Cold Adapted Nitrosospira sp.: A Potential Crucial Contributor of Ammonia Oxidation in Cryosols of Permafrost-Affected Landscapes in Northeast Siberia

Abstract

Permafrost-affected landscape soils are rich in organic matter and contain a high fraction of organic nitrogen, but much of this organic matter remains inaccessible due to nitrogen limitation. Microbial nitrification is a key process in the nitrogen cycle, controlling the availability of dissolved inorganic nitrogen (DIN) such as ammonium and nitrate. In this study, we investigate the microbial diversity of canonical nitrifiers and their potential nitrifying activity in the active layer of different Arctic cryosols in the Lena River Delta in North-East Siberia. These cryosols are located on Samoylov Island, which has two geomorphological landscapes with mineral soils in the modern floodplain and organic-rich soils in the low-centered polygonal tundra of the Holocene river terrace. Microcosm incubations show that the highest potential ammonia oxidation rates are found in low organic soils, and the rates depend on organic matter content and quality, vegetation cover, and water content. As shown by 16S rRNA amplicon sequencing, nitrifiers represented 0.6% to 6.2% of the total microbial community. More than 50% of the nitrifiers belonged to the genus Nitrosospira. Based on PCR amoA analysis, ammonia-oxidizing bacteria (AOB) were found in nearly all soil types, whereas ammonia-oxidizing archaea (AOA) were only detected in low-organic soils. In cultivation-based approaches, mainly Nitrosospira-like AOB were enriched and characterized as psychrotolerant, with temperature optima slightly above 20 °C. This study suggests a ubiquitous distribution of ammonia-oxidizing microorganisms (bacteria and archaea) in permafrost-affected landscapes of Siberia with cold-adapted AOB, especially of the genus Nitrosospira, as potentially crucial ammonia oxidizers in the cryosols.

Microorganisms as bio‐filters to mitigate greenhouse gas emissions from high‐altitude permafrost revealed by nanopore‐based metagenomics

“…Nitrosospira is a typical AOB and lives in various environments [54,55]. Although typical Nitrosospira like those in domestic wastewater treatment plants prefers warmer growing environment (25°C to 30°C) [56], a recent study had found certain species of Nitrosospira could adapt and enrich in the cold environment [53], and our results consolidated this finding. Additionally, Methylomonas is the plausible AOB in permafrost.…”

“…Nitrosospira were the active ammonia‐oxidizing bacteria (AOB) within the community of thawed permafrost, while no AOB could be identified in frozen permafrost soil, suggesting clear repression of AOB activity in frozen permafrost. We could not detect active ammonia‐oxidizing archaea (AOA) in permafrost and such AOB‐dominated nitrogen metabolism was also observed in research in cold environments like high‐altitude lakes [52] and permafrost in northeast Siberia [53]. Nitrosospira is a typical AOB and lives in various environments [54,55].…”

Seasonal nitrogen fluxes of the Lena River Delta

“…There are some studies on N cycling in permafrost-affected soils (e.g., Biasi et al 2005 ; Stewart et al 2014 ; Sanders et al 2019 ; Horn and Hetz 2021 ). Recent newer studies focus on the potential nitrous oxide (N 2 O) emissions from permafrost-affected soils (reviewed by Voigt et al ( 2020 )) and the input of C and N into the fluvial system (Hugelius et al 2020 ; Pastor et al 2020 ).…”

Biogeochemical responses over 37 years to manipulation of phosphorus concentrations in an Arctic river: The Upper Kuparuk River Experiment

“…Increasing nitrate flux supports the hypothesis that permafrost thaw routes subsurface flow through deeper, mineral‐rich soil layers (Bowden et al, 2008; Keller, Blum, & Kling, 2010), providing access to biologically available N released with thaw (Keuper et al, 2012). Nitrification is widespread in Arctic soils and rivers (Harms et al, 2016; Lafrenière, Louiseize, & Lamoureaux, 2017; Sanders, Fiencke, Hüpeden, Pfeiffer, & Spieck, 2019) and can proceed rapidly (Peterson et al, 2001; Snyder & Bowden, 2014). While nitrate uptake is important in Arctic streams, the portion of the nitrate pool that is removed by uptake per unit time is relatively small, allowing nitrate to travel further downstream (Peterson et al, 2001).…”