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, 75 (20), 6415-21

Fungal Diversity in Deep-Sea Hydrothermal Ecosystems

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Fungal Diversity in Deep-Sea Hydrothermal Ecosystems

Thomas Le Calvez et al. Appl Environ Microbiol.

Abstract

Deep-sea hydrothermal ecosystems are considered oases of life in oceans. Since the discovery of these ecosystems in the late 1970s, many endemic species of Bacteria, Archaea, and other organisms, such as annelids and crabs, have been described. Considerable knowledge has been acquired about the diversity of (micro)organisms in these ecosystems, but the diversity of fungi has not been studied to date. These organisms are considered key organisms in terrestrial ecosystems because of their ecological functions and especially their ability to degrade organic matter. The lack of knowledge about them in the sea reflects the widely held belief that fungi are terrestrial organisms. The first inventory of such organisms in deep-sea hydrothermal environments was obtained in this study. Fungal diversity was investigated by analyzing the small-subunit rRNA gene sequences amplified by culture-independent PCR using DNA extracts from hydrothermal samples and from a culture collection that was established. Our work revealed an unsuspected diversity of species in three of the five fungal phyla. We found a new branch of Chytridiomycota forming an ancient evolutionary lineage. Many of the species identified are unknown, even at higher taxonomic levels in the Chytridiomycota, Ascomycota, and Basidiomycota. This work opens the way to new studies of the diversity, ecology, and physiology of fungi in oceans and might stimulate new prospecting for biomolecules. From an evolutionary point of view, the diversification of fungi in the oceans can no longer be ignored.

Figures

FIG. 1.
FIG. 1.
Phylogenetic positions of deep-sea hydrothermal fungi. This consensus tree includes environmental SSU rRNA sequences isolated from environmental ecosystems (phylotypes 1 to 9) and isolated cultures from the same samples (phylotypes 10 to 20), along with the closest known related SSU rRNA fungal sequences. The tree was constructed using the neighbor-joining algorithm. Bootstrap values of >50% are indicated at the nodes (estimated using 1,000, 500, and 50 iterations for the neighbor-joining [NJ], maximum parsimony [MP], and maximum likelihood [ML] analyses, respectively). Stars indicate the phylotypes considered new phylotypes. The scale bar indicates 0.1 change per position computed using the NJ-K2P model. The dotted lines indicate branches not recovered in all three analyses. Designations that begin with MV followed by a hyphen indicate isolates from MARVEL cruise samples (Mid-Atlantic Ridge), and designations that begin with HE followed by a hyphen indicate isolates from “HERO” cruise samples (East Pacific Rise) (Table 1). The cultures obtained from sample MV2E1 are MV-1c to MV-4c, MV-21c, MV-23c, MV-FS1c, and MV-FS3c; the cultures obtained from sample MV2E2 are MV-8c, MV-10c, MV-25c, and MV-FS4c; the cultures obtained from sample MV2E3 are MV-15c, MV-19c, MV-26c, and MV-27c; the culture obtained from sample H18E9 is HE-5c; the cultures obtained from sample H18E11 are HE-1c to HE-3c; and the culture obtained from sample H18E12 is HE-4c. In the Ascomycota, the terminal HE-1c and HE-3c cultures were not defined as new phylotypes since their phylogenetic affinities were unclear.
FIG. 2.
FIG. 2.
Estimates of fungal community diversity as a function of sampling effort for environmental samples. Rarefaction curves were computed using 100 bootstrap replicates (upper line), and the expected richness function (lower line) is the number of phylotypes estimated (random sampling without replacement) from our sequence data set generated using ciPCRs. (A) MV2E2; (B) H18E12; (C) MV2E1; (D) MV2E3. Plots for MV5E1 and MV5E2 were not drawn since only one phylotype was found in each sample when sequence analyses of the ciPCR products obtained using primers MH2 and MH4 were performed.

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