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Gut microbiota produces biofilm-associated amyloids with potential for neurodegeneration

Author

Listed:
  • Ariadna Fernández-Calvet

    (Instituto de Agrobiotecnología (IDAB). CSIC-Gobierno de Navarra)

  • Leticia Matilla-Cuenca

    (Instituto de Agrobiotecnología (IDAB). CSIC-Gobierno de Navarra)

  • María Izco

    (Center for Biomedical Research of La Rioja)

  • Susanna Navarro

    (Universitat Autónoma de Barcelona)

  • Miriam Serrano

    (Instituto de Agrobiotecnología (IDAB). CSIC-Gobierno de Navarra)

  • Salvador Ventura

    (Universitat Autónoma de Barcelona)

  • Javier Blesa

    (Hospital Universitario HM Puerta del Sur, HM Hospitales
    HM Hospitales)

  • Maite Herráiz

    (University of Navarra
    Instituto de Investigación Sanitaria de Navarra)

  • Gorka Alkorta-Aranburu

    (Instituto de Investigación Sanitaria de Navarra
    University of Navarra)

  • Sergio Galera

    (Government of Navarra)

  • Igor Ruiz de los Mozos

    (Government of Navarra)

  • María Luisa Mansego

    (Navarrabiomed, Complejo Hospitalario de Navarra (CHN), Universidad Pública de Navarra (UPNA), IdiSNA)

  • Alejandro Toledo-Arana

    (Instituto de Agrobiotecnología (IDAB). CSIC-Gobierno de Navarra)

  • Lydia Alvarez-Erviti

    (Center for Biomedical Research of La Rioja)

  • Jaione Valle

    (Instituto de Agrobiotecnología (IDAB). CSIC-Gobierno de Navarra)

Abstract

Age-related neurodegenerative diseases involving amyloid aggregation remain one of the biggest challenges of modern medicine. Alterations in the gastrointestinal microbiome play an active role in the aetiology of neurological disorders. Here, we dissect the amyloidogenic properties of biofilm-associated proteins (BAPs) of the gut microbiota and their implications for synucleinopathies. We demonstrate that BAPs are naturally assembled as amyloid-like fibrils in insoluble fractions isolated from the human gut microbiota. We show that BAP genes are part of the accessory genomes, revealing microbiome variability. Remarkably, the abundance of certain BAP genes in the gut microbiome is correlated with Parkinson’s disease (PD) incidence. Using cultured dopaminergic neurons and Caenorhabditis elegans models, we report that BAP-derived amyloids induce α-synuclein aggregation. Our results show that the chaperone-mediated autophagy is compromised by BAP amyloids. Indeed, inoculation of BAP fibrils into the brains of wild-type mice promote key pathological features of PD. Therefore, our findings establish the use of BAP amyloids as potential targets and biomarkers of α-synucleinopathies.

Suggested Citation

  • Ariadna Fernández-Calvet & Leticia Matilla-Cuenca & María Izco & Susanna Navarro & Miriam Serrano & Salvador Ventura & Javier Blesa & Maite Herráiz & Gorka Alkorta-Aranburu & Sergio Galera & Igor Ruiz, 2024. "Gut microbiota produces biofilm-associated amyloids with potential for neurodegeneration," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48309-x
    DOI: 10.1038/s41467-024-48309-x
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