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Towards an understanding of diazocyte development and diazotrophy in the marine cyanobacterium Trichodesmium
Stockholm University, Faculty of Science, Department of Botany.
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Trichodesmium is a filamentous cyanobacterium of great ecological significance as it contributes significantly to primary production in oceans through an efficient nitrogen fixation strategy, including a unique cell type, the diazocyte. The aim of this thesis was to generate a deeper understanding of the structural and molecular background related to the development of diazocytes and the maintenance of diazotrophy in Trichodesmium erythraeum IMS101.

Data obtained demonstrated a diurnal separation of basic physiological processes, with nitrogen fixation and photosynthesis confined to the light and cell division and diazocyte development to the dark period. Diazocyte development was preceded by cell division and expression of the main regulator of heterocyst differentiation, hetR. In non-diazotrophic cultures, subject to nitrogen depletion, a developmental program was initiated in a subset of cells that differentiated into mature nitrogenase containing diazocytes, while addition of combined nitrogen abolished development. A nitrogen depletion signal initially enhanced transcription of the global nitrogen regulator ntcA and was followed by elevated expression of coxBII (respiration) and glnA (primary ammonia assimilation) and pronounced sub-cellular rearrangements. Comparative proteomic analysis further revealed a clear shift in the cellular metabolism depending on the nitrogen regime, with 94 proteins being differentially expressed in diazotrophic (with diazocytes) as opposed to in non-diazotrophic cultures. Proteins up-shifted in diazotrophic cultures were related to supporting the nitrogenase enzyme with reducing equivalents and a lower oxygen tension. In addition, two highly divergent flavodoxins were identified with different expression patterns in response to combined nitrogen additions and the data discourage the use of flavodoxins as indicators of iron stress in Trichodesmium populations.

 

Place, publisher, year, edition, pages
Stockholm: Department of Botany, Stockholm University , 2009. , 51 p.
Keyword [en]
Cyanobacteria, Trichodesmium, diazocyte, cell differentiation, nitrogen fixation, cell division, flavodoxin
National Category
Botany
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-27206ISBN: 978-91-7155-885-5 (print)OAI: oai:DiVA.org:su-27206DiVA: diva2:212971
Public defence
2009-05-29, Föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 13:00 (English)
Opponent
Supervisors
Available from: 2009-05-08 Created: 2009-04-24 Last updated: 2009-05-07Bibliographically approved
List of papers
1. Two flavodoxin genes in Trichodesmium (Oscillatoriales, Cyanophyceae): Remarkable sequence divergence and possible functional diversification
Open this publication in new window or tab >>Two flavodoxin genes in Trichodesmium (Oscillatoriales, Cyanophyceae): Remarkable sequence divergence and possible functional diversification
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2009 (English)In: Journal of Experimental Marine Biology and Ecology, ISSN 0022-0981, E-ISSN 1879-1697, Vol. 371, no 1, 93-101 p.Article in journal (Refereed) Published
Abstract [en]

We analyzed flavodoxin gene sequences and transcription patterns in the marine nitrogen-fixing cyanobacterium Trichodesmium Ehrenberg ex Gomont 1892. While a typical cyanobacterial flavodoxin ortholog (fld1) was identified from cultured (strain IMS101) and environmental Trichodesmium by PCR and Southern blot hybridization, a second flavodoxin (fld2) was identified in the genome sequence. BLAST and phylogenetic analyses indicated that the two fld genes were highly divergent: fld1 was most closely related to fld common in cyanobacteria, wheras fld2 formed a distinct cluster with a fld so far only found in the unicellular diazotrophic cyanobacteria Cyanothece and Crocosphaera (in which fld2 was the only fld). The fld2 cluster was more closely allied with a fld in non-cyanobacterial diazotrophs such as Azotobacter and Azoarcus than fld1 in other cyanobacteria. This result suggests different evolutionary history of these two genes. Real-Time RT–PCR analysis on iron-replete and iron-deplete Trichodesmium cultures revealed remarkable diel dynamics in transcription of both flds but surprisingly failed to show induction under iron stress. Addition of nitrate to these cultures depressed nifH and fld2 transcription while elevating the transcription of fld1 in iron-stressed cultures. A positive correlation between fld and nifH transcript abundances was found, which was stronger in the case of fld2 than fld1. Our data suggest that these two flavodoxins in Trichodesmium may be functionally diversified and that use of flavodoxin as an iron stress indicator needs to be validated for each organism with consideration of diel dynamics of gene expression.

