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Functional genomics of the Baltic Sea cyanobacterium Nodularia spumigena in relation to nitrogen fixation, heterocyst differentiation and toxin production
Stockholm University, Faculty of Science, Department of Botany.
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Nodularia spumigena is a filamentous, heterocystous cyanobacterium that dominates the annual, toxic cyanobacterial blooms in the Baltic Sea. The blooms are believed to have increased in recent years, due to eutrophication by phosphate and/or nitrogen. Toxicity of these blooms is well-documented and attributed to the hepatotoxin nodularin. The focus of this study was to characterize nitrogen fixation and toxin production of Nodularia spumigena, in response to various levels of combined nitrogen and phosphate. In the presence of combined nitrogen, several Nodularia spumigena strains lost aerobic nitrogen fixation activity while the heterocyst frequency along the filaments remained unchanged. The expression of nifH dropped in response to the treatment, while the expression patterns of ntcA and hetR (key genes controlling heterocyst differentiation) were not affected. It is therefore concluded that in Nodularia, nitrogen fixation and heterocyst differentiation are uncoupled. Protein profiling during ammonium supplementation revealed differential expression of 28 proteins. Proteins involved in energy metabolism, carbon and nitrogen fixation were down-regulated during ammonium supplementation while stress-related proteins were up-regulated, further indicating that N. spumigena does not benefit from ammonium supplementation. Analysis of the nodularin synthetase (nda) gene expression demonstrated an increase of all the nine nda genes upon phosphate depletion and decrease of expression in the presence of combined nitrogen. In contrast to shifts in expression, the intra- and extracellular nodularin concentrations did not vary significantly, suggesting a transcriptionally-independent regulation of nodularin biosynthesis. Together, these data suggest that neither nitrogen nor phosphate alone, especially the low levels encountered in the Baltic Sea, affects heterocyst formation and nodularin biosynthesis.

Place, publisher, year, edition, pages
Stockholm: Department of Botany, Stockholm University , 2009. , 61 p.
Keyword [en]
cyanobacteria, Nodularia, nitrogen fixation, heterocyst, nitrogenase, ammonium, phosphate, nodularin, Baltic Sea
National Category
Botany
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-29495ISBN: 978-91-7155-935-7 (print)OAI: oai:DiVA.org:su-29495DiVA: diva2:233635
Public defence
2009-10-02, Föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 10:00 (English)
Opponent
Supervisors
Note
At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Submitted. Paper 4: Manuscript. Paper 5: ManuscriptAvailable from: 2009-09-10 Created: 2009-09-01 Last updated: 2009-09-01Bibliographically approved
List of papers
1. Expression of the nodularin synthetase genes in the Baltic Sea bloom-former cyanobacterium Nodularia spumigena strain AV1.
Open this publication in new window or tab >>Expression of the nodularin synthetase genes in the Baltic Sea bloom-former cyanobacterium Nodularia spumigena strain AV1.
2008 (English)In: FEMS Microbiol Ecol, ISSN 0168-6496, Vol. 65, no 1, 31-39 p.Article in journal (Refereed) Published
Abstract [en]

Cyanobacterial blooms in the Baltic Sea are a common phenomenon and are formed by the heterocystous, filamentous species Nodularia spumigena. The toxicity of these blooms is attributed to the hepatotoxin nodularin, produced by N. spumigena. Little is known regarding the regulatory mechanisms or environmental signaling that control nodularin production. Here we report the characterization of the transcriptional expression pattern of the nodularin synthetase gene cluster (nda) during phosphate depletion, and nitrogen supplementation. Real-time PCR analysis of these genes revealed that while cells continuously expressed the nda cluster, the expression of all nda genes increased when cells were subjected to phosphate depletion, and decreased in the presence of ammonium. In contrast to the shifts in expression, the intracellular and extracellular nodularin concentrations did not vary significantly during the treatments.

