Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper

Marine nitrogen cycle ultimately depends on the biological responses of oceanic microbial communities. It indirectly regulates primary production and influences the strength of the biological pump, which contributes to the oceanic uptake of atmospheric carbon dioxide (CO2). As the microbial communit...

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Main Authors: Michał Grabski, Ewa Kotlarska, Aneta Łuczkiewicz, Konrad Hryniewicz, Grzegorz Węgrzyn, Beata Szymczycha
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Marine Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2025.1456825/full
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author Michał Grabski
Michał Grabski
Ewa Kotlarska
Aneta Łuczkiewicz
Konrad Hryniewicz
Grzegorz Węgrzyn
Beata Szymczycha
author_facet Michał Grabski
Michał Grabski
Ewa Kotlarska
Aneta Łuczkiewicz
Konrad Hryniewicz
Grzegorz Węgrzyn
Beata Szymczycha
author_sort Michał Grabski
collection DOAJ
description Marine nitrogen cycle ultimately depends on the biological responses of oceanic microbial communities. It indirectly regulates primary production and influences the strength of the biological pump, which contributes to the oceanic uptake of atmospheric carbon dioxide (CO2). As the microbial community structure and functional capacities remain underestimated in terms of temporal and geographical coverage in the Baltic Sea, our understanding of the nitrogen cycle with respect to ecosystem functioning and climate change is limited. Therefore, in this study, we investigated the seasonal and spatial structure of microbial community abundance involved in the nitrogen loss (denitrification, anammox), reduction processes (dissimilatory nitrate reduction (DNR), dissimilatory nitrite reduction to ammonium (DNRA), and oxidation process (nitrification) in the Baltic Proper (Bornholm Deep, Gdańsk Deep, and Gotland Deep). Specifically, we focused on waters below the halocline at depths ranging from 75 to 135 m, characterized by changeable oxygen conditions. The potential of selected nitrogen processes was resolved by mapping raw reads against nitrogen cycle genes identified in de novo assembled metagenomes. Taxonomic analysis of bacterial and archaeal communities, based on paired-end raw reads, revealed that nitrification, DNR, and denitrification potential were primarily associated with the Nitrosopumilaceae and Thioglobaceae families within these phyla. Ammonia oxidation products likely fueled the production of nitrous oxide (N2O), with nitric oxide reductase (NOR)—an enzyme encoded by the Thioglobaceae genome—being responsible for further reduction. Anammox-related genes were not present within sites, thus denitrification pathway enzymes, namely, NOR and N2O reductase (NOS) were responsible for nitrogen loss. At all sites, genes encoding nitrogen reduction enzymes were most abundant, while the presence of NOS encoding genes was found in Bacteroidetes and Proteobacteria phyla within all sites. Our findings revealed no significant spatial variation, suggesting that the studied ecosystem exhibits a consistent nitrogen processing capacity across different locations. However, seasonality emerged as a key factor, as changes in nutrient and oxygen conditions throughout the year significantly influence microbial activity and the associated nitrogen-cycling processes.
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spelling doaj-art-e06374282432421bb66a9b47c7af675a2025-02-10T05:16:03ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452025-02-011210.3389/fmars.2025.14568251456825Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic ProperMichał Grabski0Michał Grabski1Ewa Kotlarska2Aneta Łuczkiewicz3Konrad Hryniewicz4Grzegorz Węgrzyn5Beata Szymczycha6Department of Molecular Biology, Faculty of Biology, University of Gdańsk, Gdańsk, PolandDepartment of Marine Chemistry and Biochemistry, Institute of Oceanology of the Polish Academy of Sciences, Sopot, PolandDepartment of Genetics and Marine Biotechnology, Institute of Oceanology of the Polish Academy of Sciences, Sopot, PolandFaculty of Civil and Environmental Engineering, Gdańsk University of Technology, Gdańsk, PolandDepartment of Marketing and Quantitative Methods, Faculty of Management and Quality Science, Gdynia Maritime University, Gdynia, PolandDepartment of Molecular Biology, Faculty of Biology, University of Gdańsk, Gdańsk, PolandDepartment of Marine Chemistry and Biochemistry, Institute of Oceanology of the Polish Academy of Sciences, Sopot, PolandMarine nitrogen cycle ultimately depends on the biological responses of oceanic microbial communities. It indirectly regulates primary production and influences the strength of the biological pump, which contributes to the oceanic uptake of atmospheric carbon dioxide (CO2). As the microbial community structure and functional capacities remain underestimated in terms of temporal and geographical coverage in the Baltic Sea, our understanding of the nitrogen cycle with respect to ecosystem functioning and climate change is limited. Therefore, in this study, we investigated the seasonal and spatial structure of microbial community abundance involved in the nitrogen loss (denitrification, anammox), reduction processes (dissimilatory nitrate reduction (DNR), dissimilatory nitrite reduction to ammonium (DNRA), and oxidation process (nitrification) in the Baltic Proper (Bornholm Deep, Gdańsk Deep, and Gotland Deep). Specifically, we focused on waters below the halocline at depths ranging from 75 to 135 m, characterized by changeable oxygen conditions. The potential of selected nitrogen processes was resolved by mapping raw reads against nitrogen cycle genes identified in de novo assembled metagenomes. Taxonomic analysis of bacterial and archaeal communities, based on paired-end raw reads, revealed that nitrification, DNR, and denitrification potential were primarily associated with the Nitrosopumilaceae and Thioglobaceae families within these phyla. Ammonia oxidation products likely fueled the production of nitrous oxide (N2O), with nitric oxide reductase (NOR)—an enzyme encoded by the Thioglobaceae genome—being responsible for further reduction. Anammox-related genes were not present within sites, thus denitrification pathway enzymes, namely, NOR and N2O reductase (NOS) were responsible for nitrogen loss. At all sites, genes encoding nitrogen reduction enzymes were most abundant, while the presence of NOS encoding genes was found in Bacteroidetes and Proteobacteria phyla within all sites. Our findings revealed no significant spatial variation, suggesting that the studied ecosystem exhibits a consistent nitrogen processing capacity across different locations. However, seasonality emerged as a key factor, as changes in nutrient and oxygen conditions throughout the year significantly influence microbial activity and the associated nitrogen-cycling processes.https://www.frontiersin.org/articles/10.3389/fmars.2025.1456825/fullnitrificationDNRADNRdenitrificationanammoxmetagenome
spellingShingle Michał Grabski
Michał Grabski
Ewa Kotlarska
Aneta Łuczkiewicz
Konrad Hryniewicz
Grzegorz Węgrzyn
Beata Szymczycha
Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper
Frontiers in Marine Science
nitrification
DNRA
DNR
denitrification
anammox
metagenome
title Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper
title_full Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper
title_fullStr Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper
title_full_unstemmed Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper
title_short Spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the Baltic Proper
title_sort spatial and seasonal distribution of selected nitrogen cycle genes in deep waters of the baltic proper
topic nitrification
DNRA
DNR
denitrification
anammox
metagenome
url https://www.frontiersin.org/articles/10.3389/fmars.2025.1456825/full
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