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      Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle

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          Summary paragraph

          Nitrification, the oxidation of ammonia (NH 3) via nitrite (NO 2 -) to nitrate (NO 3 -), is a key process of the biogeochemical nitrogen cycle. For decades, ammonia and nitrite oxidation were thought to be separately catalyzed by ammonia-oxidizing bacteria (AOB) and archaea (AOA), and by nitrite-oxidizing bacteria (NOB). The recent discovery of complete ammonia oxidizers (comammox) in the NOB genus Nitrospira 1, 2, which alone convert ammonia to nitrate, raised questions about the ecological niches where comammox Nitrospira successfully compete with canonical nitrifiers. Here we isolated the first pure culture of a comammox bacterium, Nitrospira inopinata, and show that it is adapted to slow growth in oligotrophic and dynamic habitats based on a high affinity for ammonia, low maximum rate of ammonia oxidation, high growth yield compared to canonical nitrifiers, and genomic potential for alternative metabolisms. The nitrification kinetics of four AOA from soil and hot springs were determined for comparison. Their surprisingly poor substrate affinities and lower growth yields reveal that, in contrast to earlier assumptions, not all AOA are most competitive in strongly oligotrophic environments and that N. inopinata has the highest substrate affinity of all analyzed ammonia oxidizer isolates except the marine AOA Nitrosopumilus maritimus SCM1 3. These results suggest a role of comammox organisms for nitrification under oligotrophic and dynamic conditions.

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          Short-term assay of soil urease activity using colorimetric determination of ammonium

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            Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil.

            Genes of archaea encoding homologues of ammonia monooxygenases have been found on a widespread basis and in large amounts in almost all terrestrial and marine environments, indicating that ammonia oxidizing archaea (AOA) might play a major role in nitrification on Earth. However, only one pure isolate of this group from a marine environment has so far been obtained, demonstrating archaeal ammonia oxidation coupled with autotrophic growth similar to the bacterial counterparts. Here we describe the cultivation and isolation of an AOA from soil. It grows on ammonia or urea as an energy source and is capable of using higher ammonia concentrations than the marine isolate, Nitrosopumilus maritimus. Surprisingly, although it is able to grow chemolithoautotrophically, considerable growth rates of this strain are obtained only upon addition of low amounts of pyruvate or when grown in coculture with bacteria. Our findings expand the recognized metabolic spectrum of AOA and help explain controversial results obtained in the past on the activity and carbon assimilation of these globally distributed organisms.
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              Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation.

              Archaea of the phylum Thaumarchaeota are among the most abundant prokaryotes on Earth and are widely distributed in marine, terrestrial, and geothermal environments. All studied Thaumarchaeota couple the oxidation of ammonia at extremely low concentrations with carbon fixation. As the predominant nitrifiers in the ocean and in various soils, ammonia-oxidizing archaea contribute significantly to the global nitrogen and carbon cycles. Here we provide biochemical evidence that thaumarchaeal ammonia oxidizers assimilate inorganic carbon via a modified version of the autotrophic hydroxypropionate/hydroxybutyrate cycle of Crenarchaeota that is far more energy efficient than any other aerobic autotrophic pathway. The identified genes of this cycle were found in the genomes of all sequenced representatives of the phylum Thaumarchaeota, indicating the environmental significance of this efficient CO2-fixation pathway. Comparative phylogenetic analysis of proteins of this pathway suggests that the hydroxypropionate/hydroxybutyrate cycle emerged independently in Crenarchaeota and Thaumarchaeota, thus supporting the hypothesis of an early evolutionary separation of both archaeal phyla. We conclude that high efficiency of anabolism exemplified by this autotrophic cycle perfectly suits the lifestyle of ammonia-oxidizing archaea, which thrive at a constantly low energy supply, thus offering a biochemical explanation for their ecological success in nutrient-limited environments.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                31 July 2017
                23 August 2017
                14 September 2017
                23 February 2018
                : 549
                : 7671
                : 269-272
                Affiliations
                [1 ]Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network Chemistry meets Microbiology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
                [2 ]Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences, Leninsky Ave. 33, bld. 2, 119071 Moscow, Russia
                [3 ]Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, Fredrik Bajers Vej 7H, 9220 Aalborg, Denmark
                [4 ]Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Building, Edmonton, AB T6G 2E9, Canada
                Author notes
                [* ]Correspondence and requests for materials should be addressed to Holger Daims, Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria, daims@ 123456microbial-ecology.net , Phone: +43 1 4277 76604, Fax: +43 1 4277 825701
                Article
                EMS73579
                10.1038/nature23679
                5600814
                28847001
                a694962d-0192-4efa-bd7e-e56ad7f9e4be

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