Keyword
Gene Expression Regulation; Bacterial, Ligases/*genetics/metabolism, Multigene Family, Nitrogen/metabolism, Nodularia/classification/*enzymology/genetics/growth & development, Peptides; Cyclic/*metabolism, Phosphates/metabolism, RNA; Bacterial/genetics/isolation & purification/metabolism, RNA; Messenger/genetics/metabolism, Reverse Transcriptase Polymerase Chain Reaction, Seawater/*microbiology, Sweden
Identifiers
urn:nbn:se:su:diva-18476 (URN)10.1111/j.1574-6941.2008.00499.x (DOI)000256717200003 ()18503549 (PubMedID)
Available from: 2009-01-26 Created: 2009-01-26 Last updated: 2009-09-01Bibliographically approved
2. Ammonium ions inhibit nitrogen fixation but do not affect heterocyst frequency in the bloom-forming cyanobacterium Nodularia spumigena strain AV1.
Open this publication in new window or tab >>Ammonium ions inhibit nitrogen fixation but do not affect heterocyst frequency in the bloom-forming cyanobacterium Nodularia spumigena strain AV1.
2007 (English)In: Microbiology, ISSN 1350-0872, Vol. 153, no Pt 11, 3704-3712 p.Article in journal (Refereed) Published
Abstract [en]

In the presence of ammonium ion, Nodularia spumigena strain AV1, a filamentous, heterocystous cyanobacterium isolated from the Baltic Sea, lost aerobic nitrogen-fixation activity while maintaining heterocyst frequency along the filaments. Real-time RT-PCR showed that the expression of nifH (encoding the dinitrogenase reductase component of the nitrogenase enzyme) was suppressed and the levels of NifH protein decreased dramatically in response to treatment with ammonium. On the other hand, ntcA (encoding the global nitrogen regulator in cyanobacteria) and hetR (the key regulatory gene in heterocyst differentiation) were expressed and their expression patterns were not affected by the treatment with ammonium. These data demonstrate that N. spumigena strain AV1 maintains heterocyst frequency along the filaments in the presence of ammonium and in the absence of detectable N2-fixation activity.

Identifiers
urn:nbn:se:su:diva-21072 (URN)10.1099/mic.0.2007/007849-0 (DOI)000251096800009 ()17975078 (PubMedID)
Available from: 2007-12-05 Created: 2007-12-05 Last updated: 2009-09-01Bibliographically approved
3. Variability in the response of the cyanobacterium Nodularia spumigena to nitrogen supplementation
Open this publication in new window or tab >>Variability in the response of the cyanobacterium Nodularia spumigena to nitrogen supplementation
(English)Manuscript (preprint) (Other (popular science, discussion, etc.))
Keyword
Nodularia spumigena, nitrogen fixation, ammonium, nitrate, heterocyst, nitrogen supplementation
National Category
Microbiology in the medical area
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-29490 (URN)
Available from: 2009-09-01 Created: 2009-09-01 Last updated: 2010-01-14Bibliographically approved
4. Characterization of nifH gene expression, modification and rearrangement in Nodularia spumigena strain AV1
Open this publication in new window or tab >>Characterization of nifH gene expression, modification and rearrangement in Nodularia spumigena strain AV1
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(English)Manuscript (preprint) (Other academic)
National Category
Microbiology in the medical area
Research subject
Molecular Cellbiology
Identifiers
urn:nbn:se:su:diva-29491 (URN)
Available from: 2009-09-01 Created: 2009-09-01 Last updated: 2010-01-14Bibliographically approved
5. Proteomic profiling of the Baltic Sea cyanobacterium Nodularia spumigena strain AV1 during ammonium supplementation
Open this publication in new window or tab >>Proteomic profiling of the Baltic Sea cyanobacterium Nodularia spumigena strain AV1 during ammonium supplementation
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(English)Manuscript (preprint) (Other academic)
Identifiers
urn:nbn:se:su:diva-29493 (URN)
Available from: 2009-09-01 Created: 2009-09-01 Last updated: 2010-01-14Bibliographically approved

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