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      Zygomycetes in Vesicular Basanites from Vesteris Seamount, Greenland Basin – A New Type of Cryptoendolithic Fungi

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          Abstract

          Fungi have been recognized as a frequent colonizer of subseafloor basalt but a substantial understanding of their abundance, diversity and ecological role in this environment is still lacking. Here we report fossilized cryptoendolithic fungal communities represented by mainly Zygomycetes and minor Ascomycetes in vesicles of dredged volcanic rocks (basanites) from the Vesteris Seamount in the Greenland Basin. Zygomycetes had not been reported from subseafloor basalt previously. Different stages in zygospore formation are documented in the studied samples, representing a reproduction cycle. Spore structures of both Zygomycetes and Ascomycetes are mineralized by romanechite-like Mn oxide phases, indicating an involvement in Mn(II) oxidation to form Mn(III,VI) oxides. Zygospores still exhibit a core of carbonaceous matter due to their resistance to degradation. The fungi are closely associated with fossiliferous marine sediments that have been introduced into the vesicles. At the contact to sediment infillings, fungi produced haustoria that penetrated and scavenged on the remains of fragmented marine organisms. It is most likely that such marine debris is the main carbon source for fungi in shallow volcanic rocks, which favored the establishment of vital colonies.

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          Big bacteria.

          A small number of prokaryotic species have a unique physiology or ecology related to their development of unusually large size. The biomass of bacteria varies over more than 10 orders of magnitude, from the 0.2 microm wide nanobacteria to the largest cells of the colorless sulfur bacteria, Thiomargarita namibiensis, with a diameter of 750 microm. All bacteria, including those that swim around in the environment, obtain their food molecules by molecular diffusion. Only the fastest and largest swimmers known, Thiovulum majus, are able to significantly increase their food supply by motility and by actively creating an advective flow through the entire population. Diffusion limitation generally restricts the maximal size of prokaryotic cells and provides a selective advantage for microm-sized cells at the normally low substrate concentrations in the environment. The largest heterotrophic bacteria, the 80 x 600 microm large Epulopiscium sp. from the gut of tropical fish, are presumably living in a very nutrient-rich medium. Many large bacteria contain numerous inclusions in the cells that reduce the volume of active cytoplasm. The most striking examples of competitive advantage from large cell size are found among the colorless sulfur bacteria that oxidize hydrogen sulfide to sulfate with oxygen or nitrate. The several-cm-long filamentous species can penetrate up through the ca 500-microm-thick diffusive boundary layer and may thereby reach into water containing their electron acceptor, oxygen or nitrate. By their ability to store vast quantities of both nitrate and elemental sulfur in the cells, these bacteria have become independent of the coexistence of their substrates. In fact, a close relative, T. namibiensis, can probably respire in the sulfidic mud for several months before again filling up their large vacuoles with nitrate.
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            Abundance and diversity of microbial life in ocean crust.

            Oceanic lithosphere exposed at the sea floor undergoes seawater-rock alteration reactions involving the oxidation and hydration of glassy basalt. Basalt alteration reactions are theoretically capable of supplying sufficient energy for chemolithoautotrophic growth. Such reactions have been shown to generate microbial biomass in the laboratory, but field-based support for the existence of microbes that are supported by basalt alteration is lacking. Here, using quantitative polymerase chain reaction, in situ hybridization and microscopy, we demonstrate that prokaryotic cell abundances on seafloor-exposed basalts are 3-4 orders of magnitude greater than in overlying deep sea water. Phylogenetic analyses of basaltic lavas from the East Pacific Rise (9 degrees N) and around Hawaii reveal that the basalt-hosted biosphere harbours high bacterial community richness and that community membership is shared between these sites. We hypothesize that alteration reactions fuel chemolithoautotrophic microorganisms, which constitute a trophic base of the basalt habitat, with important implications for deep-sea carbon cycling and chemical exchange between basalt and sea water.
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              Evidence for microbial carbon and sulfur cycling in deeply buried ridge flank basalt.

              Sediment-covered basalt on the flanks of mid-ocean ridges constitutes most of Earth's oceanic crust, but the composition and metabolic function of its microbial ecosystem are largely unknown. By drilling into 3.5-million-year-old subseafloor basalt, we demonstrated the presence of methane- and sulfur-cycling microbes on the eastern flank of the Juan de Fuca Ridge. Depth horizons with functional genes indicative of methane-cycling and sulfate-reducing microorganisms are enriched in solid-phase sulfur and total organic carbon, host δ(13)C- and δ(34)S-isotopic values with a biological imprint, and show clear signs of microbial activity when incubated in the laboratory. Downcore changes in carbon and sulfur cycling show discrete geochemical intervals with chemoautotrophic δ(13)C signatures locally attenuated by heterotrophic metabolism.
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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
                16 July 2015
                2015
                : 10
                : 7
                : e0133368
                Affiliations
                [1 ]Department of Palaeobiology and the Center for Earth Evolution (NordCEE), Swedish Museum of Natural History, Stockholm, Sweden
                [2 ]Department of Geodynamics and Sedimentology, Center for Earth Sciences, University of Vienna, Vienna, Austria
                [3 ]Department of Botany, Swedish Museum of Natural History, Stockholm, Sweden
                [4 ]Department of Geological Sciences, Stockholm University, Svante Arrheniusväg 8, Stockholm, Sweden
                [5 ]MARUM–Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
                [6 ]Geobiology Group, Geoscience Centre, Georg-August University, Göttingen, Germany
                [7 ]Geochemistry & Isotope Biogeochemistry Group, Department for Marine Geology, Leibniz Institute for Baltic Sea Research (IOW), Warnemünde, Germany
                [8 ]School of Natural Sciences, Technology and Environmental Studies, Södertörn University, Alfred Nobels Allé 7, Stockholm, Sweden
                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 JP. Performed the experiments: MI JP AT CB WB KB JR MEB LNI. Analyzed the data: MI JP AT CB WB KB JR MEB LNI. Wrote the paper: MI JP AT CB WB.

                Article
                PONE-D-15-23913
                10.1371/journal.pone.0133368
                4504512
                26181773
                6befe5cd-1a77-4843-8ce6-54afd5c3cefc
                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
                : 5 June 2015
                : 26 June 2015
                Page count
                Figures: 8, Tables: 1, Pages: 16
                Funding
                This work was funded by the Swedish Research Council (Contract No. 2012-4364), the Deutsche Forschungsgemeinschaft through project BO 1583/3, PE 847/3, RE 665/25 within priority program 1144 ‘From Mantle to Ocean: Energy-, Material- and Lifecycles at Spreading Axes’, and the Danish National Research Foundation (DNRF53).
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