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S43247-021-00107-9.Pdf ARTICLE https://doi.org/10.1038/s43247-021-00107-9 OPEN Fossilized anaerobic and possibly methanogenesis- fueling fungi identified deep within the Siljan impact structure, Sweden ✉ Henrik Drake 1 , Magnus Ivarsson2, Christine Heim 3,4, Oona Snoeyenbos-West2, Stefan Bengtson 2, Veneta Belivanova2 & Martin Whitehouse 2 Recent discoveries of extant and fossilized communities indicate that eukaryotes, including fungi, inhabit energy-poor and anoxic environments deep within the fractured igneous crust. This subterranean biosphere may constitute the largest fungal habitat on our planet, but 1234567890():,; knowledge of abyssal fungi and their syntrophic interactions with prokaryotes and their concomitant metabolisms is scarce. Here we report findings of fossilized, chitin-bearing fungal hyphae at ~540 m depth in fractured bedrock of the Siljan impact structure, the largest crater in Europe. Strong 13C-enrichment of calcite precipitated with and on the fungi suggests formation following methanogenesis, and that the anaerobic fungi decomposed dispersed organic matter producing for example H2 that may have fueled autotrophic methanogens. An Eocene age determined for the calcite infers the first timing constraint of fossilized fungi in the continental igneous crust. Fungi may be widespread decomposers of organic matter and overlooked providers of H2 to autotrophs in the vast rock-hosted deep biosphere. 1 Department of Biology and Environmental Science, Linnæus University, Kalmar, Sweden. 2 Swedish Museum of Natural History, Stockholm, Sweden. 3 Department of Geobiology, Geoscience Centre Göttingen of the Georg-August University, Göttingen, Germany. 4 Institute for Geology and Mineralogy, ✉ University of Cologne, Cologne, Germany. email: [email protected] COMMUNICATIONS EARTH & ENVIRONMENT | (2021) 2:34 | https://doi.org/10.1038/s43247-021-00107-9 | www.nature.com/commsenv 1 ARTICLE COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-021-00107-9 he deep biosphere is the largest microbial habitat on Earth describe the fossilized fungal remains. Stable isotopes and organic Tby volume1–4. The subsurface encompasses diverse envir- molecular remains of coeval secondary minerals are used to link onments and ecosystems, including severely energy limited the fungi to prokaryotic metabolisms, such as methanogenesis. deep biosphere ecosystems, inhabited by ancient evolutionary Microbial methane has formed in this impact structure at least microbial lineages, adapted to subsurface conditions1,5,6. since the Late Cretaceous33, making it an optimal site for Knowledge of these lifeforms and processes has important exploration of potential ancient fungi–methanogen relationships. implications for life in extreme environments and evolution on Our findings suggest a link between anaerobic fungi and Earth, as well as significance for the quest for life on other planets methanogens at several hundred meters depth in the impact and icy moons7. Estimates of the total biomass in the continental crater, in a putative process where fungi fueled methanogenesis fi deep biosphere range from a couple of percent to almost 20% of via H2 production during degradation of organic matter in l- 4,8 33 Earth’s total . Research on active communities in the deep trated from black shales . This complements H2 from other biosphere has so far focused on prokaryotes. Recent studies have, sources such as abiotic and prokaryotic fermentation, and man- however, shown that microorganisms of all three domains of life ifests a potentially widespread and long-term ecological influence are abundant and active in deep aquifers in Precambrian crys- of fungi for methane formation in the vast deep biosphere talline rocks9, which make up the largest volumes of the con- environment. This may be of great importance, since methane is a tinental crust10. Eukaryotes have been detected at several very potent greenhouse gas34. We also establish the first timing kilometers depth11, but the general trend is increased proportion constraints of anaerobic fungi in the continental deep biosphere, of prokaryotes with declination12. Of the eukaryotes, organisms by linking it to previously reported U-Pb dating of coeval calcite33 of the kingdom Fungi have been detected in several studies of and, in addition, detect a tetrahymanol biodegradation product in deep present-day fracture waters13,14. Deep remnants of ancient the form of 30nor-gammacerane in the fungal remnants. fungi have been found in fractured igneous rock in Sweden15,16. Fungi are evidently inhabiting the deep igneous biosphere, but knowledge about their ecological role, and how long they have Results dwelled in this environment is far from resolved. From other The eroded Siljan crater has an age of 380.9 ± 4.6 Ma35 and