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  • 1.
    Bengtson, Stefan
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Ivarsson, Magnus
    Swedish Museum of Natural History, Department of Paleobiology.
    Astolfo, Alberto
    Paul Scherrer Institute.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Broman, Curt
    Stockholm University.
    Marone, Federica
    Paul Scherrer Institute.
    Stampanoni, Marco
    ETH Zürich.
    Deep-biosphere consortium of fungi and prokaryotes in Eocene sub-seafloor basalts.2014In: Geobiology, ISSN 1472-4677, E-ISSN 1472-4669, Vol. 12, no 6, p. 489-496Article in journal (Refereed)
    Abstract [en]

    The deep biosphere of the subseafloor crust is believed to contain a significant part of Earth’s biomass, but because of the difficulties of directly observing the living organisms, its composition and ecology are poorly known. We report here a consortium of fossilized prokaryotic and eukaryotic microorganisms, occupying cavities in deep-drilled vesicular basalt from the Emperor Seamounts, Pacific Ocean, 67.5 meters below seafloor (mbsf). Fungal hyphae provide the framework on which prokaryote-like organisms are suspended like cobwebs and iron-oxidizing bacteria form microstromatolites (Frutexites). The spatial interrelationships show that the organisms were living at the same time in an integrated fashion, suggesting symbiotic interdependence. The community is contemporaneous with secondary mineralizations of calcite partly filling the cavities. The fungal hyphae frequently extend into the calcite, indicating that they were able to bore into the substrate through mineral dissolution. A symbiotic relationship with chemoautotrophs, as inferred for the observed consortium, may be a prerequisite for the eukaryotic colonization of crustal rocks. Fossils thus open a window to the extant as well as the ancient deep biosphere.

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  • 2.
    Bengtson, Stefan
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Sallstedt, Therese
    Swedish Museum of Natural History, Department of Paleobiology.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Whitehouse, Martin
    Swedish Museum of Natural History, Department of Geology.
    Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae2017In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 15, no 3, p. 1-38, article id e2000735Article in journal (Refereed)
    Abstract [en]

    The ~1.6 Ga Tirohan Dolomite of the Lower Vindhyan in central India contains phosphatized stromatolitic microbialites. We report from there uniquely well-preserved fossils interpreted as probable crown-group rhodophytes (red algae). The filamentous form Rafatazmia chitrakootensis n. gen, n. sp. has uniserial rows of large cells and grows through diffusely distributed septation. Each cell has a centrally suspended, conspicuous rhomboidal disk interpreted as a pyrenoid. The septa between the cells have central structures that may represent pit connections and pit plugs. Another filamentous form, Denaricion mendax n. gen., n. sp., has coin-like cells reminiscent of those in large sulfur-oxidizing bacteria but much more recalcitrant than the liquid-vacuole-filled cells of the latter. There are also resemblances with oscillatoriacean cyanobacteria, although cell volumes in the latter are much smaller. The wider affinities of Denaricion are uncertain. Ramathallus lobatus n. gen., n. sp. is a lobate sessile alga with pseudoparenchymatous thallus, “cell fountains,” and apical growth, suggesting florideophycean affinity. If these inferences are correct, Rafatazmia and Ramathallus represent crown-group multicellular rhodophytes, antedating the oldest previously accepted red alga in the fossil record by about 400 million years.

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  • 3. Chi Fru, Ernest
    et al.
    Ivarsson, Magnus
    Swedish Museum of Natural History, Department of Paleobiology.
    Kilias, Stephanos P
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Marone, Federica
    Paul Scherrer Institute.
    Fortin, Danielle
    Broman, Curt
    Stampanoni, Marco
    ETH Zürich.
    Fossilized iron bacteria reveal pathway to biological origin of banded iron formation.2013In: Nature Communications, ISSN 2041-1723, Vol. 4, no 2050, p. 1-7Article in journal (Refereed)
    Abstract [en]

    Debates on the formation of banded iron formations in ancient ferruginous oceans are dominated by a dichotomy between abiotic and biotic iron cycling. This is fuelled by difficulties in unravelling the exact processes involved in their formation. Here we provide fossil environmental evidence for anoxygenic photoferrotrophic deposition of analogue banded iron rocks in shallow marine waters associated with an Early Quaternary hydrothermal vent field on Milos Island, Greece. Trace metal, major and rare earth elemental compositions suggest that the deposited rocks closely resemble banded iron formations of Precambrian origin. Well-preserved microbial fossils in combination with chemical data imply that band formation was linked to periodic massive encrustation of anoxygenic phototrophic biofilms by iron oxyhydroxide alternating with abiotic silica precipitation. The data implicate cyclic anoxygenic photoferrotrophy and their fossilization mechanisms in the construction of microskeletal fabrics that result in the formation of characteristic banded iron formation bands of varying silica and iron oxide ratios.

