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Fungus-Like Mycelial Fossils in 2.4-Billion-Year-Old Vesicular Basalt

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Fungus-Like Mycelial Fossils in 2.4-Billion-Year-Old Vesicular Basalt ARTICLES PUBLISHED: 24 APRIL 2017 | VOLUME: 1 | ARTICLE NUMBER: 0141 Fungus-like mycelial fossils in 2.4-billion-year-old vesicular basalt Stefan Bengtson1*, Birger Rasmussen2*, Magnus Ivarsson1, Janet Muhling2, 3, Curt Broman4, Federica Marone5, Marco Stampanoni5, 6 and Andrey Bekker7 Fungi have recently been found to comprise a significant part of the deep biosphere in oceanic sediments and crustal rocks. Fossils occupying fractures and pores in Phanerozoic volcanics indicate that this habitat is at least 400 million years old, but its origin may be considerably older. A 2.4-billion-year-old basalt from the Palaeoproterozoic Ongeluk Formation in South Africa contains filamentous fossils in vesicles and fractures. The filaments form mycelium-like structures growing from a basal film attached to the internal rock surfaces. Filaments branch and anastomose, touch and entangle each other. They are indistin- guishable from mycelial fossils found in similar deep-biosphere habitats in the Phanerozoic, where they are attributed to fungi on the basis of chemical and morphological similarities to living fungi. The Ongeluk fossils, however, are two to three times older than current age estimates of the fungal clade. Unless they represent an unknown branch of fungus-like organisms, the fossils imply that the fungal clade is considerably older than previously thought, and that fungal origin and early evolution may lie in the oceanic deep biosphere rather than on land. The Ongeluk discovery suggests that life has inhabited submarine volcanics for more than 2.4 billion years. he deep biosphere, hidden beneath land and sea, represents a chlorite, K-feldspar, quartz and calcite, with accessory apatite and major portion of life’s habitats and biomass on Earth1. In spite Fe-Ti oxides. Amygdales and veins are present, characterized by Tof significant discoveries from scientific ocean drilling and chlorite and calcite representing mineral infills of original vesicles metagenomics, the deep biosphere remains largely uncharted and and fractures in the lavas. The spherical to subspherical amygda- its geological history almost entirely unknown. The deep habitats les are up to 1.5 mm in diameter (Figs 2 and 3). Most have rims are protected from most of the hazards of surface life, and the deep composed of masses of very fine-grained, brownish green chlo- environments would have been potentially available to life from the rite, chlorite 1. Thermometry of chlorite 1 yields metamorphic early stages of Earth’s history. Here, we report filamentous struc- temperatures in the range of 179–260 °C (Supplementary Fig. 1; tures preserved in carbonate- and chlorite-filled amygdales and Supplementary Discussion). Where filaments are present, they are fractures in basaltic lavas of the 2.4-Gyr-old Ongeluk Formation, defined by chlorite 1. No carbonaceous material has been detected South Africa. Their morphology, dimensions and striking similar- within the filaments (Supplementary Fig. 2a). Calcite typically forms ity to fungi in Phanerozoic volcanics2–7 indicate that they represent a cylindrical layer of constant thickness around the filaments; the fossilized fungus-like mycelial organisms. The observation that blocky arrangement of crystals in the calcite, without clear relation fungus-like organisms inhabited submarine basaltic lavas more than to filament morphology (Fig. 4e), suggests that the calcite has been 2.4 Gyr ago (Ga) suggests that this habitat was extremely conserva- recrystallized. Fine-grained chlorite 1 fills the space between the cal- tive across the Proterozoic and Phanerozoic eons, and raises ques- cite cylinders (Figs 2b,d,e,g and 4; Supplementary Figs 3a,b, 4 and 5). tions about the antiquity of fungi and the early history of eukaryotes. A second generation of chlorite, chlorite 2, coarser-grained and apple green, commonly intergrown with quartz and chalcopy- Geological setting rite, is present in some amygdales and fractures. Chlorite 2 is not The Ongeluk Formation is a 900-m-thick succession of basalts in pervasive but overprints chlorite 1, including filaments defined the Griquatown West Basin, South Africa. The lavas are regionally by chlorite 1 (Fig. 4d,e; Supplementary Fig. 4d). Thermometry extensive and comprise massive flows, pillow lavas and hyaloclas- of chlorite 2 gives metamorphic temperatures of 319–411 °C tites that extruded onto the seafloor around 2.4 Ga; the basalts have (Supplementary Figs 1 and 5; Supplementary Discussion). Its asso- undergone only very low-grade metamorphism (Supplementary ciation with chalcopyrite, occurrence in veins and otherwise non- Discussion). The fossiliferous sample (AG4) is a 25-cm-long ¼ core pervasive distribution suggest that the growth of chlorite 2 was derived from drill depth 21.79–22.04 m of the Agouron drill hole linked to hydrothermal fluids. GTF01, which penetrated the lower part of the Ongeluk Formation (Fig. 1). About 70 of the ~100 observed amygdales contain filaments. Filament structure and morphology The sample is a chlorite-altered basalt with a relict igneous The filaments extend from rims of chlorite 1 attached to amygdale texture consisting of pseudomorphs of pyroxene and plagioclase and fracture walls, and form a tangled network inside vesicles and (Supplementary Discussion). The groundmass consists of intergrown fractures in the rock (Figs 2–4; Supplementary Fig. 3). The density 1Department of Palaeobiology and Nordic Center for Earth Evolution, Swedish Museum of Natural History, SE-10405 Stockholm, Sweden. 