The fungal kingdom is replete with unique adaptive capacities that allow fungi to colonize a wide variety of habitats, ranging from marine habitats to freshwater and terrestrial habitats. The diversity, importance, and ecological roles of marine fungi have recently been highlighted in deep-subsurface sediments using molecular methods. Fungi in the deep-marine subsurface may be specifically adapted to life in the deep biosphere, but this can be demonstrated only using culture-based analyses. In this study, we investigated culturable fungal communities from a record-depth sediment core sampled from the Canterbury Basin (New Zealand) with the aim to reveal endemic or ubiquist adapted isolates playing a significant ecological role(s). About 200 filamentous fungi (68%) and yeasts (32%) were isolated. Fungal isolates were affiliated with the phyla Ascomycota and Basidiomycota, including 21 genera. Screening for genes involved in secondary metabolite synthesis also revealed their bioactive compound synthesis potential. Our results provide evidence that deep-subsurface fungal communities are able to survive, adapt, grow, and interact with other microbial communities and highlight that the deep-sediment habitat is another ecological niche for fungi.

The subsurface realm is colonized by microbial communities to depths of 41000 meters below the seafloor (m.b.sf.), but little is known about overall diversity and microbial distribution patterns at the most profound depths. Here we show that not only Bacteria and Archaea but also Eukarya occur at record depths in the subseafloor of the Canterbury Basin. Shifts in microbial community composition along a core of nearly 2 km reflect vertical taxa zonation influenced by sediment depth. Representatives of some microbial taxa were also cultivated using methods mimicking in situ conditions. These results suggest that diverse microorganisms persist down to 1922 m.b.sf. in the seafloor of the Canterbury Basin and extend the previously known depth limits of microbial evidence (i) from 159 to 1740 m.b.sf. for Eukarya and (ii) from 518 to 1922 m.b.sf. for Bacteria.

The deep subseafloor, extending from a few centimeters below the sediment surface to several hundred meters into sedimentary deposits, constitutes the deep biosphere and harbors an unexpected microbial diversity. Several studies have described the occurrence, turnover, activity and function of subseafloor prokaryotes; however, subsurface eukaryotic communities still remain largely underexplored. Ribosomal RNA surveys of superficial and near-surface marine sediments have revealed an unexpected diversity of active eukaryotic communities, but knowledge of the diversity of deep subseafloor microeukaryotes is still scarce. Here, we investigated the vertical distribution of DNA and RNA fungal signatures within subseafloor sediments of the Canterbury basin (New Zealand) by 454 pyrotag sequencing of fungal genetic markers. Different shifts between the fungal classes of Tremellomycetes, Sordariomycetes, Eurotiomycetes, Saccharomycetes, Wallemiomycetes, Dothideomycetes, Exobasidiomycetes and Microbotryomycetes were observed. These data provide direct evidence that fungal communities occur at record depths in deep sediments of the Canterbury basin and extend the depth limit of fungal presence and activity, respectively 1740 and 346 mbsf. As most of the fungal sequences retrieved have a cosmopolitan distribution, it indicates that fungi are able to adapt to the deep subseafloor conditions at record-depth and must play important ecological roles in biogeochemical cycles.

The deep sedimentary biosphere, extending 100s of meters below the seafloor harbors unexpected diversity of Bacteria, Archaea, and microbial eukaryotes. Far less is known about microbial eukaryotes in subsurface habitats, albeit several studies have indicated that fungi dominate microbial eukaryotic communities and fungal molecular signatures (of both yeasts and filamentous forms) have been detected in samples as deep as 1740 mbsf. Here, we compare and contrast fungal ribosomal RNA gene signatures and whole community metatranscriptomes present in sediment core samples from 6 and 95 mbsf from Peru Margin site 1229A and from samples from 12 and 345 mbsf from Canterbury Basin site U1352. The metatranscriptome analyses reveal higher relative expression of amino acid and peptide transporters in the less nutrient rich Canterbury Basin sediments compared to the nutrient rich Peru Margin, and higher expression of motility genes in the Peru Margin samples. Higher expression of genes associated with metals transporters and antibiotic resistance and production was detected in Canterbury Basin sediments. A poly-A focused metatranscriptome produced for the Canterbury Basin sample from 345 mbsf provides further evidence for active fungal communities in the subsurface in the form of fungal-associated transcripts for metabolic and cellular processes, cell and membrane functions, and catalytic activities. Fungal communities at comparable depths at the two geographically separated locations appear dominated by distinct taxa. Differences in taxonomic composition and expression of genes associated with particular metabolic activities may be a function of sediment organic content as well as oceanic province. Microscopic analysis of Canterbury Basin sediment samples from 4 and 403 mbsf produced visualizations of septate fungal filaments, branching fungi, conidiogenesis, and spores. These images provide another important line of evidence supporting the occurrence and activity of fungi in the deep subseafloor biosphere.

Fungi are known to play key roles in ecologically important biogeochemical cycles and food webs. Most knowledge of environmental groups of fungi comes from terrestrial environments, and little is known about the potential for terrestrial fungi to colonize marine environments. We investigated the Delaware River estuary and bay as a model estuarine system to study the fungal community changes occurring along a transect from terrestrially influenced waters and sediments to a higher salinity, truly marine system. DNA-based clone libraries and a culture collection built using subseafloor sediment samples revealed that Ascomycota dominated the detected diversity ahead of Basidiomycota and Chytridiomycota. A clear transition in fungal communities from terrestrially influenced and low salinity environments to marine environments was visualized. A complementary RNA-based analysis coupled with fluorescence in situ hybridization of sediments indicated that only few fungi were metabolically active in marine sediments. Cultivation of pelagic and sedimentary fungi allowed clear identification and physiology testing of fungal communities of the Delaware Bay. Most isolates were affiliated to Ascomycota and Basidiomycota, and their growth was analyzed under different concentrations of salinity to test for habitat preference and degree of adaptability. Interestingly, most of the fungi isolated were halotolerant. The present study informs us on the source and fate of fungi that may be buried in the deep marine subsurface and is informative for future investigations of this environment.

Cadophora malorum Mo12 was isolated from the Rainbow hydrothermal site on the Mid-Atlantic Ridge. We present the draft genome sequence of this filamentous fungal strain, which has high biotechnological potentials as revealed by the presence of genes encoding biotechnologically important enzymes and genes involved in the synthesis of secondary metabolites.

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