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Kaarina Sivonen - One of the best experts on this subject based on the ideXlab platform.
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strains of the toxic and bloom forming Nodularia spumigena cyanobacteria can degrade methylphosphonate and release methane
The ISME Journal, 2018Co-Authors: Jonna E. Teikari, David P Fewer, Shengwei Hou, Wolfgang R. Hess, Rashmi Shrestha, Niina Leikoski, Minna Makela, Asko Simojoki, Kaarina SivonenAbstract:Nodularia spumigena is a nitrogen-fixing cyanobacterium that forms toxic blooms in the Baltic Sea each summer and the availability of phosphorous is an important factor limiting the formation of these blooms. Bioinformatic analysis identified a phosphonate degrading (phn) gene cluster in the genome of N. spumigena suggesting that this bacterium may use phosphonates as a phosphorus source. Our results show that strains of N. spumigena could grow in medium containing methylphosphonic acid (MPn) as the sole source of phosphorous and released methane when growing in medium containing MPn. We analyzed the total transcriptomes of N. spumigena UHCC 0039 grown using MPn and compared them with cultures growing in Pi-replete medium. The phnJ, phosphonate lyase gene, was upregulated when MPn was the sole source of phosphorus, suggesting that the expression of this gene could be used to indicate the presence of bioavailable phosphonates. Otherwise, growth on MPn resulted in only a minor reconstruction of the transcriptome and enabled good growth. However, N. spumigena strains were not able to utilize any of the anthropogenic phosphonates tested. The phosphonate utilizing pathway may offer N. spumigena a competitive advantage in the Pi-limited cyanobacterial blooms of the Baltic Sea.
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Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity
Frontiers Media S.A., 2018Co-Authors: Jonna E. Teikari, Shengwei Hou, Matti Wahlsten, Wolfgang R. Hess, Kaarina SivonenAbstract:Salinity is an important abiotic factor controlling the distribution and abundance of Nodularia spumigena, the dominating diazotrophic and toxic phototroph, in the brackish water cyanobacterial blooms of the Baltic Sea. To expand the available genomic information for brackish water cyanobacteria, we sequenced the isolate Nodularia spumigena UHCC 0039 using an Illumina-SMRT hybrid sequencing approach, revealing a chromosome of 5,294,286 base pairs (bp) and a single plasmid of 92,326 bp. Comparative genomics in Nostocales showed pronounced genetic similarity among Nodularia spumigena strains evidencing their short evolutionary history. The studied Baltic Sea strains share similar sets of CRISPR-Cas cassettes and a higher number of insertion sequence (IS) elements compared to Nodularia spumigena CENA596 isolated from a shrimp production pond in Brazil. Nodularia spumigena UHCC 0039 proliferated similarly at three tested salinities, whereas the lack of salt inhibited its growth and triggered transcriptome remodeling, including the up-regulation of five sigma factors and the down-regulation of two other sigma factors, one of which is specific for strain UHCC 0039. Down-regulated genes additionally included a large genetic region for the synthesis of two yet unidentified natural products. Our results indicate a remarkable plasticity of the Nodularia salinity acclimation, and thus salinity strongly impacts the intensity and distribution of cyanobacterial blooms in the Baltic Sea
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Table7.XLSX
2018Co-Authors: Jonna E. Teikari, Shengwei Hou, Matti Wahlsten, Wolfgang R. Hess, Kaarina SivonenAbstract:Salinity is an important abiotic factor controlling the distribution and abundance of Nodularia spumigena, the dominating diazotrophic and toxic phototroph, in the brackish water cyanobacterial blooms of the Baltic Sea. To expand the available genomic information for brackish water cyanobacteria, we sequenced the isolate Nodularia spumigena UHCC 0039 using an Illumina-SMRT hybrid sequencing approach, revealing a chromosome of 5,294,286 base pairs (bp) and a single plasmid of 92,326 bp. Comparative genomics in Nostocales showed pronounced genetic similarity among Nodularia spumigena strains evidencing their short evolutionary history. The studied Baltic Sea strains share similar sets of CRISPR-Cas cassettes and a higher number of insertion sequence (IS) elements compared to Nodularia spumigena CENA596 isolated from a shrimp production pond in Brazil. Nodularia spumigena UHCC 0039 proliferated similarly at three tested salinities, whereas the lack of salt inhibited its growth and triggered transcriptome remodeling, including the up-regulation of five sigma factors and the down-regulation of two other sigma factors, one of which is specific for strain UHCC 0039. Down-regulated genes additionally included a large genetic region for the synthesis of two yet unidentified natural products. Our results indicate a remarkable plasticity of the Nodularia salinity acclimation, and thus salinity strongly impacts the intensity and distribution of cyanobacterial blooms in the Baltic Sea.