2Department of Applied Geology, Curtin University, Bentley, Western Australia 6102, Australia. 3School of Earth and Environment, The University of Western Australia, Perth, Western Australia 6009, Australia. 4Department of Geological Sciences, Stockholm University, SE-10691 Stockholm, Sweden. 5Swiss Light Source, Paul Scherrer Institute, CH-5232 Villigen, Switzerland. 6Institute for Biomedical Engineering, University and ETH Zürich, CH-8092 Zürich, Switzerland. 7Department of Earth Sciences, University of California, Riverside, California 92521, USA. *e-mail: [email protected]; [email protected] NATURE ECOLOGY AND EVOLUTION 1, 0141 (2017) | DOI: 10.1038/s41559-017-0141 | www.nature.com/natecolevol 1 © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. ARTICLES NATURE ECOLOGY AND EVOLUTION 24° E 28° E ab c ve Kaapvaal Transvaal 24° S c Yj Craton an South Africa Ca 26° S Griqualand Johannesburg 1 mm 100 µm10 µm West d e Chl1 f 28° E 100 km an Kathu Ca 28° S Black Ridge Thrust Vryburg GTF01 Chl1 10 µm 10 µm Prieska Kuruman e 30° S h 100 µm Griqualand West Transvaal NE g Bushveld Complex Griquatown 50 km Ca Chl1 Upper Transvaal Upper Transvaal Ca Supergroup Supergroup Upper Transvaal Supergroup Kuruman and Griquatown Penge Iron Fm. Iron Formations Olifantshoek SW GTF01 Group Chl1 Campbellrand Subgroup Malmani Subgroup Prieska Postmasburg Schmidtsdrif Subgroup Wolkberg Group and Elim Groups 10 µm 100 µm Koegas Subgrp i jk SW NE ve bf bf Mooidraai Chl1 Formation Carbonate platform Hotazel Fm. Banded iron formation k bf Chl1 Ca 10 µm Ca hy Submarine basalt Diamictite Ongeluk l Ca 5 µm Formation Chl1 100 m GTF01 µ hy 50 µm Banded iron formation Makganyene Figure 2 | Ongeluk vesicular basalt with filamentous fossils, petrographic Koegas Subgrp thin sections. a, Basalt with vesicles frequently connected by veins; Griquatown Formation Carbonate platform Swedish Museum of Natural History X6129. b,c, Anastomosing network; X6130. d,e, Vesicle with broom structure; note distinction between calcite Kamden Member Kuruman (light) and chlorite (dark) cement; X6131. f, Anastomosis; X6132. g, Broom Formation structure in fracture (same specimen as in Fig. 4); X6133. h, Broom; X6134. Klein Naute i, Vesicle connected to vein filled with calcite (light) and chlorite (dark) Nauga Slope and Sandstone cement; X6135. j–l, Basal film and marginal network; X6136. Panels a–i Formation basinal show transmitted light images; panels j–l show ESEM images produced in backscatter mode. Lettered frames indicate position of enlargements in Schmidtsdrif Shale other panels. an, anastomosis; bf, basal film; Ca, calcite; Chl1, chlorite 1; hy, hypha; ve, vein; Yj, Y-junction. Figure 1 | Geological map and stratigraphic section of the Griqualand West sub-basin, showing the location of Agouron drill hole GTF01 (28° 49 39.7 S, 23° 07 24.1 E). The fossiliferous sample is from the ′ ′′ ′ ′′ Branchings at acute angles, Y-junctions, are common among lower part of the Ongeluk Formation (drill depth 21.79 m). Fm., formation; the free filaments (Figs 2c and 3f,g). T-junctions also occur subgrp, subgroup. Modified from ref. 53, Geological Society of America. (Fig. 3g), although considerably less frequently. Filaments with different orientation commonly touch and entangle each other of the filamentous network typically decreases towards the centre of (Fig. 3f,i), and crossing filaments sometimes seem to merge the cavities (Fig. 2b,d,j, 3a,e and 4b; Supplementary Fig. 3a,b). The seamlessly. Where none of the filaments change direction, chlorite rim represents an uneven basal film consisting of a jumbled the crossing is interpreted as coincidental (Fig. 2l). This phe- mass with little space remaining between filaments (Figs 2j,k and 3e; nomenon of taphonomic/diagenetic filament merging makes Supplementary Fig. 3). Scanning electron microscopy (SEM)/ it sometimes difficult to identify true branching, where a single back-scattered electron (BSE)/wavelength-dispersive X-ray spec- filament is split into two. When Y-junctions on the same appar- troscopy (WDS) images confirm that the structure and compo- ently branching filament point in opposite directions (Fig. 3c), sition are identical between filaments and basal film (Fig. 2j,k; one or both junctions may represent false branching; this can Supplementary Figs 4 and 5). also be indicated by the filament being thicker, or even appear- Filaments are 2–12 μ m wide; the width is usually constant within ing doubled, below a Y-junction. There are, however, a number a filament. No internal septa have been identified, but original inter- of cases where the morphology of the junction leaves little nal structure is not preserved (Fig.
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