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    ChiFru_etal_2013_BIF_MS
  • 4.
    Cunningham, John
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Vargas, Kelly
    Liu, Pengju
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Marone, Federica
    Martínez-Pérez, Carlos
    Guizar-Sicairos, Manuel
    Holler, Mirko
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Donoghue, Philip C.J.
    Critical appraisal of tubular putative eumetazoans from the Ediacaran Weng’an Doushantuo biota2015In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, p. 1-9, article id 2151169Article in journal (Refereed)
    Abstract [en]

    Molecular clock analyses estimate that crown-group animals began diversifying hundreds of millions of years before the start of the Cambrian period. However, the fossil record has not yielded unequivocal evidence for animals during this interval. Some of the most promising candidates for Precambrian animals occur in theWeng’an biota of South China, including a suite of tubular fossils assigned to Sinocyclocyclicus, Ramitubus, Crassitubus and Quadratitubus, that have been interpreted as soft-bodied eumetazoans comparable to tabulate corals. Here, we present new insights into the anatomy, original composition and phylogenetic affinities of these taxa based on data from synchrotron radiation X-ray tomographic microscopy, ptychographic nanotomography, scanning electron microscopy and electron probe microanalysis. The patterns of deformation observed suggest that the cross walls of Sinocyclocyclicus and Quadratitubus were more rigid than those of Ramitubus and Crassitubus. Ramitubus and Crassitubus specimens preserve enigmatic cellular clusters at terminal positions in the tubes. Specimens of Sinocyclocyclicus and Ramitubus have biological features that might be cellular tissue or subcellular structures filling the spaces between the crosswalls. These observations are incompatible with a cnidarian interpretation, in which the spaces between cross walls are abandoned parts of the former living positions of the polyp. The affinity of the Weng’an tubular fossils may lie within the algae.

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    Cunningham_etal_2015_Tubular
  • 5. Drake, Henrik
    et al.
    Ivarsson, Magnus
    Swedish Museum of Natural History, Department of Paleobiology.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Heim, Christine
    Siljeström, Sandra
    Whitehouse, Martin
    Swedish Museum of Natural History, Department of Geology.
    Broman, Curt
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Åström, Mats E.
    Anaerobic consortia of fungi and sulfate reducing bacteria in deep granite fractures2017In: Nature Communications, E-ISSN 2041-1723, Vol. 8, no 55, p. 1-9Article in journal (Refereed)
    Abstract [en]

    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.

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  • 6. Drake, Henrik
    et al.
    Ivarsson, Magnus
    Swedish Museum of Natural History, Department of Paleobiology.
    Heim, Christine
    Snoeyenbos-West, Oona
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Whitehouse, Martin
    Swedish Museum of Natural History, Department of Geology.
    Fossilized anaerobic and possibly methanogenesis-fueling fungi identified deep within the Siljan impact structure, Sweden2021In: Communications Earth & Environment, E-ISSN 2662-4435, Vol. 2, no 1, p. 1-11Article in journal (Refereed)
    Abstract [en]

    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 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.

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  • 7.
    Ivarsson, Magnus
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Stampanoni, Marco
    ETH Zürich.
    Marone, Federica
    Paul Scherrer Institute.
    Tehler, Anders
    Swedish Museum of Natural History, Department of Botany.
    Fossilized fungi in subseafloor Eocene basalts.2012In: Geology, ISSN 0091-7613, Vol. 40, no 2, p. 163-166Article in journal (Refereed)
    Abstract [en]

    The deep biosphere of subseafl oor basalts is thought to consist of mainly prokaryotes (bacteria and archaea). Here we report fossilized fi lamentous microorganisms from subseafl oor basalts interpreted as fossilized fungal hyphae, probably Dikarya, rather than fossilized prokaryotes. The basalts were collected during the Ocean Drilling Program Leg 197 at the Emperor Seamounts, North Pacifi c Ocean, and the fossilized fungi are observed in carbonate-fi lled veins and vesicles in samples that represent a depth of ~150 m below the seafl oor. Three-dimensional visualizations using synchrotron-radiation X-ray tomographic microscopy show characteristic fungal morphology of the mycelium-like network, such as frequent branching, anastomosis, and septa. Possible presence of chitin in the hypha walls was detected by staining with Wheat Germ Agglutinin conjugated with Fluorescein Isothiocyanate and examination using fl uorescence microscopy. The presence of fungi in subseafl oor basalts challenges the present understanding of the deep subseafl oor biosphere as being exclusively prokaryotic.

