Community structure and hidden phylogenetic diversity of marine fungi in the tropical Indian and western Pacific Oceans

Background Marine fungi remain a poorly understood component of ocean ecosystems despite their potential roles in marine biogeochemical cycling. Here, we investigated fungal diversity, community structure, vertical stratification, and environmental drivers across the tropical Indian and western Pacific Oceans using long-read 28S rRNA gene amplicon sequencing of 113 samples from surface waters, mesopelagic and bathypelagic zones, and sediments. Results A total of 46,938 fungal OTUs were clustered, representing 35 phyla, 164 classes, 254 orders, 509 families, 940 genera, and 1,055 species. Ascomycota dominated fungal communities, followed by Basidiomycota, Chytridiomycota, Rozellomycota. Phylogenetic analyses revealed three deeply divergent fungal lineages distinct from currently recognized phyla. Pending further molecular and morphological validation, these lineages were provisionally designated as Candidate.Taichumycota, Candidate.Shizhenmycota, and Candidate.Xihemycota. Their distinct vertical stratification suggested potential ecological differentiation: Candidate.Taichumycota was restricted to surface waters, Candidate.Shizhenmycota was broadly distributed but enriched in surface communities, whereas Candidate.Xihemycota occurred across habitats and was particularly enriched in sediments. Both fungal taxonomic and functional compositions exhibited significant vertical differentiation across habitats ( p < 0.05), with undefined saprotrophic guilds enriched in sediments and pelagic communities displaying diverse trophic strategies. Surface fungal community composition was jointly shaped by geographic and environmental gradients, with longitude, phosphate, and salinity identified as major predictors. Together, these variables explained 18.6% of the variation in surface fungal community composition. Conclusions This study reveals extensive hidden diversity and complex ecological structuring of marine fungi in the tropical Indian and western Pacific Oceans. The discovery of deeply divergent fungal lineages and habitat-associated shifts in taxonomic and predicted functional composition highlights the underestimated evolutionary diversity and ecological differentiation of marine fungal communities.