Place, publisher, year, edition, pages
Elsevier, 2009
Keyword
Cyanobacteria, Flavodoxin, Gene transcription, Iron stress, Nitrogenase, Trichodesmium
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-27219 (URN)10.1016/j.jembe.2009.01.010 (DOI)000264557900011 ()
Available from: 2009-04-26 Created: 2009-04-26 Last updated: 2017-12-13Bibliographically approved
2. Temporal separation of cell division and diazotrophy in the marine diazotrophic cyanobacterium Trichodesmium erythraeum IMS101
Open this publication in new window or tab >>Temporal separation of cell division and diazotrophy in the marine diazotrophic cyanobacterium Trichodesmium erythraeum IMS101
2009 (English)In: FEMS Microbiology Letters, ISSN 0378-1097, E-ISSN 1574-6968, Vol. 295, no 2, 281-288 p.Article in journal (Refereed) Published
Abstract [en]

Examination of the diurnal patterns of basic cellular processes in the marine nonheterocystous diazotrophic cyanobacterium Trichodesmium revealed that the division of cells occurred throughout the diurnal cycle, but that it oscillated and peaked at an early stage in the dark period. Transcription of the early cell division gene ftsZ and the occurrence of the FtsZ protein showed a similar diurnal rhythmicity that preceded the division of cells. DNA replication (dnaA gene transcription) occurred before the transcription of ftsZ and hetR, the latter encoding the key heterocyst differentiation protein. Transcription of ftsZ and hetR in turn preceded the development of the nitrogen-fixing diazocytes and nifH transcription, and were at the minimum when diazotrophy was at the maximum. The nifH gene transcription showed a negative correlation to the circadian clock gene kaiC. Together, the data show a temporal separation between cell division and diazotrophy on a diurnal basis.

Place, publisher, year, edition, pages
Blackwell, 2009
Keyword
Trichodesmium, cyanobacteria, cell division, nitrogen fixation, diazocyte differentiation
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-27220 (URN)10.1111/j.1574-6968.2009.01608.x (DOI)000266111400019 ()
Available from: 2009-04-26 Created: 2009-04-26 Last updated: 2017-12-13Bibliographically approved
3. Diazocyte differentiation is induced upon combined nitrogen deprivation in the marine cyanobacterium Trichodesmium erythraeum IMS101
Open this publication in new window or tab >>Diazocyte differentiation is induced upon combined nitrogen deprivation in the marine cyanobacterium Trichodesmium erythraeum IMS101
(English)Manuscript (Other academic)
Keyword
Trichodesmium, cyanobacteria, diazocyte, nitrogen fixation, cell differentiation
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-27221 (URN)
Available from: 2009-04-26 Created: 2009-04-26 Last updated: 2010-01-14Bibliographically approved
4. Comparative proteomic profiling of the marine cyanobacterium Trichodesmium erythraeum IMS101 grown under nitrogen-fixing and nitrogen supplemented conditions
Open this publication in new window or tab >>Comparative proteomic profiling of the marine cyanobacterium Trichodesmium erythraeum IMS101 grown under nitrogen-fixing and nitrogen supplemented conditions
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(English)Manuscript (Other academic)
Keyword
Trichodesmium, cyanobacteria, diazocyte, nitrogen fixation, comparative proteomics, 2D-PAGE
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-27222 (URN)
Available from: 2009-04-26 Created: 2009-04-26 Last updated: 2010-01-14Bibliographically approved

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