  • 8.
    Ivarsson, Magnus
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Skogby, Henrik
    Swedish Museum of Natural History, Department of Geology.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Marone, Federica
    Paul Scherrer Institute.
    Fungal colonies in open fractures of subseafloor basalt.2013In: Geo-Marine Letters, ISSN 0276-0460, E-ISSN 1432-1157, Vol. 33, no 4, p. 233-234Article in journal (Refereed)
    Abstract [en]

    The deep subseafloor crust is one of the few great frontiers of unknown biology on Earth and, still today, the notion of the deep biosphere is commonly based on the fossil record. Interpretation of palaeobiological information is thus central in the exploration of this hidden biosphere and, for each new discovery, criteria used to establish biogenicity are challenged and need careful consideration. In this paper networks of fossilized filamentous structures are for the first time described in open fractures of subseafloor basalts collected at the Emperor Seamounts, Pacific Ocean. These structures have been investigated with optical microscopy, environmental scanning electron microscope, energy dispersive spectrometer, X-ray powder diffraction as well as synchrotron-radiation X-ray tomographic microscopy, and interpreted as fossilized fungal mycelia.Morphological features such as hyphae, yeastlike growth and sclerotia were observed. The fossilized fungi are mineralized by montmorillonite, a process that probably began while the fungi were alive. It seems plausible that the fungi produced mucilaginous polysaccharides and/or extracellular polymeric substances that attracted minerals or clay particles, resulting in complete fossilization by montmorillonite. The findings are in agreement with previous observations of fossilized fungi in subseafloor basalts and establish fungi as regular inhabitants of such settings. They further show that fossilized microorganisms are not restricted to pore spaces filled by secondary mineralizations but can be found in open pore spaces as well. This challenges standard protocols for establishing biogenicity and calls for extra care in data interpretation.

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    Ivarsson_etal_2013_Fungal
  • 9.
    Ivarsson, Magnus
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Bengtson, Stefan
    Skogby, Henrik
    Lazor, Peter
    Broman, Curt
    Belivanova, Veneta
    Marone, Federica
    A fungal-prokaryotic consortium at the basalt-zeolite interface in subseafloor igneous crust2015In: PLOS ONE, E-ISSN 1932-6203Article in journal (Refereed)
  • 10.
    Ivarsson, Magnus
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Drake, Henrik
    Linnaeus University Faculty of Health and Life Sciences, Kalmar, Sweden.
    Neubeck, Anna
    Swedish Museum of Natural History, Department of Paleobiology. Uppsala University.
    Snoeyenbos-West, Oona
    Swedish Museum of Natural History, Department of Paleobiology. Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden.
    Belivanova, Veneta
    Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Introducing palaeolithobiology2021In: GFF, ISSN 1103-5897, E-ISSN 2000-0863, Vol. 143, no 2-3, p. 305-319Article in journal (Refereed)
    Abstract [en]

    A growing literature of deep but also surficial fossilized remains of lithobiological life, often associated with igneous rocks, necessitates the unfolding of a sub-discipline within paleobiology. Here, we introduce the term paleolithobiology as the new auxiliary sub-discipline under which fossilized lithobiology should be handled. We present key criteria that distinguish the paleolithobiological archive from the traditional one and discuss sample strategies as well as scientific perspectives. A majority of paleolithobiological material consists of deep biosphere fossils, and in order to highlight the relevance of these, we present new data on fungal fossils from the Lockne impact crater. Fungal fossils in the Lockne drill cores have been described previously but here we provide new insights into the presence of reproductive structures that indicate the fungi to be indigenous. We also show that these fungi frequently dissolve and penetrate secondary calcite, delineating the role lithobionts plays in geobiological cycles. We hope that the formalization of the sub-discipline paleolithobiology will not only highlight an overlooked area of paleobiology as well as simplify future studies of endo- and epilithic fossil material, but also improve our understanding of the history of the deep biosphere.

