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Control factors of the marine nitrogen cycle: The role of meiofauna, macrofauna, oxygen and aggregates
Stockholm University, Faculty of Science, Department of Geological Sciences. (Biogeochemistry group)
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The ocean is the most extended biome present on our planet. Recent decades have seen a dramatic increase in the number and gravity of threats impacting the ocean, including discharge of pollutants, cultural eutrophication and spread of alien species. It is essential therefore to understand how different impacts may affect the marine realm, its life forms and biogeochemical cycles. The marine nitrogen cycle is of particular importance because nitrogen is the limiting factor in the ocean and a better understanding of its reaction mechanisms and regulation is indispensable. Furthermore, new nitrogen pathways have continuously been described. The scope of this project was to better constrain cause-effect mechanisms of microbially mediated nitrogen pathways, and how these can be affected by biotic and abiotic factors.

This thesis demonstrates that meiofauna, the most abundant animal group inhabiting the world’s seafloors, considerably alters nitrogen cycling by enhancing nitrogen loss from the system. In contrast, larger fauna such as the polychaete Marenzelleria spp. enhance nitrogen retention, when they invade eutrophic Baltic Sea sediments. Sediment anoxia, caused by nutrient excess, has negative consequences for ecosystem processes such as nitrogen removal because it stops nitrification, which in turn limits both denitrification and anammox. This was the case of Himmerfjärden and Byfjord, two estuarine systems affected by anthropogenic activities, such as treated sewage discharges. When Byfjord was artificially oxygenated, nitrate reduction mechanisms started just one month after pumping. However, the balance between denitrification and nitrate ammonification did not favor either nitrogen removal or its retention.

Anoxia is also present in aggregates of the filamentous cyanobacteria Nodularia spumigena. This thesis shows that even in fully oxic waters, millimetric aggregates can host anaerobic nitrogen processes, with clear implications for the pelagic compartment. While the thesis contributed to our knowledge on marine nitrogen cycling, more data need to be collected and experiments performed in order to understand key processes and regulation mechanisms of element cycles in the ocean. In this way, stakeholders may follow and take decisions in order to limit the continuous flow of human metabolites and impacts on the marine environment.

Place, publisher, year, edition, pages
Stockholm: Department of Geological Sciences, Stockholm University , 2015. , 35 p.
Series
Meddelanden från Stockholms universitets institution för geologiska vetenskaper, 357
Keyword [en]
Nitrogen cycle, denitrification, DNRA, anammox, anoxia, hypoxia, eutrophication, meiofauna, macrofauna, aggregates, cyanobacteria, Baltic Sea
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
URN: urn:nbn:se:su:diva-115036ISBN: 978-91-7649-129-4 (print)OAI: oai:DiVA.org:su-115036DiVA: diva2:795493
Public defence
2015-04-29, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 13:00 (English)
Opponent
Supervisors
Funder
Baltic Ecosystem Adaptive Management (BEAM)Swedish Research Council Formas
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 2: Manuscript.

Available from: 2015-04-07 Created: 2015-03-16 Last updated: 2015-07-01Bibliographically approved
List of papers
1. Seasonal oxygen, nitrogen and phosphorus benthic cycling along an impacted Baltic Sea estuary: regulation and spatial patterns
Open this publication in new window or tab >>Seasonal oxygen, nitrogen and phosphorus benthic cycling along an impacted Baltic Sea estuary: regulation and spatial patterns
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2014 (English)In: Biogeochemistry, ISSN 0168-2563, E-ISSN 1573-515X, Vol. 119, no 1-3, 139-160 p.Article in journal (Refereed) Published
Abstract [en]

