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      Archaea dominate oxic subseafloor communities over multimillion-year time scales

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          Abstract

          Archaea have dominated oxic subseafloor communities for millions of years by minimizing energy loss.

          Abstract

          Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.

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          Most cited references52

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          Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.

          Nitrification, the microbial oxidation of ammonia to nitrite and nitrate, occurs in a wide variety of environments and plays a central role in the global nitrogen cycle. Catalyzed by the enzyme ammonia monooxygenase, the ability to oxidize ammonia was previously thought to be restricted to a few groups within the beta- and gamma-Proteobacteria. However, recent metagenomic studies have revealed the existence of unique ammonia monooxygenase alpha-subunit (amoA) genes derived from uncultivated, nonextremophilic Crenarchaeota. Here, we report molecular evidence for the widespread presence of ammonia-oxidizing archaea (AOA) in marine water columns and sediments. Using PCR primers designed to specifically target archaeal amoA, we find AOA to be pervasive in areas of the ocean that are critical for the global nitrogen cycle, including the base of the euphotic zone, suboxic water columns, and estuarine and coastal sediments. Diverse and distinct AOA communities are associated with each of these habitats, with little overlap between water columns and sediments. Within marine sediments, most AOA sequences are unique to individual sampling locations, whereas a small number of sequences are evidently cosmopolitan in distribution. Considering the abundance of nonextremophilic archaea in the ocean, our results suggest that AOA may play a significant, but previously unrecognized, role in the global nitrogen cycle.
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            Archaeal dominance in the mesopelagic zone of the Pacific Ocean.

            The ocean's interior is Earth's largest biome. Recently, cultivation-independent ribosomal RNA gene surveys have indicated a potential importance for archaea in the subsurface ocean. But quantitative data on the abundance of specific microbial groups in the deep sea are lacking. Here we report a year-long study of the abundance of two specific archaeal groups (pelagic euryarchaeota and pelagic crenarchaeota) in one of the ocean's largest habitats. Monthly sampling was conducted throughout the water column (surface to 4,750 m) at the Hawai'i Ocean Time-series station. Below the euphotic zone (> 150 m), pelagic crenarchaeota comprised a large fraction of total marine picoplankton, equivalent in cell numbers to bacteria at depths greater than 1,000 m. The fraction of crenarchaeota increased with depth, reaching 39% of total DNA-containing picoplankton detected. The average sum of archaea plus bacteria detected by rRNA-targeted fluorescent probes ranged from 63 to 90% of total cell numbers at all depths throughout our survey. The high proportion of cells containing significant amounts of rRNA suggests that most pelagic deep-sea microorganisms are metabolically active. Furthermore, our results suggest that the global oceans harbour approximately 1.3 x 10(28) archaeal cells, and 3.1 x 10(28) bacterial cells. Our data suggest that pelagic crenarchaeota represent one of the ocean's single most abundant cell types.
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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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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                June 2019
                19 June 2019
                : 5
                : 6
                : eaaw4108
                Affiliations
                [1 ]Department of Earth and Environmental Sciences, Paleontology & Geobiology, Ludwig-Maximilians-Universität München, 80333 Munich, Germany.
                [2 ]Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
                [3 ]College of Earth, Ocean, and Environment, University of Delaware, Lewes, DE 19958, USA.
                [4 ]Graduate School of Oceanography, University of Rhode Island, Narragansett, RI 02882, USA.
                [5 ]Department of Earth and Environment, Boston University, Boston, MA 02215, USA.
                [6 ]GeoBio-Center, Ludwig-Maximilians-Universität München, 80333 Munich, Germany.
                Author notes
                [* ]Corresponding author. Email: w.orsi@ 123456lrz.uni-muenchen.de
                Author information
                http://orcid.org/0000-0002-7724-8931
                http://orcid.org/0000-0002-7683-0225
                http://orcid.org/0000-0002-9454-0563
                http://orcid.org/0000-0001-8704-1339
                http://orcid.org/0000-0002-2293-3827
                http://orcid.org/0000-0003-0627-5788
                http://orcid.org/0000-0002-7688-4098
                http://orcid.org/0000-0002-4094-5637
                Article
                aaw4108
                10.1126/sciadv.aaw4108
                6584578
                31223656
                5b7b288e-df61-4f47-a992-d648856170d6
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 18 December 2018
                : 10 May 2019
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: NSF-OCE-1433150
                Funded by: doi http://dx.doi.org/10.13039/100013505, Center for Dark Energy Biosphere Investigations;
                Award ID: OCE-0939564
                Funded by: doi http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: OR 417/1-1
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Ecology
                Custom metadata
                Ariel Francis Banag

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