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48739-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Alfredo Mazza & Prisco Piscitelli & Andrea Falco & Maria Lucia Santoro & Manuela Colangelo & Giovanni Imbriani & Adele Idolo & Antonella De Donno & Leopoldo Iannuzzi & Annamaria Colao, 2018. "Heavy Environmental Pressure in Campania and Other Italian Regions: A Short Review of Available Evidence," IJERPH, MDPI, vol. 15(1), pages 1-12, January.
    2. Maria Triassi & Rossella Alfano & Maddalena Illario & Antonio Nardone & Oreste Caporale & Paolo Montuori, 2015. "Environmental Pollution from Illegal Waste Disposal and Health Effects: A Review on the “Triangle of Death”," IJERPH, MDPI, vol. 12(2), pages 1-21, January.
    3. Lucas P. Henry & Marjolein Bruijning & Simon K. G. Forsberg & Julien F. Ayroles, 2021. "The microbiome extends host evolutionary potential," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Edoardo Pasolli & Duy Tin Truong & Faizan Malik & Levi Waldron & Nicola Segata, 2016. "Machine Learning Meta-analysis of Large Metagenomic Datasets: Tools and Biological Insights," PLOS Computational Biology, Public Library of Science, vol. 12(7), pages 1-26, July.
    5. Michael Zimmermann & Maria Zimmermann-Kogadeeva & Rebekka Wegmann & Andrew L. Goodman, 2019. "Mapping human microbiome drug metabolism by gut bacteria and their genes," Nature, Nature, vol. 570(7762), pages 462-467, June.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Maurizio Bifulco, 2015. "Comments on Triassi et al. Environmental Pollution from Illegal Waste Disposal and Health Effects: A Review on the “Triangle of Death”. Int. J. Environ. Res. Public Health 2015, 12 , 1216–1236," IJERPH, MDPI, vol. 12(3), pages 1-2, March.
    2. Jaron Thompson & Renee Johansen & John Dunbar & Brian Munsky, 2019. "Machine learning to predict microbial community functions: An analysis of dissolved organic carbon from litter decomposition," PLOS ONE, Public Library of Science, vol. 14(7), pages 1-16, July.
    3. Vivianni Palmeira Wanderley & Fernando Luiz Affonso Fonseca & André Vala Quiaios & José Nuno Domingues & Susana Paixão & João Figueiredo & Ana Ferreira & Cleonice De Almeida Pinto & Odair Ramos Da Sil, 2017. "Socio-Environmental and Hematological Profile of Landfill Residents (São Jorge Landfill–Sao Paulo, Brazil)," IJERPH, MDPI, vol. 14(1), pages 1-12, January.
    4. Benett Siyabonga Madonsela & Machete Machete & Karabo Shale, 2024. "Indigenous Knowledge Systems of Solid Waste Management in Bushbuckridge Rural Communities, South Africa," Waste, MDPI, vol. 2(3), pages 1-19, August.
    5. Yadid M. Algavi & Elhanan Borenstein, 2023. "A data-driven approach for predicting the impact of drugs on the human microbiome," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Elżbieta M. Zębek & Jakub J. Zięty, 2022. "Effect of Landfill Arson to a “Lax” System in a Circular Economy under the Current EU Energy Policy: Perspective Review in Waste Management Law," Energies, MDPI, vol. 15(22), pages 1-25, November.
    7. Salvatore Raimondo & Mariacira Gentile & Giusy Esposito & Tommaso Gentile & Ida Ferrara & Claudia Crescenzo & Mariangela Palmieri & Felice Cuomo & Stefania De Filippo & Gennaro Lettieri & Marina Pisco, 2021. "Could Kallikrein-Related Serine Peptidase 3 Be an Early Biomarker of Environmental Exposure in Young Women?," IJERPH, MDPI, vol. 18(16), pages 1-15, August.
