Biofilms inactivate the free-living stage of Batrachochytrium dendrobatidis, the most destructive pathogen for vertebrate diversity

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Sentenac, Hugo | Schmeller, Dirk, S | Caubet, Solène | Carsin, Adélaïde | Guillet, Rémi | Ferriol, Jessica | Leflaive, Joséphine | Loyau, Adeline

Edité par CCSD ; Nature Publishing Group -

Data availability statement: Data and all codes (field and laboratory studies) for this paper are available on the Figshare repository at https://10.6084/m9.figshare.252367512. Biofilm sequence read data are archived in the European Nucleotide Archive (ENA) of the European Bioinformatics Institute (EBML-EBI) under the accession numbers PRJEB64636 (prokaryotes) and PRJEB65851 (eukaryotes). The sequence of the isolate Bd GPL IA043 was deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under the accession number PRJNA413876 (BioSample: SAMN07773623; Sample name: IA043_cryo; SRA: SRS2757170).Ethical statements: Basic rules of biosecurity were applied under all circumstances in the field and the laboratory to avoid pathogen pollution. During fieldwork, a unique pair of gloves was used for each individual or each set of tadpoles (from a same lake), and footwear as well as all equipment in contact with water or amphibians were disinfected by spraying Virkon, away from water bodies, between each lake. Permits for capture were granted by the Direction Régionale de l'Environnement, de l’Aménagement et du Logement (DREAL) of regions Occitanie (permit 2017-s-33, 2017-s-33-m1, 161338295000) and Nouvelle-Aquitaine (permit 51-2021 DBEC), by the Parc National des Pyrénées (permits 2016-110, 2016-111, 2022-169), and the Instituto Aragonés de Gestión Ambiental (permit 500201/24/2021/01870).. International audience. Emerging infectious diseases threaten biodiversity and human health. Many emerging pathogens have aquatic life stages and all immersed substrates have biofilms on their surface, i.e., communities of microorganisms producing a gelatinous matrix. However, the outcome of the interactions between environmental biofilms and pathogens is poorly understood. Here we demonstrate that biofilms reduce the survival of the most impactful pathogen for vertebrate diversity, the invasive chytrid fungus Batrachochytrium dendrobatidis. Effects on its zoospores varied with biofilm composition in controlled settings and biofilm compositional variation also coincided with divergent impacts of chytridiomycosis on amphibian populations in nature. Our results suggest that biofilms form a biotic component of ecosystem resistance to Batrachochytrium dendrobatidis by reducing environmental transmission, and that they could be used to develop nature-based technologies to limit the impacts and spread of this invasive chytrid fungus. Our study warrants further research into the interactions between environmental biofilms and pathogenic and/or invasive micro-organisms.

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