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Image8.PDF
2018Co-Authors: Jonna E. Teikari, Shengwei Hou, Matti Wahlsten, Wolfgang R. Hess, Kaarina SivonenAbstract:Salinity is an important abiotic factor controlling the distribution and abundance of Nodularia spumigena, the dominating diazotrophic and toxic phototroph, in the brackish water cyanobacterial blooms of the Baltic Sea. To expand the available genomic information for brackish water cyanobacteria, we sequenced the isolate Nodularia spumigena UHCC 0039 using an Illumina-SMRT hybrid sequencing approach, revealing a chromosome of 5,294,286 base pairs (bp) and a single plasmid of 92,326 bp. Comparative genomics in Nostocales showed pronounced genetic similarity among Nodularia spumigena strains evidencing their short evolutionary history. The studied Baltic Sea strains share similar sets of CRISPR-Cas cassettes and a higher number of insertion sequence (IS) elements compared to Nodularia spumigena CENA596 isolated from a shrimp production pond in Brazil. Nodularia spumigena UHCC 0039 proliferated similarly at three tested salinities, whereas the lack of salt inhibited its growth and triggered transcriptome remodeling, including the up-regulation of five sigma factors and the down-regulation of two other sigma factors, one of which is specific for strain UHCC 0039. Down-regulated genes additionally included a large genetic region for the synthesis of two yet unidentified natural products. Our results indicate a remarkable plasticity of the Nodularia salinity acclimation, and thus salinity strongly impacts the intensity and distribution of cyanobacterial blooms in the Baltic Sea.
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DataSheet1.DOCX
2018Co-Authors: Jonna E. Teikari, Shengwei Hou, Matti Wahlsten, Wolfgang R. Hess, Kaarina SivonenAbstract:Salinity is an important abiotic factor controlling the distribution and abundance of Nodularia spumigena, the dominating diazotrophic and toxic phototroph, in the brackish water cyanobacterial blooms of the Baltic Sea. To expand the available genomic information for brackish water cyanobacteria, we sequenced the isolate Nodularia spumigena UHCC 0039 using an Illumina-SMRT hybrid sequencing approach, revealing a chromosome of 5,294,286 base pairs (bp) and a single plasmid of 92,326 bp. Comparative genomics in Nostocales showed pronounced genetic similarity among Nodularia spumigena strains evidencing their short evolutionary history. The studied Baltic Sea strains share similar sets of CRISPR-Cas cassettes and a higher number of insertion sequence (IS) elements compared to Nodularia spumigena CENA596 isolated from a shrimp production pond in Brazil. Nodularia spumigena UHCC 0039 proliferated similarly at three tested salinities, whereas the lack of salt inhibited its growth and triggered transcriptome remodeling, including the up-regulation of five sigma factors and the down-regulation of two other sigma factors, one of which is specific for strain UHCC 0039. Down-regulated genes additionally included a large genetic region for the synthesis of two yet unidentified natural products. Our results indicate a remarkable plasticity of the Nodularia salinity acclimation, and thus salinity strongly impacts the intensity and distribution of cyanobacterial blooms in the Baltic Sea.