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  • 11.
    Ivarsson, Magnus
    et al.
    Swedish Museum of Natural History, Department of Paleobiology. University of Southern Denmark, Department of Biology and Nordic Center for Earth Evolution, Campusvej 55, Odense M, DK-5230, Denmark.
    Skogby, Henrik
    Swedish Museum of Natural History, Department of Geology.
    Phichaikamjornwut, Bongkot
    Gems and Jewelry Program, Faculty of Science, Srinakharinwirot University, Bangkok, Thailand .
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Siljeström, Sandra
    RISE Research Institutes of Sweden, Bioscience and Materials/Chemistry and Materials, Stockholm, Sweden.
    Ounchanum, Prayote
    Department of Geological Sciences, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand.
    Boonsong, Apichet
    Department of Geological Sciences, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand.
    Kruachanta, M
    Department of Geological Sciences, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand .
    Marone, Federica
    Swiss Light Source, Paul Scherrer Institute, Villigen, Switzerland.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Sara, Holmström
    Stockholm University, Department of Geological Sciences, Stockholm, Sweden.
    Intricate tunnels in garnets from soils and rivere sediments in Thailand - possible endolithic microborings2018In: PLOS ONE, E-ISSN 1932-6203, Vol. 13, no 8, article id e0200351Article in journal (Refereed)
    Abstract [en]

    Garnets from disparate geographical environments and origins such as oxidized soils and river sediments in Thailand host intricate systems of microsized tunnels that significantly decrease the quality and value of the garnets as gems. The origin of such tunneling has previously been attributed to abiotic processes. Here we present physical and chemical remains of endolithic microorganisms within the tunnels and discuss a probable biological origin of the tunnels. Extensive investigations with synchrotron-radiation X-ray tomographic microscopy (SRXTM) reveal morphological indications of biogenicity that further support a euendolithic interpretation. We suggest that the production of the tunnels was initiated by a combination of abiotic and biological processes, and that at later stages biological processes came to dominate. In environments such as river sediments and oxidized soils garnets are among the few remaining sources of bio-available Fe2+, thus it is likely that microbially mediated boring of the garnets has trophic reasons. Whatever the reason for garnet boring, the tunnel system represents a new endolithic habitat in a hard silicate mineral otherwise known to be resistant to abrasion and chemical attack.

  • 12.
    McMahon, Sean
    et al.
    UK Centre for Astrobiology School of Physics and Astronomy University of Edinburgh Edinburgh UK;School of Geosciences Grant Institute University of Edinburgh Edinburgh UK.
    Ivarsson, Magnus
    Swedish Museum of Natural History, Department of Paleobiology. Department of Paleobiology Swedish Museum of Natural History Stockholm Sweden.
    Wacey, David
    Centre for Microscopy Characterisation and Analysis The University of Western Australia Perth WA Australia.
    Saunders, Martin
    Centre for Microscopy Characterisation and Analysis The University of Western Australia Perth WA Australia.
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology. Department of Paleobiology Swedish Museum of Natural History Stockholm Sweden.
    Muirhead, David
    School of Geosciences King's College University of Aberdeen Aberdeen UK.
    Knoll, Pamela
    Department of Chemistry and Biochemistry Florida State University Tallahassee FL USA.
    Steinbock, Oliver
    Department of Chemistry and Biochemistry Florida State University Tallahassee FL USA.
    Frost, Daniel A.
    Department of Earth & Planetary Science University of California Berkeley CA USA.
    Dubiofossils from a Mars‐analogue subsurface palaeoenvironment: The limits of biogenicity criteria2021In: Geobiology, ISSN 1472-4677, E-ISSN 1472-4669, Vol. 19, no 5, p. 473-488Article in journal (Refereed)
    Abstract [en]

    The search for a fossil record of Earth's deep biosphere, partly motivated by potential analogies with subsurface habitats on Mars, has uncovered numerous assemblages of inorganic microfilaments and tubules inside ancient pores and fractures. Although these enigmatic objects are morphologically similar to mineralized microorganisms (and some contain organic carbon), they also resemble some abiotic structures. Palaeobiologists have responded to this ambiguity by evaluating problematic filaments against checklists of “biogenicity criteria”. Here, we describe material that tests the limits of this approach. We sampled Jurassic calcite veins formed through subseafloor serpentinization, a water–rock reaction that can fuel the deep biosphere and is known to have occurred widely on Mars. At two localities ~4 km apart, veins contained curving, branched microfilaments composed of Mg-silicate and Fe-oxide minerals. Using a wide range of analytical techniques including synchrotron X-ray microtomography and scanning transmission electron microscopy, we show that these features meet many published criteria for biogenicity and are comparable to fossilized cryptoendolithic fungi or bacteria. However, we argue that abiotic processes driven by serpentinization could account for the same set of lifelike features, and report a chemical garden experiment that supports this view. These filaments are, therefore, most objectively described as dubiofossils, a designation we here defend from criticism and recommend over alternative approaches, but which nevertheless signifies an impasse. Similar impasses can be anticipated in the future exploration of subsurface palaeo-habitats on Earth and Mars. To avoid them, further studies are required in biomimetic geochemical self-organization, microbial taphonomy and micro-analytical techniques, with a focus on subsurface habitats.

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