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Non-cyanobacterial nitrogen fixation insights in humic freshwater lakes and ponds
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The biological basis of nitrogen fixation beyond the canonical role of Cyanobacteria is not well understood in freshwater ecosystems. To address this gap in knowledge, the main objective of this thesis is to study non-cyanobacterial nitrogen fixation in freshwater lakes and ponds.

Microbial communities and diazotrophic potential were characterized by direct metagenome sequencing from seasonally stratified lakes and permafrost thaw ponds, both of which are systems featuring strong redox gradients. To quantify the nitrogen fixation process, we also adopted and applied a 15N tracer method to estimate realized diazotrophic activity in five of the studied lakes. Chemical characteristics were also measured concomitantly to link diazotroph distribution patterns to chemical features and metabolic traits in the studied freshwaters.

Exploring a 3-year metagenomic time series of a humic lake (Trout Bog), widespread and stable occurrence of nifH genes were detected. This marker gene for nitrogen fixation appeared with accessory genes, validating the marker. The diazotrophic community was diverse and dynamic with contributions from Geobacter, Desulfobacterales, Methylococcales, Acidobacteria, Verrucomicrobia and Chlorobi. Accordingly, nitrogen fixation may be fueled by a variety of metabolic processes (heterotrophic sulfate/iron reducers, methylotrophs and photolithotrophs) in oxygen depleted dark waters. Interestingly the photolithotrophic Chlorobi also carried a Fe-only nitrogenase (anfH) recently implicated in alternative methane production. Overall, we demonstrated widespread potential for nitrogen fixation within hypolimnia in stratified humic lakes, and analyses of depth profiles also confirmed the presence of active diazotrophic communities in boreal lakes. These active nitrogen fixing communities were characterized by overall higher bacterial abundances, cellular aggregation and increased phosphorus availability as compared to communities where nitrogen fixation was not detected.

Expanding our work to include recently formed freshwater ecosystems, we characterized microbial communities in arctic thaw ponds at different ontogenetic stages. We also investigated the possible role of anfH in methane production, but the abundance of this gene was not correlated with high methane concentration in the water column. NifH was detected in all systems, and interestingly the hypolimnetic waters in the more established systems emerged as suitable niche for diazotrophs with nifH abundances positively correlated to elevated methane concentrations. Based on this observation, we propose that nitrogen-fixing microorganisms may be important partners in complex syntrophic networks established between bacteria and archaeal methanogens.  

In conclusion, the results presented across the different types of terrestrially influenced freshwater systems revealed widespread potential for nitrogen fixation within hypolimnia of humic lakes and permafrost thaw ponds. Furthermore, nitrogen fixation was confirmed at and below the redoxcline in five Finnish humic lakes. This implies that we need to look beyond phototrophic cyanobacteria to more fully understand the role of nitrogen fixation and overall nitrogen cycling in freshwater ecosystems.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. , p. 51
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1867
Keywords [en]
humic lakes, thaw ponds, non-cyanobacterial diazotrophs, nitrogen fixation, nitrogenase
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-395057ISBN: 978-91-513-0781-7 (print)OAI: oai:DiVA.org:uu-395057DiVA, id: diva2:1360350
Public defence
2019-11-29, Zootissalen, Evolutionary Biology Center, Villavägen 9, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2019-11-07 Created: 2019-10-11 Last updated: 2019-11-27
List of papers
1. Nitrogenase gene seasonal dynamics reveal diazotrophic potential in a humic bog lake
Open this publication in new window or tab >>Nitrogenase gene seasonal dynamics reveal diazotrophic potential in a humic bog lake
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-395054 (URN)
Available from: 2019-10-11 Created: 2019-10-11 Last updated: 2019-10-15
2. Uncoupled diazotrophy and oxygenic photosynthesis inferred from freshwater metagenomes collected from hypolimnetic dark-water
Open this publication in new window or tab >>Uncoupled diazotrophy and oxygenic photosynthesis inferred from freshwater metagenomes collected from hypolimnetic dark-water
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-395055 (URN)
Available from: 2019-10-11 Created: 2019-10-11 Last updated: 2019-10-15
3. High bacterial abundances and aggregation in humic lakes enhance nitrogen fixation potential via non-cyanobacterial diazotrophs
Open this publication in new window or tab >>High bacterial abundances and aggregation in humic lakes enhance nitrogen fixation potential via non-cyanobacterial diazotrophs
(English)Manuscript (preprint) (Other academic)
National Category
Social Sciences
Identifiers
urn:nbn:se:uu:diva-395056 (URN)
Available from: 2019-10-11 Created: 2019-10-11 Last updated: 2019-10-15
4. Non‐cyanobacterial diazotrophs dominate nitrogen‐fixing communities in permafrost thaw ponds
Open this publication in new window or tab >>Non‐cyanobacterial diazotrophs dominate nitrogen‐fixing communities in permafrost thaw ponds
2019 (English)In: Limnology and Oceanography, ISSN 0024-3590, E-ISSN 1939-5590Article in journal (Refereed) Published
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-395051 (URN)
Available from: 2019-10-11 Created: 2019-10-11 Last updated: 2019-10-15

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