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

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          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.

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          Microbial ecology of the dark ocean above, at, and below the seafloor.

          The majority of life on Earth--notably, microbial life--occurs in places that do not receive sunlight, with the habitats of the oceans being the largest of these reservoirs. Sunlight penetrates only a few tens to hundreds of meters into the ocean, resulting in large-scale microbial ecosystems that function in the dark. Our knowledge of microbial processes in the dark ocean-the aphotic pelagic ocean, sediments, oceanic crust, hydrothermal vents, etc.-has increased substantially in recent decades. Studies that try to decipher the activity of microorganisms in the dark ocean, where we cannot easily observe them, are yielding paradigm-shifting discoveries that are fundamentally changing our understanding of the role of the dark ocean in the global Earth system and its biogeochemical cycles. New generations of researchers and experimental tools have emerged, in the last decade in particular, owing to dedicated research programs to explore the dark ocean biosphere. This review focuses on our current understanding of microbiology in the dark ocean, outlining salient features of various habitats and discussing known and still unexplored types of microbial metabolism and their consequences in global biogeochemical cycling. We also focus on patterns of microbial diversity in the dark ocean and on processes and communities that are characteristic of the different habitats.
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            Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation.

            The study of the role that fungi have played and are playing in fundamental geological processes can be termed 'geomycology' and this article seeks to emphasize the fundamental importance of fungi in several key areas. These include organic and inorganic transformations and element cycling, rock and mineral transformations, bioweathering, mycogenic mineral formation, fungal-clay interactions, metal-fungal interactions, and the significance of such processes in the environment and their relevance to areas of environmental biotechnology such as bioremediation. Fungi are intimately involved in biogeochemical transformations at local and global scales, and although such transformations occur in both aquatic and terrestrial habitats, it is the latter environment where fungi probably have the greatest influence. Within terrestrial aerobic ecosystems, fungi may exert an especially profound influence on biogeochemical processes, particularly when considering soil, rock and mineral surfaces, and the plant root-soil interface. The geochemical transformations that take place can influence plant productivity and the mobility of toxic elements and substances, and are therefore of considerable socio-economic relevance, including human health. Of special significance are the mutualistic symbioses, lichens and mycorrhizas. Some of the fungal transformations discussed have beneficial applications in environmental biotechnology, e.g. in metal leaching, recovery and detoxification, and xenobiotic and organic pollutant degradation. They may also result in adverse effects when these processes are associated with the degradation of foodstuffs, natural products, and building materials, including wood, stone and concrete. It is clear that a multidisciplinary approach is essential to understand fully all the phenomena encompassed within geomycology, and it is hoped that this review will serve to catalyse further research, as well as stimulate interest in an area of mycology of global significance.
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              Gene expression in the deep biosphere.

              Scientific ocean drilling has revealed a deep biosphere of widespread microbial life in sub-seafloor sediment. Microbial metabolism in the marine subsurface probably has an important role in global biogeochemical cycles, but deep biosphere activities are not well understood. Here we describe and analyse the first sub-seafloor metatranscriptomes from anaerobic Peru Margin sediment up to 159 metres below the sea floor, represented by over 1 billion complementary DNA (cDNA) sequence reads. Anaerobic metabolism of amino acids, carbohydrates and lipids seem to be the dominant metabolic processes, and profiles of dissimilatory sulfite reductase (dsr) transcripts are consistent with pore-water sulphate concentration profiles. Moreover, transcripts involved in cell division increase as a function of microbial cell concentration, indicating that increases in sub-seafloor microbial abundance are a function of cell division across all three domains of life. These data support calculations and models of sub-seafloor microbial metabolism and represent the first holistic picture of deep biosphere activities.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 October 2015
                2015
                : 10
                : 10
                : e0140106
                Affiliations
                [1 ]Department of Palaeobiology and Nordic Center for Earth Evolution, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden
                [2 ]Department of Geosciences, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden
                [3 ]Department of Earth Sciences, Uppsala University, Villavägen 16, SE-752 36 Uppsala, Sweden
                [4 ]Department of Geological Sciences, Stockholm University, Svante Arrheniusväg 8, SE-106 91, Stockholm, Sweden
                [5 ]Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden
                [6 ]Swiss Light Source, Paul Scherrer Institute, CH-5232 Villigen, Switzerland
                The University of Wisconsin - Madison, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MI SB. Performed the experiments: MI SB HS PL CB VB FM. Analyzed the data: MI SB HS PL CB VB FM. Wrote the paper: MI SB HS PL CB.

                Article
                PONE-D-15-26070
                10.1371/journal.pone.0140106
                4619311
                26488482
                d8887246-44d7-41ad-a853-e3f3a9d53417
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 16 June 2015
                : 22 September 2015
                Page count
                Figures: 11, Tables: 0, Pages: 19
                Funding
                SB and MI was funded by the Swedish Research Council (Contracts No. 2010-3929 and 2012-4364): http://www.vr.se/, and the Danish National Research Foundation (DNRF53): http://dg.dk/en/. The work was also funded by a grant to Phil Donoghue (PI) and SB (Co-PI) by Paul Scherrer Institute (20130185 and 20141047): http://www.psi.ch/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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