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      Rapid metabolism fosters microbial survival in the deep, hot subseafloor biosphere

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          Abstract

          A fourth of the global seabed sediment volume is buried at depths where temperatures exceed 80 °C, a previously proposed thermal barrier for life in the subsurface. Here, we demonstrate, utilizing an extensive suite of radiotracer experiments, the prevalence of active methanogenic and sulfate-reducing populations in deeply buried marine sediment from the Nankai Trough subduction zone, heated to extreme temperature (up to ~120 °C). The small microbial community subsisted with high potential cell-specific rates of energy metabolism, which approach the rates of active surface sediments and laboratory cultures. Our discovery is in stark contrast to the extremely low metabolic rates otherwise observed in the deep subseafloor. As cells appear to invest most of their energy to repair thermal cell damage in the hot sediment, they are forced to balance delicately between subsistence near the upper temperature limit for life and a rich supply of substrates and energy from thermally driven reactions of the sedimentary organic matter.

          Abstract

          In the deep sedimentary biosphere, 80 °C has been proposed as an upper thermal barrier for life. Using a suite of radiotracer experiments, this study reports active methanogenic and sulfate-reducing microbial populations with high cell-specific metabolic rates in deeply buried marine sediments from the Nankai Trough subduction zone, which reach temperatures up to 120 °C.

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          Most cited references68

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          SUPCRT92: A software package for calculating the standard molal thermodynamic properties of minerals, gases, aqueous species, and reactions from 1 to 5000 bar and 0 to 1000°C

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            Microbial life under extreme energy limitation.

            A great number of the bacteria and archaea on Earth are found in subsurface environments in a physiological state that is poorly represented or explained by laboratory cultures. Microbial cells in these very stable and oligotrophic settings catabolize 10⁴- to 10⁶-fold more slowly than model organisms in nutrient-rich cultures, turn over biomass on timescales of centuries to millennia rather than hours to days, and subsist with energy fluxes that are 1,000-fold lower than the typical culture-based estimates of maintenance requirements. To reconcile this disparate state of being with our knowledge of microbial physiology will require a revised understanding of microbial energy requirements, including identifying the factors that comprise true basal maintenance and the adaptations that might serve to minimize these factors.
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              Thermodynamics of hydrothermal systems at elevated temperatures and pressures

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                Author and article information

                Contributors
                ttreude@g.ucla.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                25 January 2022
                25 January 2022
                2022
                : 13
                : 312
                Affiliations
                [1 ]GRID grid.7048.b, ISNI 0000 0001 1956 2722, Center for Geomicrobiology, Department of Bioscience, , Aarhus University, ; Ny Munkegade 114, 8000 Aarhus C, Denmark
                [2 ]GRID grid.23731.34, ISNI 0000 0000 9195 2461, GFZ German Research Center for Geosciences, Section 3.7 Geomicrobiology, Telegrafenberg, ; 14473 Potsdam, Germany
                [3 ]GRID grid.7704.4, ISNI 0000 0001 2297 4381, MARUM-Center for Marine Environmental Sciences, , University of Bremen, ; Leobener Strasse 8, 28359 Bremen, Germany
                [4 ]GRID grid.5801.c, ISNI 0000 0001 2156 2780, Department of Environmental Systems Science, ETH Zürich, ; Universitätstrasse 16, 8092 Zürich, Switzerland
                [5 ]GRID grid.20431.34, ISNI 0000 0004 0416 2242, Graduate School of Oceanography, , University of Rhode Island, Narragansett Bay Campus, ; 215 South Ferry Road, Narragansett, RI 02882 USA
                [6 ]GRID grid.410588.0, ISNI 0000 0001 2191 0132, Kochi Institute for Core Sample Research, , Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Nankoku, ; Kochi, 783-8502 Japan
                [7 ]GRID grid.410588.0, ISNI 0000 0001 2191 0132, Mantle Drilling Promotion Office, , Institute for Marine-Earth Exploration and Engineering, JAMSTEC, ; Yokosuka, 237-0061 Japan
                [8 ]GRID grid.19006.3e, ISNI 0000 0000 9632 6718, Department of Earth, Planetary and Space Sciences, , University of California Los Angeles, ; Los Angeles, CA 90095 USA
                [9 ]GRID grid.19006.3e, ISNI 0000 0000 9632 6718, Department of Atmospheric and Oceanic Sciences, , University of California Los Angeles, ; Los Angeles, CA 90095 USA
                [10 ]GRID grid.8761.8, ISNI 0000 0000 9919 9582, Present Address: Department of Marine Sciences, , University of Gothenburg, ; Carl Skottsbergs Gata 22B, 413 19 Göteborg, Sweden
                Author information
                http://orcid.org/0000-0002-1618-3978
                http://orcid.org/0000-0002-3624-9639
                http://orcid.org/0000-0002-0938-2952
                http://orcid.org/0000-0002-1856-116X
                http://orcid.org/0000-0001-9943-4092
                http://orcid.org/0000-0003-2887-6525
                http://orcid.org/0000-0002-6440-1140
                http://orcid.org/0000-0001-8928-4254
                http://orcid.org/0000-0001-6366-286X
                Article
                27802
                10.1038/s41467-021-27802-7
                8789916
                35078973
                d06738b9-2bcf-44cb-908f-5615aabf1b4d
                © The Author(s) 2022

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 9 April 2021
                : 10 December 2021
                Funding
                Funded by: National Science Foundation Prime Award OCE-1450528 Please note that complete funding information is provided in the acknowledgements.
                Categories
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                © The Author(s) 2022

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                carbon cycle
                Uncategorized
                carbon cycle

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