Compartment-specific microbial communities highlight the ecological roles of fungi in a subtropical seagrass...

Plant-associated compartments provide habitats for various microbes. Seagrasses are the only submerged marine angiosperms. However, the simultaneous investigation of fungi and prokaryotes inhabiting different seagrass-associated compartments is limited, and much remains to be learned about the functional roles of seagrass fungi. We examined the diversity, composition, and networks of fungal and prokaryotic communities in multiple compartments associated with the seagrass Halophila ovalis to shed light on the significance of fungi in the seagrass ecosystem. Seagrass compartments primarily differentiated the microbial communities. Notably, the root and rhizome tissues of visually healthy H. ovalis exhibited a very narrow, single-species dominated and enriched fungal spectrum, leading us to hypothesize the possible establishment of a symbiotic relationship between the Lulworthiaceae mycobiont, Halophilomyces hongkongensis, and the seagrass host. In addition, the Vibrionaceae family, represented by the genus Vibrio, emerged as the most abundant prokaryotic taxon enriched in the roots/rhizomes, showing exclusive positive correlations with H. hongkongensis within the tissues, implying a cross-kingdom reciprocal interaction between these taxa in the endosphere of H. ovalis. Fungal-prokaryotic interdomain network analysis identified H. hongkongensis as a keystone taxon, essential for coordinating microbial interactions in H. ovalis-associated compartments, while robustness analysis of interdomain networks suggested fungi plays a more crucial role in sustaining the network structures of H. ovalis inner tissues compared to surrounding compartments. These findings provide valuable insights into the seagrass-fungi relationship and emphasize the importance of fungi in the seagrass ecosystem.IMPORTANCEAlthough plant-associated microbes are key determinants of plant health, fitness, and stress resilience, microbial communities associated with seagrasses remain poorly understood compared to those in land plants, particularly concerning the diversity and ecological roles of their fungal associates. Our work provides a comprehensive assessment of fungal and prokaryotic communities across multiple above- and below-ground compartments associated with Halophila ovalis, the most widespread seagrass species in Hong Kong, through a year-round sampling. Our findings reveal compartment-specific patterns in diversity, network topology, and stability of microbial communities, highlighting the critical roles of fungi in seagrass-associated microbial networks and advancing our understanding of plant-fungal interactions in the marine environment.