Expanded genetic and functional diversity of oceanic fungi.

Background: Fungi are known members of marine microbiomes that can act as saprotrophs, parasites, and pathogens. Although a few studies utilizing cultivation-based methods and metabarcoding have been conducted, the diversity, ecological roles, and functional activities of fungi in the open ocean remain vastly underexplored. This gap in knowledge is particularly notable in oxygen minimum zones (OMZ) of the ocean, which have expanded over the past 50 years, affecting marine ecosystems and biogeochemical cycles. The eastern tropical North Pacific Ocean (ETNP) is the largest oxygen minimum zone where fungi have been implicated in the production of the potent greenhouse gas nitrous oxide. Nevertheless, anaerobic metabolisms have rarely been investigated for fungi within the oxygen-depleted water columns of the ocean.

Results: We report previously unrecognized diversity and activity of fungi in the ETNP OMZ. Phylogenetic analysis based on ribosomal proteins and carbohydrate-active enzyme (CAZyme) gene families revealed that oceanic fungi form distinct evolutionary clades that diverge from their terrestrial counterparts, challenging earlier models of multiple, intermingled marine-terrestrial transitions. Despite comprising a very low percentage of the total DNA and RNA pool, fungi accounted for a disproportionate share of extracellular CAZyme expression, with glycoside hydrolase family 7 (GH7) emerging as the dominant enzyme. The high expression of fungal GH7 genes suggests a specialized role fungi play in particle degradation, potentially acting on cellulose derived from dinoflagellates and pelagic tunicates, as well as chitosan derived from bacterial deacetylation of chitin. The strong correlation between the gene expression of fungal GH7 and bacterial chitin deacetylase suggests a potential synergy between bacteria and fungi in the degradation of chitin. Moreover, the correlation between dissimilatory nitrogen cycling processes and fungal hydrolytic activities provides new evidence for fungi as key players in linking carbon remineralization and nitrogen cycling in oxygen minimum zones.

Conclusions: Our results point to fungi as pivotal contributors to particle remineralization in the ocean, potentially modulating the coupled cycles of carbon and nitrogen in OMZs. Integrating these fungal processes into marine ecosystem models may therefore be essential for improving our understanding of global biogeochemical dynamics and predicting responses to ocean deoxygenation. Video Abstract.