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      Ammonia‐oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

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          Summary

          Ammonia‐oxidizing archaea (AOA) constitute a considerable fraction of microbial biomass in the global ocean, comprising 20%–40% of the ocean's prokaryotic plankton. However, it remains enigmatic to what extent these chemolithoautotrophic archaea release dissolved organic carbon (DOC). A combination of targeted and untargeted metabolomics was used to characterize the exometabolomes of three model AOA strains of the Nitrosopumilus genus. Our results indicate that marine AOA exude a suite of organic compounds with potentially varying reactivities, dominated by nitrogen‐containing compounds. A significant fraction of the released dissolved organic matter (DOM) consists of labile compounds, which typically limit prokaryotic heterotrophic activity in open ocean waters, including amino acids, thymidine and B vitamins. Amino acid release rates corresponded with ammonia oxidation activity and the three Nitrosopumilus strains predominantly released hydrophobic amino acids, potentially as a result of passive diffusion. Despite the low contribution of DOC released by AOA (~0.08%–1.05%) to the heterotrophic prokaryotic carbon demand, the release of physiologically relevant metabolites could be crucial for microbes that are auxotrophic for some of these compounds, including members of the globally abundant and ubiquitous SAR11 clade.

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          The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

          ABSTRACT Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and “Candidatus Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.
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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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              Genome streamlining in a cosmopolitan oceanic bacterium.

              The SAR11 clade consists of very small, heterotrophic marine alpha-proteobacteria that are found throughout the oceans, where they account for about 25% of all microbial cells. Pelagibacter ubique, the first cultured member of this clade, has the smallest genome and encodes the smallest number of predicted open reading frames known for a free-living microorganism. In contrast to parasitic bacteria and archaea with small genomes, P. ubique has complete biosynthetic pathways for all 20 amino acids and all but a few cofactors. P. ubique has no pseudogenes, introns, transposons, extrachromosomal elements, or inteins; few paralogs; and the shortest intergenic spacers yet observed for any cell.
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                Author and article information

                Contributors
                barbara.bayer@outlook.com
                Journal
                Environ Microbiol
                Environ. Microbiol
                10.1111/(ISSN)1462-2920
                EMI
                Environmental Microbiology
                John Wiley & Sons, Inc. (Hoboken, USA )
                1462-2912
                1462-2920
                06 August 2019
                November 2019
                : 21
                : 11 ( doiID: 10.1111/emi.v21.11 )
                : 4062-4075
                Affiliations
                [ 1 ] Division of Bio‐Oceanography, Department of Limnology and Bio‐Oceanography, Centre of Functional Ecology University of Vienna Vienna 1090 Austria
                [ 2 ] International Atomic Energy Agency – Environment Laboratories Radioecology Laboratory, 98000 Monaco Monaco
                [ 3 ] ICBM‐MPI Bridging Group for Marine Geochemistry University of Oldenburg, 26129 Oldenburg Germany
                [ 4 ] Department of Marine Microbiology and Biogeochemistry NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, 1790 AB Den Burg, Texel The Netherlands
                Author notes
                [*] [* ]For correspondence. E‐mail barbara.bayer@ 123456outlook.com ; Tel: +4369919053434.
                Author information
                https://orcid.org/0000-0003-3968-5804
                https://orcid.org/0000-0002-2223-2852
                Article
                EMI14755
                10.1111/1462-2920.14755
                6899801
                31336026
                44c664f2-3693-4b6a-88f6-94d880e3f743
                © 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 May 2019
                : 17 July 2019
                : 18 July 2019
                Page count
                Figures: 6, Tables: 2, Pages: 14, Words: 10741
                Funding
                Funded by: Austrian Science Fund , open-funder-registry 10.13039/501100002428;
                Award ID: P28781‐B21
                Award ID: W1257‐B20
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                November 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.2 mode:remove_FC converted:05.12.2019

                Microbiology & Virology
                Microbiology & Virology

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