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Genetic variability and nitrogenase activity of cyanobacterial communities associated with tropical seagrass meadows (western Indian Ocean)
Stockholm University, Faculty of Science, Department of Botany. (Plant Physiology, Birgitta Bergman's group)
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Tropical seagrass ecosystems are highly productive and important for sustaining marine life and associated coastal societies. In this study, the diversity and role of nitrogen-fixing cyanobacteria associated with five common seagrass genera in coastal regions of the western Indian Ocean (WIO; Tanzania) were examined, as well as the impact of anthropogenic activities. Cyanobacteria were characterized morphologically and genetically (16S rRNA and nifH gene phylogeny), as were diel variations in nifH gene expression, NifH protein levels and nitrogenase activity. The results revealed that WIO seagrass beds supported rich cyanobacterial diversity and that these represented approx. 83% of total clones obtained (DNA and RNA nifH clone libraries). Non-heterocystous genera, such as Oscillatoria, Lyngbya, Leptolyngbya, Phormidium and Microcoleus dominated, while heterocystous morphotypes such as Calothrix were less frequent and unicellular morphotypes (e.g. Gloeocapsa, Chroococcus and Chroococcidiopsis) were few. Additionally, the phylogenetic analysis revealed several novel uncharacterized cyanobacterial clades. Cyanobacterial composition and nitrogenase activity varied over seasons and between the seagrass species. Day time nitrogenase activity originated primarily from heterocystous phylotypes, while non-heterocystous filamentous phylotypes fixed nitrogen at night. The highest activity in the diel cycle was 358 ± 232 nmol C2H4 g-1 h-1at 09.00 associated with epiphytes of the seagrass Cymodocea. Nitrogenase activity was consistently lower in anthropogenically disturbed (eutrophication) seagrass sites. Such data suggest that diazotrophic cyanobacteria may be a significant source of ‘new’ nitrogen in the often oligotrophic coastal regions of tropical oceans. It is also proposed that the rapid shifts in the cyanobacterial population and function found may also be used as early disturbance indicator in coastal management practices.

Place, publisher, year, edition, pages
Stockholm: Department of Botany, Stockholm University , 2010. , 57 p.
Keyword [en]
cyanobacteria, nitrogenase activity, diazotrophs, seagrass, western Indian ocean
National Category
Botany
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-38278ISBN: 978-91-7447-001-7 (print)OAI: oai:DiVA.org:su-38278DiVA: diva2:309240
Public defence
2010-05-06, föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 10:00 (English)
Opponent
Supervisors
Projects
SIDA SAREC Bilateral Marine Sciences ProjectThe Swedish Foundation for International Cooperation in Research and Higher Education
Note
At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Manuscript. Available from: 2010-04-14 Created: 2010-04-07 Last updated: 2010-04-14Bibliographically approved
List of papers
1. Cyanobacteria Occurrence and Nitrogen Fixation Ratesin the Seagrass Meadows of the East Coast of Zanzibar: Comparisons of Sites With and Without Seaweed Farms
Open this publication in new window or tab >>Cyanobacteria Occurrence and Nitrogen Fixation Ratesin the Seagrass Meadows of the East Coast of Zanzibar: Comparisons of Sites With and Without Seaweed Farms
2008 (English)In: Western Indian Ocean journal of marine science, ISSN 0856-860X, Vol. 7, no 1, 45-55 p.Article in journal (Refereed) Published
Abstract [en]

The occurrence and biological nitrogen fixation rates of epiphytic and benthic diazotrophs were studied in seagrass meadows at sites with seaweed farms and at a control site without seaweed farms from two locations, Chwaka Bay and Jambiani, along the east coast of Zanzibar. Ten species of cyanobacteria were encountered and Lyngbya majuscula and Microcoleus sp. were dominant in Chwaka Bay and Jambiani respectively. Cyanobacterial occurrence was significantly higher in seagrass meadows without seaweed farms (P<0.02), but there was no significant difference (P>0.05) in biomass (chlorophyll a). Biomass averaged 2.96±0.73 and 3.10±1.24 μg Chl a cm-2 in seaweed farms and 3.46±1.72 μg Chl a cm-2 at Chwaka Bay and 3.14±1.31 μg Chl a cm-2 at Jambiani in transects without seaweed farms. Nitrogenase activity showed no significant differences between sites with and without seaweed farms, (P=0.66 Chwaka and 0.75 at Jambiani). Fixation rates in sites without seaweed farms averaged 35.8±39.9 (Chwaka Bay) and 13.1±12.7 (Jambiani) μmol of C2H4 produced/m2/hr, while with seaweed farms averaged 22.6±22.5 and 12.8±14.9 μmol C2H4 produced/m2/hr at the same sites. There were no significant differences in nutrient levels between locations, sites with and without seaweed farms, or between tidal levels except for nitrate, which was significantly higher (P=0.01) at Jambiani than at Chwaka Bay. It was concluded that diazotrophs contribute a significant amount of exogenous nitrogen to the seagrass ecosystem, but no significant differences could be found between sites with or without seaweed farms.

