Anaerobic consortia of fungi and sulfate reducing bacteria in deep granite fractures

Abstract

The deep biosphere is one of the least understood ecosystems on Earth. Although most microbiological studies in this system have focused on prokaryotes and neglected microeukaryotes, recent discoveries have revealed existence of fossil and active fungi in marine sediments and sub-seafloor basalts, with proposed importance for the subsurface energy cycle. However, studies of fungi in deep continental crystalline rocks are surprisingly few. Consequently, the characteristics and processes of fungi and fungus-prokaryote interactions in this vast environment remain enigmatic. Here we report the first findings of partly organically preserved and partly mineralized fungi at great depth in fractured crystalline rock (−740 m). Based on environmental parameters and mineralogy the fungi are interpreted as anaerobic. Synchrotron-based techniques and stable isotope microanalysis confirm a coupling between the fungi and sulfate reducing bacteria. The cryptoendolithic fungi have significantly weathered neighboring zeolite crystals and thus have implications for storage of toxic wastes using zeolite barriers.

A Cryptic Alternative for the Evolution of Hyphae

“…The last decade has witnessed the discovery of a fungal fossil record in deep igneous rocks, both in the oceanic and the continental crust. [ 41–43 ] Most of the fungal fossils consist of hyphae propagating from mineral surfaces into the open pore space of fractures and vugs where they form complex mycelium‐like networks. [ 18,44 ] Additional to hyphae, yeast‐like growth stages and reproductive organs like sporophores, spores and spore sacs have been described.…”

“…[ 52,53,54 ] In continental crystalline basement fungal fossils ranging back to Devonian age (≈400 Ma) have been described from various sites in the Swedish igneous basement. [ 43,55–58 ] Thus, hyphal fungi were present at great depths in the oceanic and continental crust contemporaneous with the presumed evolution of hyphae as plants and fungi colonized the terrestrial realm. [ 18,57 ]…”

“…However, this does not seem to be the entire explanation because endolithic fungal colonization starts from a biofilm laid down on the fracture walls from which the hyphae grow out in the open pore space. [ 18,43,44,60,61 ] The dominant function of hyphae among the endolithic fungi seems to be to conquer the open pore space rather than attachment. Numerous samples from the oceanic crust show how fungal hyphae fill the entire pore space by forming a three‐dimensional network ( Figure 2a–c).…”

High Diversity in Iron Cycling Microbial Communities in Acidic, Iron-Rich Water of the Pyhäsalmi Mine, Finland

“…Fungi are generally found in various environments covering a wide pH range from at least pH 1 to pH 11 [47]. They have, for example, been found in deep terrestrial bedrock environments [48][49][50][51], in the deep (2 km below land surface) boreholes of the Pyhäsalmi mine [32], in the extremely acidic and metal-rich Rio Tinto [8], and other AMD-affected streams [9][10][11]52]. A striking feature of the fungal communities in the extremely acidic environments is their high diversity, which was also detected in the present study, although Baker et al [52] reported a low number of eukaryotic species in extremely acidic (pH < 0 9) runoff in the Richmond underground mine (USA).…”

A New Frontier for Palaeobiology: Earth's Vast Deep Biosphere

“…Open pores and fractures in rocks and sediments are ubiquitously encrusted and occluded over time by the progressive development of calcite, quartz/chalcedony, clays, zeolites, sulfides, and other mineral cements; it would be surprising if this process did not also coat, entomb, and replace microbial remains in the deep biosphere. Indeed, a recent study of 740‐m‐deep granitic drill core provided a snapshot of this phenomenon in action; degraded fracture‐dwelling filaments and purported colonies (interpreted as fungi and bacteria, probably ancient) were found to be incipiently mineralized but largely still organic in composition . Moreover, many micro‐organisms themselves deposit minerals and can thereby “auto‐fossilize.”…”