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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Microbiol. | doi: 10.3389/fmicb.2019.01571

Ammonia oxidation by the arctic terrestrial thaumarchaeote Ca. Nitrosocosmicus arcticus is stimulated by increasing temperatures

 Ricardo J. Alves1, 2,  Melina Kerou2, Anna Zappe2, 3, Romana Bittner2,  Sophie S. Abby4,  Heiko Schmidt3, Kevin Pfeifer2, 5 and  Christa Schleper2*
  • 1Climate and Ecosystem Science Division, Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, United States
  • 2Department of Ecogenomics and Systems Biology, Faculty of Sciences, University of Vienna, Austria
  • 3Max F. Perutz Laboratories GmbH, Austria
  • 4Université Grenoble Alpes, France
  • 5University of Natural Resources and Life Sciences Vienna, Austria

Climate change is causing arctic regions to warm disproportionally faster than those at lower latitudes, leading to alterations in carbon and nitrogen cycling, and potentially higher greenhouse gas emissions. It is thus increasingly important to better characterize the microorganisms driving arctic biogeochemical processes and their potential responses to changing conditions. Here, we describe a novel thaumarchaeon enriched from an arctic soil, Candidatus Nitrosocosmicus arcticus strain Kfb, which has been maintained for seven years in stable laboratory cultures as an aerobic ammonia oxidizer with ammonium or urea as substrates. Genomic analyses show that this organism harbors all genes involved in ammonia oxidation and in carbon fixation via the 3-hydroxypropionate/4-hydroxybutyrate cycle, characteristic of all AOA, as well as those for urea utilization and potentially also for heterotrophic metabolism, similar to other AOA. Although Ca. N. arcticus oxidizes ammonia optimally at 20 to 28°C, it showed growth at faster rates at 4 °C without detectable nitrite production. Growth independent of ammonia oxidation was observed at lower temperatures in multiple cultures from different inocula and at different enrichment stages, based on amoA and 16S rRNA gene quantification, but could not be induced systematically in the laboratory. These results add to cumulating evidence for a greater metabolic and physiological versatility of AOA and suggest that increasing temperatures might drastically affect archaeal function in arctic soils, potentially by stimulating nitrification activity of archaeal populations that thrive on alternative metabolism(s) under colder conditions.

Keywords: ammonia oxidation, Archaea, Thaumarchaea, Nitrification, Arctic ecosystems, Soil Microbiology

Received: 04 Apr 2019; Accepted: 24 Jun 2019.

Edited by:

Satoshi Tsuneda, Waseda University, Japan

Reviewed by:

Lisa Y. Stein, University of Alberta, Canada
Hidetoshi Urakawa, Florida Gulf Coast University, United States  

Copyright: © 2019 Alves, Kerou, Zappe, Bittner, Abby, Schmidt, Pfeifer and Schleper. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Christa Schleper, Department of Ecogenomics and Systems Biology, Faculty of Sciences, University of Vienna, Vienna, 1090, Vienna, Austria, christa.schleper@univie.ac.at