Place, publisher, year, edition, pages
Zanzibar, Tanzania: Wiomsa, 2008
Keyword
Cyanobacteria, Nitrogen Fixation, Seagrass, Seaweed Farming
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-38275 (URN)
Projects
Masma SeagrassSida/SAREC Bilateral Marine Science Programme
Available from: 2010-04-07 Created: 2010-04-07 Last updated: 2017-12-12Bibliographically approved
2. Nitrogen fixation by epiphytic and epibenthic diazotrophs associated with seagrass meadows along the Tanzanian coast, Western Indian Ocean
Open this publication in new window or tab >>Nitrogen fixation by epiphytic and epibenthic diazotrophs associated with seagrass meadows along the Tanzanian coast, Western Indian Ocean
2009 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 57, 33-42 p.Article in journal (Refereed) Published
Abstract [en]

Seasonal, diurnal, and age-dependent variations in nitrogen fixation (nitrogenase activity) by epiphytic diazotrophs colonizing the seagrasses Halodule uninervis, Cymodocea rotundata, Thalassodendron ciliatum, and Thalassia hemprichii, and by epibenthic diazotrophs associated with seagrass-vegetated and nonvegetated sediments, were estimated at 2 sites along the Tanzanian coast, Western Indian Ocean. Acetylene reduction-gas chromatography showed that nitrogenase activity values were significantly higher (p = 0.0004) at the site with low nutrient levels (Mjimwema) than at the site with higher nutrient levels (Ocean Road). The nitrogenase activity ranged from 10 to 192 nmol N g–1 h–1 for H. uninervis, 7 to 80 nmol N g–1 h–1 for C. rotundata, 10 to 75 nmol N g–1 h–1 for Thalassia hemprichii, and from 4 to 61 nmol N g–1 h–1 for Thalassodendron ciliatum. Nitrogenase activity values in sediments covered by seagrasses were significantly higher than in surrounding nonvegetated sediments (t = 4.021, p = 0.0005). Significant variations in nitrogenase activity were apparent depending on leaf age and season, with highest activity being found in mid-aged leaves during the northeastern monsoon (NEM), and in older leaves during the southeastern monsoon (SEM). Daytime nitrogenase activity was appreciable on above-ground seagrass parts, while rhizosphere activity peaked at night-time. Collectively our data show that diazotrophs (cyanobacteria and other bacteria) are associated with seagrasses (leaves and roots), and potentially constitute an integral part of the ecosystem. They show highly dynamic nitrogenase activity and a succession in seagrass colonization, and we concluded that their presence may contribute to the productivity of the seagrass beds.

