Change search
CiteExportLink to record
Permanent link

Direct link
Cite
Citation style
  • apa
  • ieee
  • modern-language-association-8th-edition
  • vancouver
  • Other style
More styles
Language
  • de-DE
  • en-GB
  • en-US
  • fi-FI
  • nn-NO
  • nn-NB
  • sv-SE
  • Other locale
More languages
Output format
  • html
  • text
  • asciidoc
  • rtf
Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Geological Sciences.
Stockholm University, Faculty of Science, Department of Geological Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
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.

Place, publisher, year, edition, pages
2015. Vol. 9, no 1, 1456-1466 p.
Keyword [en]
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: urn:nbn:se:su:diva-115034DOI: 10.1038/ismej.2014.232ISI: 000354786700016OAI: oai:DiVA.org:su-115034DiVA: diva2:795477
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
In thesis
1. Control factors of the marine nitrogen cycle: The role of meiofauna, macrofauna, oxygen and aggregates
Open this publication in new window or tab >>Control factors of the marine nitrogen cycle: The role of meiofauna, macrofauna, oxygen and aggregates
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
Nitrogen cycle, denitrification, DNRA, anammox, anoxia, hypoxia, eutrophication, meiofauna, macrofauna, aggregates, cyanobacteria, Baltic Sea
National Category
Geochemistry
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-115036 (URN)978-91-7649-129-4 (ISBN)
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
2. Marine nitrogen fixation: Cyanobacterial nitrogen fixation and the fate of new nitrogen in the Baltic Sea
Open this publication in new window or tab >>Marine nitrogen fixation: Cyanobacterial nitrogen fixation and the fate of new nitrogen in the Baltic Sea
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Biogeochemical processes in the marine biosphere are important in global element cycling and greatly influence the gas composition of the Earth’s atmosphere. The nitrogen cycle is a key component of marine biogeochemical cycles. Nitrogen is an essential constituent of living organisms, but bioavailable nitrogen is often short in supply thus limiting primary production. The largest input of nitrogen to the marine environment is by N2-fixation, the transformation of inert N2 gas into bioavailable ammonium by a distinct group of microbes. Hence, N2-fixation bypasses nitrogen limitation and stimulates productivity in oligotrophic regions of the marine biosphere.

Extensive blooms of N2-fixing cyanobacteria occur regularly during summer in the Baltic Sea. N2-fixation during these blooms adds several hundred kilotons of new nitrogen into the Baltic Proper, which is similar in magnitude to the annual nitrogen load by riverine discharge and more than twice the atmospheric nitrogen deposition in this area. N2-fixing cyanobacteria are therefore a critical constituent of nitrogen cycling in the Baltic Sea. In this thesis N2 fixation of common cyanobacteria in the Baltic Sea and the direct fate of newly fixed nitrogen in otherwise nitrogen-impoverished waters were investigated. Initially, the commonly used 15N-stable isotope assay for N2-fixation measurements was evaluated and optimized in terms of reliability and practicality (Paper I), and later applied for N2-fixation assessments (Paper II–IV). N2 fixation in surface waters of the Baltic Sea was restricted to large filamentous heterocystous cyanobacteria (Aphanizomenon sp., Nodularia spumigena, Dolichospermum spp.) and absent in smaller filamentous cyanobacteria such as Pseudanabaena sp., and unicellular and colonial picocyanobacteria (Paper II-III). Most of the N2-fixation in the Northern Baltic Proper was contributed by Aphanizomenon sp. due to its high abundance throughout the summer and similar rates of specific N2-fixation as Dolichospermum spp. and N. spumigena. Specific N2 fixation was substantially higher near the coast than in an offshore region (Paper II). Half of the fixed nitrogen was released as ammonium at the site near the coast and taken up by non-N2-fixing organisms including phototrophic and heterotrophic, prokaryotic and eukaryotic planktonic organisms. Newly fixed nitrogen was thereby rapidly turned-over in the nitrogen-depleted waters (Paper III). In colonies of N. spumigena even the potential for a complete nitrogen cycle condensed to a microcosm of a few millimeters could be demonstrated (Paper IV). Cyanobacterial colonies can therefore be hot-spots of nitrogen transformation processes potentially including nitrogen gain, recycling and loss processes. In conclusion, blooms of cyanobacteria are instrumental for productivity and CO2 sequestration in the Baltic Sea. These findings advance our understanding of biogeochemical cycles and ecosystem functioning in relation to cyanobacterial blooms in the Baltic Sea with relevance for both ecosystem-based management in the Baltic Sea, and N2-fixation and nitrogen cycling in the global ocean.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2015. 41 p.
Keyword
biogeochemistry, nitrogen cycling, nitrogen fixation, cyanobacteria, Baltic Sea
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-122080 (URN)978-91-7649-278-9 (ISBN)
Public defence
2015-11-27, sal P216, NPQ-huset, Svante Arrhenius väg 20 A, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

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

Available from: 2015-11-05 Created: 2015-10-23 Last updated: 2015-12-15Bibliographically approved

Open Access in DiVA

No full text

Other links

Publisher's full text

Search in DiVA

By author/editor
Isabell, KlawonnBonaglia, StefanoBrüchert, VolkerPloug, Helle
By organisation
Department of Ecology, Environment and Plant SciencesDepartment of Geological Sciences
In the same journal
The ISME Journal
Earth and Related Environmental SciencesBiological Sciences

Search outside of DiVA

GoogleGoogle Scholar

doi
urn-nbn

Altmetric score

doi
urn-nbn
Total: 292 hits
CiteExportLink to record
Permanent link

Direct link
Cite
Citation style
  • apa
  • ieee
  • modern-language-association-8th-edition
  • vancouver
  • Other style
More styles
Language
  • de-DE
  • en-GB
  • en-US
  • fi-FI
  • nn-NO
  • nn-NB
  • sv-SE
  • Other locale
More languages
Output format
  • html
  • text
  • asciidoc
  • rtf