Recent discoveries highlighted pelagic fungi as significant contributors to the recycling of organic matter in the ocean. However, whether the environmental clustering/differentiation observed in the functional role of other pelagic microbes also applies to pelagic fungi remains unknown. In this study, we employed multi-omics approaches, including metagenomics and metatranscriptomics, to explore the fungal functional diversity, biogeography, and activity in the ocean. Our research focused on the role of fungi as metabolic degraders of organic matter, investigating both surface and deep chlorophyll maximum layers. This high-resolution spatial analysis covered a broad range of environments, from subtropical to polar regions in the open Atlantic and Southern Ocean, and differentiating between small (0.2–3 µm, SF) and large (>3 µm, LF) size fraction communities. Fungi constituted 1 - 2% of total eukaryotic genes and transcripts in metagenomes and metatranscriptomes. In contrast, fungi were assigned to > 3% of the eukaryotic CAZyme transcripts (but only 0.16% for proteases), indicating a preferential role of pelagic fungi in carbohydrate degradation. Our analysis revealed distinct ecological niches and resource partitioning between polar and non-polar oceans, with CAZymes more abundant in non-polar regions and peptidases dominating polar waters. Additionally, in non-polar regions, fungal groups exhibited distinct size fraction preferences, underscoring the importance of size fractionation in understanding their ecological roles. Collectively, this study highlights significant shifts in the functional diversity and taxonomic affiliation of fungal CAZymes and peptidases across polar and non-polar waters, revealing the distinct biogeography of pelagic fungi in organic matter degradation.

Oceanic fungi,CAZymes,peptidases,metagenomic,metatranscriptomic,non-polar and polar oceans