    8. Daniel Chang & Vinod K. Gupta & Benjamin Hur & Sergio Cobo-López & Kevin Y. Cunningham & Nam Soo Han & Insuk Lee & Vanessa L. Kronzer & Levi M. Teigen & Lioudmila V. Karnatovskaia & Erin E. Longbrake , 2024. "Gut Microbiome Wellness Index 2 enhances health status prediction from gut microbiome taxonomic profiles," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Paolo Manghi & Michele Filosi & Moreno Zolfo & Lucas G. Casten & Albert Garcia-Valiente & Stefania Mattevi & Vitor Heidrich & Davide Golzato & Samuel Perini & Andrew M. Thomas & Simone Montalbano & Sa, 2024. "Large-scale metagenomic analysis of oral microbiomes reveals markers for autism spectrum disorders," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Reilly Pidgeon & Sacha Mitchell & Michael Shamash & Layan Suleiman & Lharbi Dridi & Corinne F. Maurice & Bastien Castagner, 2025. "Diet-derived urolithin A is produced by a dehydroxylase encoded by human gut Enterocloster species," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    11. Mason. R. Stothart & Philip. D. McLoughlin & Sarah. A. Medill & Ruth. J. Greuel & Alastair. J. Wilson & Jocelyn. Poissant, 2024. "Methanogenic patterns in the gut microbiome are associated with survival in a population of feral horses," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Dong-Woo Lim & Jing-Hua Wang, 2022. "Gut Microbiome: The Interplay of an “Invisible Organ” with Herbal Medicine and Its Derived Compounds in Chronic Metabolic Disorders," IJERPH, MDPI, vol. 19(20), pages 1-16, October.
    13. Emmanuel Kazuva & Jiquan Zhang, 2019. "Analyzing Municipal Solid Waste Treatment Scenarios in Rapidly Urbanizing Cities in Developing Countries: The Case of Dar es Salaam, Tanzania," IJERPH, MDPI, vol. 16(11), pages 1-21, June.
    14. Qi Su & Qin Liu & Raphaela Iris Lau & Jingwan Zhang & Zhilu Xu & Yun Kit Yeoh & Thomas W. H. Leung & Whitney Tang & Lin Zhang & Jessie Q. Y. Liang & Yuk Kam Yau & Jiaying Zheng & Chengyu Liu & Mengjin, 2022. "Faecal microbiome-based machine learning for multi-class disease diagnosis," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    15. Paolo Montuori & Elvira De Rosa & Fabiana Di Duca & Donatella Paola Provvisiero & Pasquale Sarnacchiaro & Antonio Nardone & Maria Triassi, 2021. "Estimation of Polycyclic Aromatic Hydrocarbons Pollution in Mediterranean Sea from Volturno River, Southern Italy: Distribution, Risk Assessment and Loads," IJERPH, MDPI, vol. 18(4), pages 1-19, February.
    16. Babak Moeini & Erfan Ayubi & Majid Barati & Saeid Bashirian & Leili Tapak & Khadije Ezzati-Rastgar & Maryam Hashemian, 2023. "Effect of Household Interventions on Promoting Waste Segregation Behavior at Source: A Systematic Review," Sustainability, MDPI, vol. 15(24), pages 1-16, December.
    17. Alfredo Mazza & Prisco Piscitelli & Andrea Falco & Maria Lucia Santoro & Manuela Colangelo & Giovanni Imbriani & Adele Idolo & Antonella De Donno & Leopoldo Iannuzzi & Annamaria Colao, 2018. "Heavy Environmental Pressure in Campania and Other Italian Regions: A Short Review of Available Evidence," IJERPH, MDPI, vol. 15(1), pages 1-12, January.
    18. Alfredo Mazza & Prisco Piscitelli & Cosimo Neglia & Giulia Della Rosa & Leopoldo Iannuzzi, 2015. "Illegal Dumping of Toxic Waste and Its Effect on Human Health in Campania, Italy," IJERPH, MDPI, vol. 12(6), pages 1-14, June.
    19. M. McCauley & T. L. Goulet & C. R. Jackson & S. Loesgen, 2023. "Systematic review of cnidarian microbiomes reveals insights into the structure, specificity, and fidelity of marine associations," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    20. Pierre H. H. Schneeberger & Morgan Gueuning & Sophie Welsche & Eveline Hürlimann & Julian Dommann & Cécile Häberli & Jürg E. Frey & Somphou Sayasone & Jennifer Keiser, 2022. "Different gut microbial communities correlate with efficacy of albendazole-ivermectin against soil-transmitted helminthiases," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48739-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.