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      A robust nitrifying community in a bioreactor at 50 °C opens up the path for thermophilic nitrogen removal

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          Abstract

          <p class="first" id="d6376468e275">The increasing production of nitrogen-containing fertilizers is crucial to meet the global food demand, yet high losses of reactive nitrogen associated with the food production/consumption chain progressively deteriorate the natural environment. Currently, mesophilic nitrogen-removing microbes eliminate nitrogen from wastewaters. Although thermophilic nitrifiers have been separately enriched from natural environments, no bioreactors are described that couple these processes for the treatment of nitrogen in hot wastewaters. Samples from composting facilities were used as inoculum for the batch-wise enrichment of thermophilic nitrifiers (350 days). Subsequently, the enrichments were transferred to a bioreactor to obtain a stable, high-rate nitrifying process (560 days). The community contained up to 17% ammonia-oxidizing archaea (AOAs) closely related to ‘ <i>Candidatus</i> Nitrososphaera gargensis', and 25% nitrite-oxidizing bacteria (NOBs) related to <i>Nitrospira calida</i>. Incorporation of <sup>13</sup>C-derived bicarbonate into the respective characteristic membrane lipids during nitrification supported their activity as autotrophs. Specific activities up to 198±10 and 894±81 mg N g <sup>−1</sup> VSS per day for AOAs and NOBs were measured, where NOBs were 33% more sensitive to free ammonia. The NOBs were extremely sensitive to free nitrous acid, whereas the AOAs could only be inhibited by high nitrite concentrations, independent of the free nitrous acid concentration. The observed difference in product/substrate inhibition could facilitate the development of NOB inhibition strategies to achieve more cost-effective processes such as deammonification. This study describes the enrichment of autotrophic thermophilic nitrifiers from a nutrient-rich environment and the successful operation of a thermophilic nitrifying bioreactor for the first time, facilitating opportunities for thermophilic nitrogen removal biotechnology. </p>

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          Most cited references 41

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          The habitat and nature of early life.

          Earth is over 4,500 million years old. Massive bombardment of the planet took place for the first 500-700 million years, and the largest impacts would have been capable of sterilizing the planet. Probably until 4,000 million years ago or later, occasional impacts might have heated the ocean over 100 degrees C. Life on Earth dates from before about 3,800 million years ago, and is likely to have gone through one or more hot-ocean 'bottlenecks'. Only hyperthermophiles (organisms optimally living in water at 80-110 degrees C) would have survived. It is possible that early life diversified near hydrothermal vents, but hypotheses that life first occupied other pre-bottleneck habitats are tenable (including transfer from Mars on ejecta from impacts there). Early hyperthermophile life, probably near hydrothermal systems, may have been non-photosynthetic, and many housekeeping proteins and biochemical processes may have an original hydrothermal heritage. The development of anoxygenic and then oxygenic photosynthesis would have allowed life to escape the hydrothermal setting. By about 3,500 million years ago, most of the principal biochemical pathways that sustain the modern biosphere had evolved, and were global in scope.
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            Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol.

            The widespread occurrence and diversity of ammonia oxidizing Archaea suggests their contribution to the nitrogen cycle is of global significance. Their distribution appeared limited to low- and moderate-temperature environments until the recent finding of a diagnostic membrane lipid, crenarchaeol, in terrestrial hot springs. We report here the cultivation of a thermophilic nitrifier ('Candidatus Nitrosocaldus yellowstonii'), an autotrophic crenarchaeote growing up to 74 degrees C by aerobic ammonia oxidation. The major core lipid of this archaeon growing at 72 degrees C is crenarchaeol, providing the first direct evidence for its synthesis by a thermophile. These findings greatly extend the upper temperature limit of nitrification and document that the capacity for ammonia oxidation is broadly distributed among the Crenarchaeota.
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              A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring.

              The recent discovery of ammonia-oxidizing archaea (AOA) dramatically changed our perception of the diversity and evolutionary history of microbes involved in nitrification. In this study, a moderately thermophilic (46 degrees C) ammonia-oxidizing enrichment culture, which had been seeded with biomass from a hot spring, was screened for ammonia oxidizers. Although gene sequences for crenarchaeotal 16S rRNA and two subunits of the ammonia monooxygenase (amoA and amoB) were detected via PCR, no hints for known ammonia-oxidizing bacteria were obtained. Comparative sequence analyses of these gene fragments demonstrated the presence of a single operational taxonomic unit and thus enabled the assignment of the amoA and amoB sequences to the respective 16S rRNA phylotype, which belongs to the widely distributed group I.1b (soil group) of the Crenarchaeota. Catalyzed reporter deposition (CARD)-FISH combined with microautoradiography (MAR) demonstrated metabolic activity of this archaeon in the presence of ammonium. This finding was corroborated by the detection of amoA gene transcripts in the enrichment. CARD-FISH/MAR showed that the moderately thermophilic AOA is highly active at 0.14 and 0.79 mM ammonium and is partially inhibited by a concentration of 3.08 mM. The enriched AOA, which is provisionally classified as "Candidatus Nitrososphaera gargensis," is the first described thermophilic ammonia oxidizer and the first member of the crenarchaeotal group I.1b for which ammonium oxidation has been verified on a cellular level. Its preference for thermophilic conditions reinvigorates the debate on the thermophilic ancestry of AOA.
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                Author and article information

                Journal
                The ISME Journal
                ISME J
                Springer Nature
                1751-7362
                1751-7370
                September 2016
                February 19 2016
                September 2016
                : 10
                : 9
                : 2293-2303
                Article
                10.1038/ismej.2016.8
                4989323
                26894446
                © 2016

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