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      An Improved Method for Extracting Viruses From Sediment: Detection of Far More Viruses in the Subseafloor Than Previously Reported

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          Abstract

          Viruses are the most abundant biological entities on Earth and perform essential ecological functions in aquatic environments by mediating biogeochemical cycling and lateral gene transfer. Cellular life as well as viruses have been found in deep subseafloor sediment. However, the study of deep sediment viruses has been hampered by the complexities involved in efficiently extracting viruses from a sediment matrix. Here, we developed a new method for the extraction of viruses from sediment based on density separation using a Nycodenz density step gradient. The density separation method resulted in up to 2 orders of magnitude greater recovery of viruses from diverse subseafloor sediments compared to conventional methods. The density separation method also showed more consistent performance between samples of different sediment lithology, whereas conventional virus extraction methods were highly inconsistent. Using this new method, we show that previously published virus counts have underestimated viral abundances by up to 2 orders of magnitude. These improvements suggest that the carbon contained within viral biomass in the subseafloor environment may potentially be revised upward to 0.8–3.7 Gt from current estimates of 0.2 Gt. The vastly improved recovery of viruses indicate that viruses represent a far larger pool of organic carbon in subseafloor environments than previously estimated.

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          Most cited references 61

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          Viruses in the sea.

          Viruses exist wherever life is found. They are a major cause of mortality, a driver of global geochemical cycles and a reservoir of the greatest genetic diversity on Earth. In the oceans, viruses probably infect all living things, from bacteria to whales. They affect the form of available nutrients and the termination of algal blooms. Viruses can move between marine and terrestrial reservoirs, raising the spectre of emerging pathogens. Our understanding of the effect of viruses on global systems and processes continues to unfold, overthrowing the idea that viruses and virus-mediated processes are sidebars to global processes.
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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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              Viruses manipulate the marine environment.

              Marine viruses affect Bacteria, Archaea and eukaryotic organisms and are major components of the marine food web. Most studies have focused on their role as predators and parasites, but many of the interactions between marine viruses and their hosts are much more complicated. A series of recent studies has shown that viruses have the ability to manipulate the life histories and evolution of their hosts in remarkable ways, challenging our understanding of this almost invisible world.
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                Author and article information

                Affiliations
                1Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology , Yokosuka, Japan
                2Geomicrobiology Group, Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology , Nankoku, Japan
                3Research and Development Center for Submarine Resources, Japan Agency for Marine-Earth Science and Technology , Yokosuka, Japan
                4Research and Development Center for Ocean Drilling Science, Japan Agency for Marine-Earth Science and Technology , Yokohama, Japan
                5Earth-Life Science Institute, Tokyo Institute of Technology , Tokyo, Japan
                Author notes

                Edited by: Dawn Cardace, The University of Rhode Island, United States

                Reviewed by: Kenneth Stedman, Portland State University, United States; Rui Zhang, Xiamen University, China

                *Correspondence: Donald Pan, donald.pan@ 123456jamstec.go.jp

                Present address: Donald Pan, Yuki Morono, and Ken Takai, X-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan; Fumio Inagaki, Mantle Drilling Promotion Office (MDP), Institute for Marine-Earth Exploration and Engineering (MarE3), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokohama, Japan

                This article was submitted to Extreme Microbiology, a section of the journal Frontiers in Microbiology

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                29 April 2019
                2019
                : 10
                10.3389/fmicb.2019.00878
                6501758
                Copyright © 2019 Pan, Morono, Inagaki and Takai.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Counts
                Figures: 5, Tables: 0, Equations: 0, References: 65, Pages: 11, Words: 0
                Funding
                Funded by: Japan Society for the Promotion of Science 10.13039/501100001691
                Award ID: 16H07489
                Categories
                Microbiology
                Methods

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