Fungal Diversity in Deep-Sea Hydrothermal Ecosystems

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.Since the discovery of hydrothermal vent ecosystems 30 years ago, unexpected species diversity has been revealed that has shed light on the functional coupling between the geosphere and the biosphere. When submersibles dive to the seafloor, they bring numerous organisms back to the surface, and this has resulted in the description of nearly two new species per month (10). Deep-sea hydrothermal ecosystems are considered hotspots of microbial diversity on the seafloor. Indeed, they are ecosystems that produce biomass using the wide range of chemical compounds released by the polymetallic sulfite chimneys or "black smokers" that represent the huge quantity of chemical energy that is available (26). The vent fluid, having been heated close to a magma chamber, can have a temperature of 400°C when it is emitted. It is also characterized by a lack of dissolved oxygen, strong acidity (pH 2 to 3), a high concentration of electron donors (i.e., reduced compounds such as methane and hydrogen sulfide), and the presence of heavy metals (36). Continual mixing with the cold ocean water (2 to 4°C) that is rich in electron acceptors creates a dynamic chemical disequilibrium that is a source of energy for microorganisms that control the rates of redox reactions (16).Each ridge displays varied geochemistry, and the vent fluids differ, even at scales as small as the fractures, pipes, and porosities in the black smokers, creating diverse microhabitats for biota (10,

Ecological succession reveals potential signatures of marine–terrestrial transition in salt marsh fungal communities

“…As such, it is tempting to speculate that the majority of the novel unidentified sequences belong to fungal lineages that are potentially affiliated to an early radiation of the Dikaria clade, close to the chytrid branches (Richards et al, 2012) and/or to yeast-like basal fungal lineages. These arguments collectively corroborate previous studies that have suggested that coastal environments host diverse as-yet-unclassified fungal lineages that may be typical for the (ancient) transition from marine to terrestrial systems (Le Calvez et al, 2009;Mohamed and Martiny, 2011). As succession proceeds to the more mature terrestrial stages, the fungal communities apparently evolved towards a dominance of filamentous and, to a larger extent, saprotrophic fungi, as their mode of exploration for nutrients is fine tuned to the utilization of complex substrates such as the organic matter derived from plant biomass (Richards et al, 2012;Treseder and Lennon, 2015).…”

Living strategy of cold-adapted fungi with the reference to several representative species

“…Fungi isolated from deep seas were first reported nearly 50 years ago (Roth et al 1964), then a great number of fungi including some novel species have been published by both conventional culture-dependent (Raghukumar et al 2004; Gadanho and Sampaio 2005; Damare et al 2006; Nagahama et al 2006; Le Calvez et al 2009; Singh et al 2010) and culture-independent methods (Lai et al 2007; Le Calvez et al 2009; Nagano et al 2010). Le Calvez et al (2009) reported striking differences in their comparison of deep-sea fungal diversity assessed by culture-dependent and culture-independent methods.…”

“…Le Calvez et al (2009) reported striking differences in their comparison of deep-sea fungal diversity assessed by culture-dependent and culture-independent methods. Generally, ascomycetes can be frequently and easily isolated in deep-sea environments, but chytrids and other basal fungi may be missed because many chytrids can not be isolated on solid growth media, especially those to which chloramphenicol has been added (Gleason and Marano 2011).…”

Temporal variation of the small eukaryotic community in two freshwater lakes: emphasis on zoosporic fungi

“…Recent applications of molecular approaches to characterize eukaryotic communities have revealed that zoosporic fungi significantly contribute to the eukaryotic diversity in a range of ecosystems, such as high-elevation soils (Freeman et al 2009), deep-sea hydrothermal ecosystems (Le Calvez et al 2009, Nagahama et al 2011, and streams (Nikolcheva & Bär-locher 2004, Seena et al 2008. In freshwater lakes, ABSTRACT: Applications of molecular approaches to the study of microbial eukaryotic communities in freshwater lakes are transforming our understanding of these ecosystems.…”