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

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...

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Main Authors: Alves, Ricardo J Eloy, Kerou, Melina, Zappe, Anna, Bittner, Romana, Abby, Sophie S, Schmidt, Heiko A, Pfeifer, Kevin, Schleper, Christa
Format: Article in Journal/Newspaper
Language:unknown
Published: eScholarship, University of California 2019
Subjects:
Online Access:https://escholarship.org/uc/item/8k44t81j
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spelling ftcdlib:oai:escholarship.org:ark:/13030/qt8k44t81j 2024-01-07T09:41:00+01:00 Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures Alves, Ricardo J Eloy Kerou, Melina Zappe, Anna Bittner, Romana Abby, Sophie S Schmidt, Heiko A Pfeifer, Kevin Schleper, Christa 1571 2019-01-01 application/pdf https://escholarship.org/uc/item/8k44t81j unknown eScholarship, University of California qt8k44t81j https://escholarship.org/uc/item/8k44t81j public Frontiers in Microbiology, vol 10, iss JULY Biological Sciences Ecology Climate Action ammonia oxidation archaea thaumarchaeota nitrification arctic ecosystems soil microbiology Environmental Science and Management Soil Sciences Microbiology Medical microbiology article 2019 ftcdlib 2023-12-11T19:07:21Z 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. Article in Journal/Newspaper Arctic Climate change University of California: eScholarship Arctic
institution Open Polar
collection University of California: eScholarship
op_collection_id ftcdlib
language unknown
topic Biological Sciences
Ecology
Climate Action
ammonia oxidation
archaea
thaumarchaeota
nitrification
arctic ecosystems
soil microbiology
Environmental Science and Management
Soil Sciences
Microbiology
Medical microbiology
spellingShingle Biological Sciences
Ecology
Climate Action
ammonia oxidation
archaea
thaumarchaeota
nitrification
arctic ecosystems
soil microbiology
Environmental Science and Management
Soil Sciences
Microbiology
Medical microbiology
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
topic_facet Biological Sciences
Ecology
Climate Action
ammonia oxidation
archaea
thaumarchaeota
nitrification
arctic ecosystems
soil microbiology
Environmental Science and Management
Soil Sciences
Microbiology
Medical microbiology
description 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.
format Article in Journal/Newspaper
author Alves, Ricardo J Eloy
Kerou, Melina
Zappe, Anna
Bittner, Romana
Abby, Sophie S
Schmidt, Heiko A
Pfeifer, Kevin
Schleper, Christa
author_facet Alves, Ricardo J Eloy
Kerou, Melina
Zappe, Anna
Bittner, Romana
Abby, Sophie S
Schmidt, Heiko A
Pfeifer, Kevin
Schleper, Christa
author_sort Alves, Ricardo J Eloy
title Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures
title_short Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures
title_full Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures
title_fullStr Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures
title_full_unstemmed Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures
title_sort ammonia oxidation by the arctic terrestrial thaumarchaeote candidatus nitrosocosmicus arcticus is stimulated by increasing temperatures
publisher eScholarship, University of California
publishDate 2019
url https://escholarship.org/uc/item/8k44t81j
op_coverage 1571
geographic Arctic
geographic_facet Arctic
genre Arctic
Climate change
genre_facet Arctic
Climate change
op_source Frontiers in Microbiology, vol 10, iss JULY
op_relation qt8k44t81j
https://escholarship.org/uc/item/8k44t81j
op_rights public
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