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Title: Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures

Abstract

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 enrichment 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 the capability for urea utilization and potentially also for heterotrophic metabolism, similar to other AOA. Ca. N. arcticus oxidizes ammonia optimally between 20 and 28°C, well above average temperatures in its native high arctic environment (-13-4°C). Ammonia oxidation rates were nevertheless much lower than those of most cultivated mesophilic AOA (20-45°C). Intriguingly, we repeatedly observed apparent faster growth rates (based on marker gene counts) at lower temperatures (4-8°C) but without detectable nitrite production. Together with potential metabolisms predicted from its genome content, thesemore » observations indicate that Ca. N. arcticus is not a strict chemolithotrophic ammonia oxidizer and add to cumulating evidence for a greater metabolic and physiological versatility of AOA. The physiology of Ca. N. arcticus suggests that increasing temperatures might drastically affect nitrification in arctic soils by stimulating archaeal ammonia oxidation.« less

Authors:
 [1];  [1];  [2];  [1];  [1];  [3];  [4];  [1]
  1. Univ. of Vienna, Vienna (Austria). Archaea Biology and Ecogenomics Division, Dept. of Ecogenomics and Systems Biology
  2. Univ. of Vienna, Vienna (Austria). Archaea Biology and Ecogenomics Division, Dept. of Ecogenomics and Systems Biology; Univ. of Vienna, Vienna (Austria). Medical Univ. of Vienna, Max F. Perutz Lab., Center for Integrative Bioinformatics Vienna
  3. Univ. of Vienna, Vienna (Austria). Medical Univ. of Vienna, Max F. Perutz Lab., Center for Integrative Bioinformatics Vienna
  4. Univ. of Vienna, Vienna (Austria). Archaea Biology and Ecogenomics Division, Dept. of Ecogenomics and Systems Biology; Univ. of Natural Resources and Life Sciences, Vienna (Austria). Inst. for Synthetic Bioarchitectures
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1571953
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 10; Journal Issue: JULY; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Alves, Ricardo J. Eloy, Kerou, Melina, Zappe, Anna, Bittner, Romana, Abby, Sophie S., Schmidt, Heiko A., Pfeifer, Kevin, and Schleper, Christa. Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures. United States: N. p., 2019. Web. doi:10.3389/fmicb.2019.01571.
Alves, Ricardo J. Eloy, Kerou, Melina, Zappe, Anna, Bittner, Romana, Abby, Sophie S., Schmidt, Heiko A., Pfeifer, Kevin, & Schleper, Christa. Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures. United States. doi:10.3389/fmicb.2019.01571.
Alves, Ricardo J. Eloy, Kerou, Melina, Zappe, Anna, Bittner, Romana, Abby, Sophie S., Schmidt, Heiko A., Pfeifer, Kevin, and Schleper, Christa. Wed . "Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures". United States. doi:10.3389/fmicb.2019.01571. https://www.osti.gov/servlets/purl/1571953.
@article{osti_1571953,
title = {Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures},
author = {Alves, Ricardo J. Eloy and Kerou, Melina and Zappe, Anna and Bittner, Romana and Abby, Sophie S. and Schmidt, Heiko A. and Pfeifer, Kevin and Schleper, Christa},
abstractNote = {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 enrichment 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 the capability for urea utilization and potentially also for heterotrophic metabolism, similar to other AOA. Ca. N. arcticus oxidizes ammonia optimally between 20 and 28°C, well above average temperatures in its native high arctic environment (-13-4°C). Ammonia oxidation rates were nevertheless much lower than those of most cultivated mesophilic AOA (20-45°C). Intriguingly, we repeatedly observed apparent faster growth rates (based on marker gene counts) at lower temperatures (4-8°C) but without detectable nitrite production. Together with potential metabolisms predicted from its genome content, these observations indicate that Ca. N. arcticus is not a strict chemolithotrophic ammonia oxidizer and add to cumulating evidence for a greater metabolic and physiological versatility of AOA. The physiology of Ca. N. arcticus suggests that increasing temperatures might drastically affect nitrification in arctic soils by stimulating archaeal ammonia oxidation.},
doi = {10.3389/fmicb.2019.01571},
journal = {Frontiers in Microbiology},
number = JULY,
volume = 10,
place = {United States},
year = {2019},
month = {7}
}

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