Psychrophilic pucciniomycotinous yeasts inhabit snowfields and glacial ecosystems worldwide, yet their ecological role remains unclear. We isolated a clonal strain of Phenoliferia psychrophenolica (LCC-F-001-001) from an alpine red snowfield. Its 42-Mbp genome contains 11,523 genes, including 37 ice-binding protein genes, the highest number recorded in fungi, mainly acquired through horizontal transfers. This yeast tolerates freezing, grows optimally at 10 °C and forms pseudohyphae above 15 °C. Known to assimilate phenol and small metabolites, we found LCC-F-001-001 also hydrolyzes carotenoid and phenolic pigments from snow and glacier ice algae. LCC-F-001-001 genome encodes ~ 500 carbohydrate-active enzymes, ranking among the most catalytically versatile sequenced Microbotryomycetes, alongside a related permafrost species. P. psychrophenolica and related fungi are therefore key players in snow and ice ecosystems, capable of degrading organic molecules in snowfields and glaciers, likely during algal bloom declines, and connecting the carbon cycle between cryospheric environments and soils through their exceptional metabolic adaptability.

Architecture et Fonction des Macromolécules Biologiques UMR 7257 Centre National de la Recherche Scientifique Aix Marseille Univ USC 1408 Institut National de Recherche pour l'Agriculture l'Alimentation et l'Environnement Marseille France

Biodiversité et Biotechnologie Fongique UMR1163 Institut National de Recherche pour l'Agriculture l'Alimentation et l'Environnement Aix Marseille Univ Marseille France

Department of Ecology Faculty of Science Charles University Prague Czech Republic

Department of Environment and Biodiversity University of Salzburg Salzburg Austria

Jardin du Lautaret Université Grenoble Alpes Centre National de la Recherche Scientifique; 2233 rue de la piscine Domaine Universitaire Gières France

Laboratoire de Physiologie Cellulaire et Végétale Centre National de la Recherche Scientifique Institut National de Recherche pour l'Agriculture l'Alimentation et l'Environnement Commissariat à l'Energie Atomique et aux Energies Alternatives Université Grenoble Alpes; IRIG CEA Grenoble Grenoble France

Sequentia Biotech SL Barcelona Spain

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