Place, publisher, year, edition, pages
Germany: Inter-Research, 2009
Keyword
Nitrogen fixation, Diazotrophs, Epibenthic, Epiphytes, Seagrass, Western Indian Ocean
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-38264 (URN)10.3354/AME01323 (DOI)000271056500003 ()
Projects
Sida/SAREC Bilateral Marine Science Programme
Available from: 2010-04-06 Created: 2010-04-06 Last updated: 2017-12-12Bibliographically approved
3. Cyanobacteria associated with the phyllosphere of the seagrass Cymodocea rotundata: Diversity, diel nifH expression and nitrogenase activity: Diversity, nifH expression and activity in seagrass
Open this publication in new window or tab >>Cyanobacteria associated with the phyllosphere of the seagrass Cymodocea rotundata: Diversity, diel nifH expression and nitrogenase activity: Diversity, nifH expression and activity in seagrass
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Tropical seagrass ecosystems are highly productive and extremely important for sustaining marine life. As seagrasses are associated with complex assemblages of poorly examined epiphytic microbes, we proposed that nitrogen-fixing microorganisms may contribute to the productivity. The morphological and genetic diversity (based on the 16S rRNA and nifH genes) of cyanobacteria and diel variations in nifH gene expression, NifH protein levels and nitrogenase (nitrogen-fixing) activity were examined in the phyllosphere of Cymodocea rotundata of coastal areas of the western Indian Ocean (Tanzania). The 16S rRNA and nifH gene analyses during two consecutive years (October-November, 2007 and 2008) revealed the dominance of a mixed cyanobacterial community. Most sequences represented free-living uncultured cyanobacteria previously reported as benthic in the region, clearly separated from marine planktonic phylotypes, while a few sequences clustered with cyanobacterial symbionts of diatoms. Appreciable, but varying nitrogenase activities were found on a diel as well as monthly basis, with the highest activity encountered, 358 ± 232 and 258 ± 139 nmol C2H4 g-1 h-1, in November. On a diel basis, nifH gene expression coincided with the NifH protein level (Oct 2008) and nitrogenase activity. At day time, nifH gene expression primarily originated from heterocystous phylotypes, while from non-heterocystous filamentous phylotypes (mainly Oscillatoriales) at night. The data suggest that a variety of diazotrophic cyanobacteria are common among the epiphytes on Cymodocea and we propose that these may represent a valuable source of ‘new’ nitrogen in the often oligotrophic, but ecologically important seagrass ecosystems.

Keyword
Cymodocea rotundata, diazotrophs, diversity, nifH, nitrogenase activity, seagras phyllosphere
National Category
Cell and Molecular Biology Botany Ecology
Research subject
Marine Ecology; Plant Physiology; Molecular Biology
Identifiers
urn:nbn:se:su:diva-38267 (URN)
Projects
Sida/SAREC Bilateral Marine Science Programme
Available from: 2010-04-06 Created: 2010-04-06 Last updated: 2010-04-07Bibliographically approved
4. Changes in the epiphytic cyanobacterial community and diazotrophic activity on the tropical seagrasses induced by varying nutrient regimes
Open this publication in new window or tab >>Changes in the epiphytic cyanobacterial community and diazotrophic activity on the tropical seagrasses induced by varying nutrient regimes
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Seagrasses were subject to different nitrogen (N) and phosphorus (P) regimes in a flow trough system (four weeks) to study the influence of moderate nutrient enrichments on the associated cyanobacterial diversity and diazotrophic activity. The seagrass Cymodocea serrulata (R. Brown) were collected outside an urbanized area, west of the Unguja Island, Zanzibar in the Indian Ocean. The epiphytic cyanobacterial community was characterized morphologically (light microscopy) and phylogenetically by DGGE fingerprinting using the 16S rRNA and nifH genes. A lower diversity of both heterocystous and non-heterocystous cyanobacteria was apparent in the natural seagrass stands, when compare to the pulsed nutrient additions that stimulated the growth of the cyanobacterial epiphytes. Non-heterocystous morpho- and genotypes (e.g. Lyngbya, Oscillatoria and Leptolyngbya) dominated and were intermixed with a few representatives of the heterocystous genus Calothrix. Many of the cyanobacterial sequences retrieved represented uncultured and potentially novel diazotrophic phylotypes. Diel nifH gene transcription levels and patterns, and the diel nitrogenase activity (acetylene reduction; max levels of 70.1 ±.19 nmol C2H4 g-1 h-1) verified the presence of a distinct proportion of diazotrophs, which however was negatively affected even by moderate nutrient additions. Although the seagrass host remained unaffected, the increased nutrients levels, mimicking anthropogenic eutrophication in these coastal regions, promoted a rapid change in the epiphytic community composition

Keyword
nifH gene, DGGE, epiphytes, diazotrophy, seagrass
National Category
Ecology Botany
Research subject
Marine Ecology; Plant Physiology
Identifiers
urn:nbn:se:su:diva-38271 (URN)
Projects
Sida/SAREC Bilateral Marine Science ProgrammeThe Swedish Foundation for International Cooperation in Research and Higher Education
Available from: 2010-04-06 Created: 2010-04-06 Last updated: 2011-04-14Bibliographically approved

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