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      Microbial activity in the marine deep biosphere: progress and prospects

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          Abstract

          The vast marine deep biosphere consists of microbial habitats within sediment, pore waters, upper basaltic crust and the fluids that circulate throughout it. A wide range of temperature, pressure, pH, and electron donor and acceptor conditions exists—all of which can combine to affect carbon and nutrient cycling and result in gradients on spatial scales ranging from millimeters to kilometers. Diverse and mostly uncharacterized microorganisms live in these habitats, and potentially play a role in mediating global scale biogeochemical processes. Quantifying the rates at which microbial activity in the subsurface occurs is a challenging endeavor, yet developing an understanding of these rates is essential to determine the impact of subsurface life on Earth's global biogeochemical cycles, and for understanding how microorganisms in these “extreme” environments survive (or even thrive). Here, we synthesize recent advances and discoveries pertaining to microbial activity in the marine deep subsurface, and we highlight topics about which there is still little understanding and suggest potential paths forward to address them. This publication is the result of a workshop held in August 2012 by the NSF-funded Center for Dark Energy Biosphere Investigations (C-DEBI) “theme team” on microbial activity ( www.darkenergybiosphere.org).

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          Most cited references143

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          Trends, rhythms, and aberrations in global climate 65 Ma to present.

          Since 65 million years ago (Ma), Earth's climate has undergone a significant and complex evolution, the finer details of which are now coming to light through investigations of deep-sea sediment cores. This evolution includes gradual trends of warming and cooling driven by tectonic processes on time scales of 10(5) to 10(7) years, rhythmic or periodic cycles driven by orbital processes with 10(4)- to 10(6)-year cyclicity, and rare rapid aberrant shifts and extreme climate transients with durations of 10(3) to 10(5) years. Here, recent progress in defining the evolution of global climate over the Cenozoic Era is reviewed. We focus primarily on the periodic and anomalous components of variability over the early portion of this era, as constrained by the latest generation of deep-sea isotope records. We also consider how this improved perspective has led to the recognition of previously unforeseen mechanisms for altering climate.
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            Global distribution of microbial abundance and biomass in subseafloor sediment.

            The global geographic distribution of subseafloor sedimentary microbes and the cause(s) of that distribution are largely unexplored. Here, we show that total microbial cell abundance in subseafloor sediment varies between sites by ca. five orders of magnitude. This variation is strongly correlated with mean sedimentation rate and distance from land. Based on these correlations, we estimate global subseafloor sedimentary microbial abundance to be 2.9⋅10(29) cells [corresponding to 4.1 petagram (Pg) C and ∼0.6% of Earth's total living biomass]. This estimate of subseafloor sedimentary microbial abundance is roughly equal to previous estimates of total microbial abundance in seawater and total microbial abundance in soil. It is much lower than previous estimates of subseafloor sedimentary microbial abundance. In consequence, we estimate Earth's total number of microbes and total living biomass to be, respectively, 50-78% and 10-45% lower than previous estimates.
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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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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                11 July 2013
                2013
                : 4
                : 189
                Affiliations
                [1] 1Bigelow Laboratory for Ocean Sciences East Boothbay, ME, USA
                [2] 2Department of Earth Sciences, University of Southern California Los Angeles, CA, USA
                [3] 3College of Earth, Ocean and Environment, University of Delaware Lewes, DE, USA
                [4] 4College of Earth, Ocean and Atmospheric Sciences, Oregon State University OR, USA
                [5] 5Department of Oceanography, University of Hawai'i and Manoa Honolulu, HI, USA
                [6] 6Marine and Environmental Biology, University of Southern California Los Angeles, CA, USA
                [7] 7Graduate School of Oceanography, University of Rhode Island Narragansett, RI, USA
                [8] 8Chesapeake Biological Laboratory, University of Maryland Center for Environmental Sciences Solomons, MD, USA
                [9] 9Department of Biology, University of Houston Clear Lake TX, USA
                [10] 10Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution Woods Hole, MA, USA
                [11] 11Global Undersea Research Unit, University of Alaska Fairbanks Moss Landing, CA, USA
                Author notes

                Edited by: Axel Schippers, Federal Institute for Geosciences and Natural Resources (BGR), Germany

                Reviewed by: Takuro Nunoura, Japan Agency for Marine-Earth Science & Technology, Japan; Jens Kallmeyer, Helmholtz Zentrum Potsdam-GFZ, Germany; Gordon Webster, Cardiff University, UK

                *Correspondence: Beth N. Orcutt, Bigelow Laboratory for Ocean Sciences, 60 Bigelow Drive, PO Box 380, East Boothbay, ME 04544, USA e-mail: borcutt@ 123456bigelow.org

                This article was submitted to Frontiers in Extreme Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2013.00189
                3708129
                23874326
                06499a26-e5e8-48bb-b83f-8826c1f577ba
                Copyright © 2013 Orcutt, LaRowe, Biddle, Colwell, Glazer, Reese, Kirkpatrick, Lapham, Mills, Sylvan, Wankel and Wheat.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 20 April 2013
                : 20 June 2013
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 201, Pages: 15, Words: 14334
                Categories
                Microbiology
                Review Article

                Microbiology & Virology
                deep biosphere,iodp,biogeochemistry,sediment,oceanic crust,c-debi,subsurface microbiology

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