has settings, ancient remains of fungi or fungus-like structures have down-faulted Devonian and Silurian sedimentary rocks with been detected in cavities and/or beddings of Neoproterozoic thicknesses of up to 400–500 m36,37 in a circular crater rim sedimentary rocks17,18 and in vesicular basalt of Devonian19 and depression (Fig. 1). Cored boreholes of up to 700 m depth Paleoproterozoic age20. The most convincing fungal fossils are penetrate the rim zone38. Open fractures in seven of these drill Phanerozoic in age21. cores representing both the sedimentary units and the underlying The shift to anoxic conditions generally occurs within the Paleoproterozoic felsic host rock were screened for the presence upper tens of meters in continental igneous aquifers22 suggesting of fossilized microorganisms. A methane-dominated gas was that the majority of deep biosphere microorganisms, including encountered at several depths during borehole drilling, both in fungi, have adapted to an anaerobic lifestyle. Most studies of the sedimentary units and in the deeper basement33. Bituminous obligate anaerobic fungi, and hence most well-established meta- material and seep oil of shale origin are scattered in the pore bolic models, are of the phylum Neocallimastigomycota living in space and fractures of both sedimentary rocks39,40 and the deeper the rumens of herbivores. Neocallimastigomycota possess redox igneous rocks33. A highly fractured and porous core section in organelles called hydrogenosomes instead of mitochondria that granite-rhyolite at depths between 534 and 542 m in borehole produce H2 (as well as CO2, lactate, and formate) as a metabolic CC1 contained scattered filamentous carbonaceous material waste product23–25. In the rumen, fungi consort symbiotically resembling fungal hyphae. Five fractures in this section were with prokaryotes, such as methanogens26,27, and symbiotic rela- sampled for detailed analysis. This rock section is >125 m below tionships between gut fungi and methanogens in relation to the contact to the Paleozoic sedimentary units and represents a changing diets have been reported28. For the deep biosphere, sub-vertically dipping fracture network structure. The fractures anaerobic fungi have been shown to have distinct survival stra- are partly sealed by mineral infillings, but abundant open cavities tegies to adapt to anaerobic ecosystems (e.g., ethanol fermenta- with euhedral crystals remain, providing open pore space for tion and production of amino acids by Schizophyllum commune colonization by microorganisms (Fig. 1c, d). The open cavities 20R-7-F01 in sediments at 2 km below the seafloor29) and a were exposed in the laboratory by opening the fractures physi- similar type of syntrophic consortium as in rumens has been cally with a chisel. The exposed fracture surfaces contain carbo- proposed, where fungi produce H2 that can be used by indigenous naceous material, euhedral crystals of calcite, pyrite, and clay autotrophic prokaryotes, such as sulfate reducers16,30,31. The minerals grown on older euhedral quartz that lines the host rock hypothesis includes degradation of prokaryotic biofilms by het- contact (Fig. 1e). The morphology of the calcite crystals reveals erotrophic fungi and production of H2 as a waste product that more than one generation; an older core and an overgrowth then fuels the autotrophic communities, marking a potentially (Calcite-1 and Calcite-OG, Fig. 1e). key ecological role for fungi in the deep biosphere31. When The carbonaceous material occurs as thin films resembling anaerobic fungi are enriched together with methanogens, they are extracellular polymeric substance (EPS) biofilms on the fracture able to degrade lignocellulose and produce more methane than surface, preferentially on quartz (Fig. 2a) but also on the euhedral bacteria and methanogens do32. This suggests that consortia of calcite crystals (Fig. 1e). From this presumed biofilm, filamentous anaerobic fungi and methanogens in the deep subsurface hold the structures protrude into the open cavity as single filaments or as potential for methane production, not only from lignocellulose, intertwined mycelium-like networks (Fig. 2b, c) that are inter- but also from other sources of organic matter that may be more grown with the outermost parts of the calcite overgrowths. The recalcitrant to degradation by bacteria and methanogens. This filaments have diameters of ~10 ± 5 µm, and extend as undulating opens up a unique niche and new role for subsurface, fungal- features of more than a millimeter (Fig. 3a) from the onset at the methanogen consortia to fill, but in situ evidence of such con- biofilm (Fig. 3b). At contact with mineral surfaces the filaments sortia has not yet been reported form the deep subsurface. widen in a tapered fashion
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