The regulatory roles of temperature, eutrophication and oxygen availability on benthic nitrogen (N) cycling and the stoichiometry of regenerated nitrogen and phosphorus (P) were explored along a Baltic Sea estuary affected by treated sewage discharge. Rates of sediment denitrification, anammox, dissimilatory nitrate reduction to ammonium (DNRA), nutrient exchange, oxygen (O2) uptake and penetration were measured seasonally. Sediments not affected by the nutrient plume released by the sewage treatment plant (STP) showed a strong seasonality in rates of O2 uptake and coupled nitrification-denitrification, with anammox never accounting for more than 20% of the total dinitrogen (N2) production. N cycling in sediments close to the STP was highly dependent on oxygen availability, which masked temperature-related effects. These sediments switched from low N loss and high ammonium (NH4+) efflux under hypoxic conditions in the fall, to a major N loss system in the winter when the sediment surface was oxidized. In the fall DNRA outcompeted denitrification as the main nitrate (NO3-) reduction pathway, resulting in N recycling and potential spreading of eutrophication. A comparison with historical records of nutrient discharge and denitrification indicated that the total N loss in the estuary has been tightly coupled to the total amount of nutrient discharge from the STP. Changes in dissolved inorganic nitrogen (DIN) released from the STP agreed well with variations in sedimentary N2 removal. This indicates that denitrification and anammox efficiently counterbalance N loading in the estuary across the range of historical and present-day anthropogenic nutrient discharge. Overall low N/P ratios of the regenerated nutrient fluxes impose strong N limitation for the pelagic system and generate a high potential for nuisance cyanobacterial blooms.

Keyword
Sediment, Benthic flux, Denitrification, Anammox, DNRA, Eutrophication
National Category
Earth and Related Environmental Sciences
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-97297 (URN)10.1007/s10533-014-9953-6 (DOI)000336028400010 ()
Projects
Baltic NutrientsBaltic Ecosystem Adaptive Management - BEAMStockholm University Marine research Centre
Funder
Ecosystem Approach to the Baltic Sea (Upphört/Closed 2010)Swedish Research Council Formas
Available from: 2013-12-06 Created: 2013-12-06 Last updated: 2017-12-06Bibliographically approved
2. Oxygenation of an anoxic fjord basin strongly stimulates benthic denitrification and DNRA
Open this publication in new window or tab >>Oxygenation of an anoxic fjord basin strongly stimulates benthic denitrification and DNRA
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(English)Manuscript (preprint) (Other academic)
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-115044 (URN)
Available from: 2015-03-16 Created: 2015-03-16 Last updated: 2016-01-29Bibliographically approved
3. Effect of reoxygenation and Marenzelleria spp. bioturbation on Baltic Sea sediment metabolism
Open this publication in new window or tab >>Effect of reoxygenation and Marenzelleria spp. bioturbation on Baltic Sea sediment metabolism
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2013 (English)In: Marine Ecology Progress Series, ISSN 0171-8630, E-ISSN 1616-1599, Vol. 482, 43-55 p.Article in journal (Refereed) Published
Abstract [en]

Nutrient reduction and the improvement of bottom water oxygen concentrations are thought to be key factors in the recovery of eutrophic aquatic ecosystems. The effects of reoxygenation and bioturbation of natural hypoxic sediments in the Baltic Sea were studied using a mesocosm experiment. Anoxic sediment box cores were collected from 100 m depth in Kanholmsfjärden (Stockholm Archipelago) and maintained in flow-through mesocosms with 3 treatments: (1) hypoxic: supplied with hypoxic water; (2) normoxic: supplied with oxic water; and (3) Marenzelleria: supplied with oxic water and the polychaete Marenzelleria spp. (2000 ind. m–2). After a 7 wk long conditioning period, net fluxes of dissolved O2, CH4, Fe2+, Mn2+, NH4+, NO2-, NO3-, PO43- and H4SiO4, and rates of nitrate ammonification (DNRA), denitrification and anammox were determined. Phosphate was taken up by the sediment in all treatments, and the uptake was highest in the normoxic treatment with Marenzelleria. Normoxic conditions stimulated the denitrification rate by a factor of 5. Denitrification efficiency was highest under normoxia (50%), intermediate in bioturbated sediments (16%), and very low in hypoxic sediments (4%). The shift from hypoxic to normoxic conditions resulted in a significantly higher retention of NH4+, H4SiO4 and Mn2+ in the sediment, but the bioturbation by Marenzelleria reversed this effect. Results from our study suggest that bioturbation by Marenzelleria stimulates the exchange of solutes between sediment and bottom water through irrigation and enhances bacterial sulfate reduction in the burrow walls. The latter may have a toxic effect on nitrifying bacteria, which, in turn, suppresses denitrification rates.

