A Fungal-Prokaryotic Consortium at the Basalt-Zeolite Interface in Subseafloor Igneous Crust

Abstract

We have after half a century of coordinated scientific drilling gained insight into Earth´s largest microbial habitat, the subseafloor igneous crust, but still lack substantial understanding regarding its abundance, diversity and ecology. Here we describe a fossilized microbial consortium of prokaryotes and fungi at the basalt-zeolite interface of fractured subseafloor basalts from a depth of 240 m below seafloor (mbsf). The microbial consortium and its relationship with the surrounding physical environment are revealed by synchrotron-based X-ray tomographic microscopy (SRXTM), environmental scanning electron microscopy (ESEM), and Raman spectroscopy. The base of the consortium is represented by microstromatolites—remains of bacterial communities that oxidized reduced iron directly from the basalt. The microstromatolites and the surrounding basalt were overlaid by fungal cells and hyphae. The consortium was overgrown by hydrothermally formed zeolites but remained alive and active during this event. After its formation, fungal hyphae bored in the zeolite, producing millimetre-long tunnels through the mineral substrate. The dissolution could either serve to extract metals like Ca, Na and K essential for fungal growth and metabolism, or be a response to environmental stress owing to the mineral overgrowth. Our results show how microbial life may be maintained in a nutrient-poor and extreme environment by close ecological interplay and reveal an effective strategy for nutrient extraction from minerals. The prokaryotic portion of the consortium served as a carbon source for the eukaryotic portion. Such an approach may be a prerequisite for prokaryotic-eukaryotic colonisation of, and persistence in, subseafloor igneous crust.

Authigenic Mineral Texture in Submarine 1979 Basalt Drill Core, Surtsey Volcano, Iceland

“…The dissolution mechanism(s) remain unclear. Elemental carbon concentrations outline cavity perimeters and Raman spectra indicate poorly ordered carbonaceous matter (Figures c and a), similar to that which is used as an indicator for the biological origin of putative fossilized structures (Bower et al, ; Ivarsson et al, ).…”

Colonization, penetration and transformation of manganese oxide nodules by Aspergillus niger

“…The results extend the understanding of the possible interactions between fungi and manganese‐containing mineral substrates that are widespread in the biosphere, although the significance of such transformations in the natural manganese nodule deep sea environment is a matter for conjecture. Nevertheless, future work on the deep sea microbial consortia colonizing such substrates may reveal hitherto undiscovered geomicrobial processes as has been the case for other deep subsurface locations (Ivarsson et al ., , ,b). Our findings may also have practical significance for future mineral bioprocessing applications using fungi, with additional relevance to environmental processes involving chemoorganotrophic microorganisms and manganese minerals.…”

“…Biomineralized hyphae are frequently observed in deep sub‐surface locations (Reitner et al ., ) and as well as penetration of carbonates and zeolites (Bengtson et al ., ; Ivarsson et al ., ). Fungi can also be associated with manganese oxides both in terms of formation through Mn(II) oxidation to Mn(IV) (Ivarsson et al ., ) or properties of Mn(IV) dissolution (Wei et al ., ).…”

Ecology, adaptation, and function of methane‐sulfidic spring water biofilm microorganisms, including a strain of anaerobic fungus Mucor hiemalis

“…Abundant Archaea were connected with each other by EPS structures to form Chains of Pearls in association with fungal hyphae (Figure ). Similarly, a fungal‐prokaryotic consortium was detected in the subseafloor igneous crust at the basal–zeolite interface (Ivarsson et al., ). Bengtson et al.…”