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Global Diversity and Biogeography of the Zostera marina Mycobiome.

ABSTRACT: Seagrasses are marine flowering plants that provide critical ecosystem services in coastal environments worldwide. Marine fungi are often overlooked in microbiome and seagrass studies, despite terrestrial fungi having critical functional roles as decomposers, pathogens, or endophytes in global ecosystems. Here, we characterize the distribution of fungi associated with the seagrass Zostera marina, using leaves, roots, and rhizosphere sediment from 16 locations across its full biogeographic range. Using high-throughput sequencing of the ribosomal internal transcribed spacer (ITS) region and 18S rRNA gene, we first measured fungal community composition and diversity. We then tested hypotheses of neutral community assembly theory and the degree to which deviations suggested that amplicon sequence variants (ASVs) were plant selected or dispersal limited. Finally, we identified a core mycobiome and investigated the global distribution of differentially abundant ASVs. We found that the fungal community is significantly different between sites and that the leaf mycobiome follows a weak but significant pattern of distance decay in the Pacific Ocean. Generally, there was evidence for both deterministic and stochastic factors contributing to community assembly of the mycobiome, with most taxa assembling through stochastic processes. The Z. marina core leaf and root mycobiomes were dominated by unclassified Sordariomycetes spp., unclassified Chytridiomycota lineages (including Lobulomycetaceae spp.), unclassified Capnodiales spp., and Saccharomyces sp. It is clear from the many unclassified fungal ASVs and fungal functional guilds that knowledge of marine fungi is still rudimentary. Further studies characterizing seagrass-associated fungi are needed to understand the roles of these microorganisms generally and when associated with seagrasses. IMPORTANCE Fungi have important functional roles when associated with land plants, yet very little is known about the roles of fungi associated with marine plants, like seagrasses. In this study, we report the results of a global effort to characterize the fungi associated with the seagrass Zostera marina across its full biogeographic range. Although we defined a putative global core fungal community, it is apparent from the many fungal sequences and predicted functional guilds that had no matches to existing databases that general knowledge of seagrass-associated fungi and marine fungi is lacking. This work serves as an important foundational step toward future work investigating the functional ramifications of fungi in the marine ecosystem.

SUBMITTER: Ettinger CL

PROVIDER: S-EPMC8174750 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Seagrasses are globally distributed marine flowering plants that are foundation species in coastal ecosystems. Seagrass beds play essential roles as habitats and hatcheries, in nutrient cycling, and in protecting the coastline from erosion. Although many studies have focused on seagrass ecology, only a limited number have investigated their associated fungi. In terrestrial systems, fungi can have beneficial and detrimental effects on plant fitness. However, not much is known about marine fungi and even less is known about seagrass associated fungi. Here we used culture-independent sequencing of the ribosomal internal transcribed spacer (ITS) region to characterize the taxonomic diversity of fungi associated with the seagrass, Zostera marina. We sampled from two Z. marina beds in Bodega Bay over three time points to investigate fungal diversity within and between plants. Our results indicate that there are many fungal taxa for which a taxonomic assignment cannot be made living on and inside Z. marina leaves, roots and rhizomes and that these plant tissues harbor distinct fungal communities. We also identified differences in the abundances of the orders, Glomerellales, Agaricales and Malasseziales, between seagrass tissues. The most prevalent ITS amplicon sequence variants (ASVs) associated with Z. marina tissues could not initially be confidently assigned to a fungal phylum, but shared significant sequence similarity with Chytridiomycota and Aphelidomycota. To obtain a more definitive taxonomic classification of the most abundant ASV associated with Z. marina leaves, we used PCR with one primer targeting a unique region of this ASV's ITS2 and a second primer targeting fungal 28S rRNA genes to amplify part of the 28S rRNA gene region corresponding to this ASV. Sequencing and phylogenetic analysis of the resulting partial 28S rRNA gene revealed that the organism that this ASV comes from is a member of Novel Clade SW-I in the order Lobulomycetales in the phylum Chytridiomycota. This clade includes known parasites of freshwater diatoms and algae and it is possible this chytrid is directly infecting Z. marina leaf tissues. This work highlights a need for further studies focusing on marine fungi and the potential importance of these understudied communities to the larger seagrass ecosystem.

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Global Diversity and Biogeography of the Zostera marina Mycobiome.

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