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      Single cell analyses reveal contrasting life strategies of the two main nitrifiers in the ocean

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          Abstract

          Nitrification, the oxidation of ammonia via nitrite to nitrate, is a key process in marine nitrogen (N) cycling. Although oceanic ammonia and nitrite oxidation are balanced, ammonia-oxidizing archaea (AOA) vastly outnumber the main nitrite oxidizers, the bacterial Nitrospinae. The ecophysiological reasons for this discrepancy in abundance are unclear. Here, we compare substrate utilization and growth of Nitrospinae to AOA in the Gulf of Mexico. Based on our results, more than half of the Nitrospinae cellular N-demand is met by the organic-N compounds urea and cyanate, while AOA mainly assimilate ammonium. Nitrospinae have, under in situ conditions, around four-times higher biomass yield and five-times higher growth rates than AOA, despite their ten-fold lower abundance. Our combined results indicate that differences in mortality between Nitrospinae and AOA, rather than thermodynamics, biomass yield and cell size, determine the abundances of these main marine nitrifiers. Furthermore, there is no need to invoke yet undiscovered, abundant nitrite oxidizers to explain nitrification rates in the ocean.

          Abstract

          Ammonia oxidizing archaea and Nitrospinae are the main known nitrifiers in the ocean, but the much greater abundance of the former is puzzling. Here, the authors show that differences in mortality, rather than thermodynamics, cell size or biomass yield, explain the discrepancy, without the need to invoke yet undiscovered, abundant nitrite oxidizers.

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          Most cited references65

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            The microbial nitrogen-cycling network

            Nitrogen is an essential component of all living organisms and the main nutrient limiting life on our planet. By far, the largest inventory of freely accessible nitrogen is atmospheric dinitrogen, but most organisms rely on more bioavailable forms of nitrogen, such as ammonium and nitrate, for growth. The availability of these substrates depends on diverse nitrogen-transforming reactions that are carried out by complex networks of metabolically versatile microorganisms. In this Review, we summarize our current understanding of the microbial nitrogen-cycling network, including novel processes, their underlying biochemical pathways, the involved microorganisms, their environmental importance and industrial applications.
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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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                Author and article information

                Contributors
                kkitzing@mpi-bremen.de
                hmarchan@mpi-bremen.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                7 February 2020
                7 February 2020
                2020
                : 11
                : 767
                Affiliations
                [1 ]ISNI 0000 0004 0491 3210, GRID grid.419529.2, Max Planck Institute for Marine Microbiology, ; 28359 Bremen, Germany
                [2 ]ISNI 0000 0001 2286 1424, GRID grid.10420.37, Centre for Microbiology and Environmental Systems Science, Division of Microbial Ecology, , University of Vienna, ; 1090 Vienna, Austria
                [3 ]ISNI 0000 0001 0728 0170, GRID grid.10825.3e, Department of Biology, , University of Southern Denmark, ; 5230 Odense, Denmark
                [4 ]ISNI 0000 0001 2097 4943, GRID grid.213917.f, School of Biological Sciences, Georgia Institute of Technology, ; Atlanta, GA 30332–0230 USA
                [5 ]ISNI 0000 0001 2286 1424, GRID grid.10420.37, The Comammox Research Platform, , University of Vienna, ; 1090 Vienna, Austria
                [6 ]ISNI 0000 0001 2286 1424, GRID grid.10420.37, Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna, ; 1090 Vienna, Austria
                [7 ]ISNI 0000 0001 0742 471X, GRID grid.5117.2, Center for Microbial Communities, Department of Chemistry and Bioscience, , Aalborg University, ; 9220 Aalborg, Denmark
                Author information
                http://orcid.org/0000-0001-7382-7103
                http://orcid.org/0000-0002-1482-9165
                http://orcid.org/0000-0003-3479-0197
                http://orcid.org/0000-0001-7344-302X
                http://orcid.org/0000-0002-9778-7684
                Article
                14542
                10.1038/s41467-020-14542-3
                7005884
                32034151
                326b6873-6803-44f7-b0a4-a811369bea57
                © The Author(s) 2020

                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
                : 14 June 2019
                : 17 January 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100002428, Austrian Science Fund (Fonds zur Förderung der Wissenschaftlichen Forschung);
                Award ID: W 1257
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100004189, Max-Planck-Gesellschaft (Max Planck Society);
                Funded by: European Research Council Advanced Grant (ERC-AG), funding nr. 294343
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                ecology,environmental microbiology,physiology,biogeochemistry
                Uncategorized
                ecology, environmental microbiology, physiology, biogeochemistry

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