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N2-fixation, ammonium release and N-transfer to the microbial and classical food web within a plankton community
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
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2016 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 10, no 2, 450-459 p.Article in journal (Refereed) Published
Abstract [en]

We investigated the role of N2-fixation by the colony-forming cyanobacterium, Aphanizomenon spp., for the plankton community and N-budget of the N-limited Baltic Sea during summer by using stable isotope tracers combined with novel secondary ion mass spectrometry, conventional mass spectrometry and nutrient analysis. When incubated with 15N2Aphanizomenon spp. showed a strong 15N-enrichment implying substantial 15N2-fixation. Intriguingly, Aphanizomenon did not assimilate tracers of 15NH4+ from the surrounding water. These findings are in line with model calculations that confirmed a negligible N-source by diffusion-limited NH4+ fluxes to Aphanizomenon colonies at low bulk concentrations (<250 nm) as compared with N2-fixation within colonies. No N2-fixation was detected in autotrophic microorganisms <5 μm, which relied on NH4+uptake from the surrounding water. Aphanizomenon released about 50% of its newly fixed N2 as NH4+. However, NH4+ did not accumulate in the water but was transferred to heterotrophic and autotrophic microorganisms as well as to diatoms (Chaetoceros sp.) and copepods with a turnover time of ~5 h. We provide direct quantitative evidence that colony-formingAphanizomenon releases about half of its recently fixed N2 as NH4+, which is transferred to the prokaryotic and eukaryotic plankton forming the basis of the food web in the plankton community. Transfer of newly fixed nitrogen to diatoms and copepods furthermore implies a fast export to shallow sediments via fast-sinking fecal pellets and aggregates. Hence, N2-fixing colony-forming cyanobacteria can have profound impact on ecosystem productivity and biogeochemical processes at shorter time scales (hours to days) than previously thought.

Place, publisher, year, edition, pages
2016. Vol. 10, no 2, 450-459 p.
National Category
Biological Sciences
Research subject
Marine Ecology
Identifiers
URN: urn:nbn:se:su:diva-122075DOI: 10.1038/ismej.2015.126ISI: 000368561100015OAI: oai:DiVA.org:su-122075DiVA: diva2:862750
Available from: 2015-10-23 Created: 2015-10-23 Last updated: 2017-12-01Bibliographically approved
In thesis
1. 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
2. Cyanobacterial Nitrogen Fixation in the Baltic Sea: With focus on Aphanizomenon sp.
Open this publication in new window or tab >>Cyanobacterial Nitrogen Fixation in the Baltic Sea: With focus on Aphanizomenon sp.
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Cyanobacteria are widely distributed in marine, freshwater and terrestrial habitats. Some cyanobacterial genera can convert di-nitrogen gas (N2) to bioavailable ammonium, i.e. perform nitrogen (N) fixation, and are therefore of profound significance for N cycling. N fixation by summer blooms of cyanobacteria is one of the largest sources of new N for the Baltic Sea. This thesis investigated N fixation by cyanobacteria in the Baltic Sea and explored the fate of fixed N at different spatial and temporal scales. In Paper I, we measured cell-specific N fixation by Aphanizomenon sp. at 10 ºC, early in the season. Fixation rates were high and comparable to those in late summer, indicating that Aphanizomenon sp. is an important contributor to N fixation already in its early growth season. In Paper II, we studied fixation and release of N by Aphanizomenon sp. and found that about half of the fixed N was rapidly released and transferred to other species, including autotrophic and heterotrophic bacteria, diatoms and copepods. In Paper III, we followed the development of a cyanobacterial bloom and related changes in dissolved and particulate N pools in the upper mixed surface layer. The bloom-associated total N (TN) increase was mainly due to higher particulate organic N (PON) concentrations, but also to increases in dissolved organic nitrogen (DON). About half the PON-increase could be explained by the sum of N-fixing cyanobacteria, other phytoplankton (>2µm) and zooplankton, indicating that production was stimulated by the N fixation. In Paper IV, we used a growth model based on measured photosynthesis–irradiance relationships to explore the production potential of Aphanizomenon sp. The model included data on irradiance, biomass, temperature and light attenuation (1999–2013). Until the bloom peak, the modelled production matched the measured biomass, indicating low production losses. Over the whole season, the modelled production could explain a substantial part of the summer TN increase, assuming that plausible losses (such as grazing or cell lysis) are retained within the upper mixed layer. Complementing the other data, we also investigated the nutrient content (Paper I) and varying cell width (Paper IV) of Aphanizomenon sp. By a combination of approaches, this thesis has contributed new information on cyanobacterial N fixation rates, the transfer of fixed N to other organisms in the food web and shown the potential for fixed N to stimulate summer primary and secondary production in the Baltic Sea.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2016. 43 p.
Keyword
cyanobacteria, Baltic Sea, nitrogen fixation, Aphanizomenon sp., dissolved nitrogen, particulate nitrogen, sedimentation
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-132773 (URN)978-91-7649-481-3 (ISBN)
External cooperation:
Public defence
2016-10-14, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 09:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 215-2009-813Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 215-2010-779Max Planck SocietyBaltic Ecosystem Adaptive Management (BEAM)Swedish Research Council, 621-2011-4406Knut and Alice Wallenberg Foundation
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 4: Manuscript.

Available from: 2016-09-21 Created: 2016-08-23 Last updated: 2016-09-12Bibliographically approved

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