Keyword
Hypoxia, Macrofauna, Mesocosm, Denitrification, Dissimilatory nitrate reduction to ammonium, DNRA, Benthic Flux, Baltic Sea
National Category
Earth and Related Environmental Sciences
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-90105 (URN)10.3354/meps10232 (DOI)000319337100004 ()
Note

AuthorCount: 8;

Available from: 2013-05-22 Created: 2013-05-22 Last updated: 2017-12-06Bibliographically approved
4. Meiofauna increases bacterial denitrification in marine sediments
Open this publication in new window or tab >>Meiofauna increases bacterial denitrification in marine sediments
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2014 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 5, 5133- p.Article in journal (Refereed) Published
Abstract [en]

Denitrification is a critical process that can alleviate the effects of excessive nitrogen availability in aquatic ecosystems subject to eutrophication. An important part of denitrification occurs in benthic systems where bioturbation by meiofauna (invertebrates <1mm) and its effect on element cycling are still not well understood. Here we study the quantitative impact of meiofauna populations of different abundance and diversity, in the presence and absence of macrofauna, on nitrate reduction, carbon mineralization and methane fluxes. In sediments with abundant and diverse meiofauna, denitrification is double that in sediments with low meiofauna, suggesting that meiofauna bioturbation has a stimulating effect on nitrifying and denitrifying bacteria. However, high meiofauna densities in the presence of bivalves do not stimulate denitrification, while dissimilatory nitrate reduction to ammonium rate and methane efflux are significantly enhanced. We demonstrate that the ecological interactions between meio-, macrofauna and bacteria are important in regulating nitrogen cycling in soft-sediment ecosystems.

National Category
Earth and Related Environmental Sciences
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-110208 (URN)10.1038/ncomms6133 (DOI)000343980300007 ()
Note

AuthorCount:5;

Available from: 2014-12-09 Created: 2014-12-08 Last updated: 2017-12-05Bibliographically approved
5. Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates
Open this publication in new window or tab >>Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates
2015 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 9, no 1, 1456-1466 p.Article in journal (Refereed) Published
Abstract [en]

Colonies of N2-fixing cyanobacteria are key players in supplying new nitrogen to the ocean, but the biological fate of this fixed nitrogen remains poorly constrained. Here, we report on aerobic and anaerobic microbial nitrogen transformation processes that co-occur within millimetre-sized cyanobacterial aggregates (Nodularia spumigena) collected in aerated surface waters in the Baltic Sea. Microelectrode profiles showed steep oxygen gradients inside the aggregates and the potential for nitrous oxide production in the aggregates’ anoxic centres. 15N-isotope labelling experiments and nutrient analyses revealed that N2 fixation, ammonification, nitrification, nitrate reduction to ammonium, denitrification and possibly anaerobic ammonium oxidation (anammox) can co-occur within these consortia. Thus, N. spumigena aggregates are potential sites of nitrogen gain, recycling and loss. Rates of nitrate reduction to ammonium and N2 were limited by low internal nitrification rates and low concentrations of nitrate in the ambient water. Presumably, patterns of N-transformation processes similar to those observed in this study arise also in other phytoplankton colonies, marine snow and fecal pellets. Anoxic microniches, as a pre-condition for anaerobic nitrogen transformations, may occur within large aggregates (1 mm) even when suspended in fully oxygenated waters, whereas anoxia in small aggregates (<1 to 0.1 mm) may only arise in low-oxygenated waters (25 μM). We propose that the net effect of aggregates on nitrogen loss is negligible in NO3-depleted, fully oxygenated (surface) waters. In NO3-enriched (>1.5 μM), O2-depleted water layers, for example, in the chemocline of the Baltic Sea or the oceanic mesopelagic zone, aggregates may promote N-recycling and -loss processes.

Keyword
Nitrogen cycle /Cyanobacteria/macroaggregates/O2 and N2O microsensors/isotope pairing technique/Oxygen Minimum Zones
National Category
Earth and Related Environmental Sciences Biological Sciences
Research subject
Geochemistry; Marine Ecology
Identifiers
urn:nbn:se:su:diva-115034 (URN)10.1038/ismej.2014.232 (DOI)000354786700016 ()
Funder
Baltic Ecosystem Adaptive Management (BEAM)Swedish Research Council Formas
Available from: 2015-03-16 Created: 2015-03-16 Last updated: 2017-12-04Bibliographically approved

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