Rehab Elshehawy - One of the best experts on this subject based on the ideXlab platform.
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insights into the physiology and ecology of the brackish water adapted cyanobacterium Nodularia spumigena ccy9414 based on a genome transcriptome analysis
PLOS ONE, 2013Co-Authors: Bjorn Vos, Birgitta Bergman, David P Fewer, Rehab Elshehawy, Henk Bolhuis, Matthias Kopf, Fred Moke, Fabian B Haas, P K Hayes, Kaarina SivonenAbstract:Nodularia spumigena is a filamentous diazotrophic cyanobacterium that dominates the annual late summer cyanobacterial blooms in the Baltic Sea. But N. spumigena also is common in brackish water bodies worldwide, suggesting special adaptation allowing it to thrive at moderate salinities. A draft genome analysis of N. spumigena sp. CCY9414 yielded a single scaffold of 5,462,271 nucleotides in length on which genes for 5,294 proteins were annotated. A subsequent strand-specific transcriptome analysis identified more than 6,000 putative transcriptional start sites (TSS). Orphan TSSs located in intergenic regions led us to predict 764 non-coding RNAs, among them 70 copies of a possible retrotransposon and several potential RNA regulators, some of which are also present in other N2-fixing cyanobacteria. Approximately 4% of the total coding capacity is devoted to the production of secondary metabolites, among them the potent hepatotoxin nodularin, the linear spumigin and the cyclic nodulapeptin. The transcriptional complexity associated with genes involved in nitrogen fixation and heterocyst differentiation is considerably smaller compared to other Nostocales. In contrast, sophisticated systems exist for the uptake and assimilation of iron and phosphorus compounds, for the synthesis of compatible solutes, and for the formation of gas vesicles, required for the active control of buoyancy. Hence, the annotation and interpretation of this sequence provides a vast array of clues into the genomic underpinnings of the physiology of this cyanobacterium and indicates in particular a competitive edge of N. spumigena in nutrient-limited brackish water ecosystems.
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characterization of nifh gene expression modification and rearrangement in Nodularia spumigena strain av1
FEMS Microbiology Ecology, 2011Co-Authors: Simina Vintila, Birgitta Bergman, Tiago Toscano Selao, Agneta Noren, Rehab ElshehawyAbstract:The annually reoccurring blooms that characterize the surface waters of the Baltic Sea are dominated by filamentous, heterocystous cyanobacteria such as Nodularia spumigena. In a previous study, we have demonstrated that N. spumigena strain AV1 differentiates heterocysts in the absence of detectable nitrogen fixation activity, an unusual physiological trait that is clearly distinct from other well-studied cyanobacteria. To further analyze the uncoupling between these two processes, we analyzed the gene expression and modification of the nitrogenase enzyme (the enzyme responsible for nitrogen fixation) in N. spumigena AV1, as well as in several other N. spumigena strains. Here, we demonstrate the occurrence of two nifH gene copies in N. spumigena strain AV1, only one of which is located in a complete nifHDK cluster and several NifH protein forms. Furthermore, we demonstrate the occurrence of a DNA rearrangement mechanism acting within the nifH gene copy located in the nifHDK cluster and present only in the strains exhibiting the previously reported uncoupling between heterocyst differentiation and nitrogen fixation processes. These data stress the existence of a distinct and complex regulatory circuit related to nitrogen fixation in this ecologically significant bloom-forming cyanobacterium.
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variability in the response of the cyanobacterium Nodularia spumigena to nitrogen supplementation
Journal of Environmental Monitoring, 2010Co-Authors: Simina Vintila, Rehab ElshehawyAbstract:Nodularia spumigena is a filamentous cyanobacterium that is commonly found in brackish water bodies. The species is capable of fixing atmospheric nitrogen in specialized cells termed heterocysts. N. spumigena dominates the annual toxic summer blooms in the Baltic Sea causing environmental and economical problems. We have previously demonstrated that N. spumigena strain AV1 exhibits a different response to the presence of combined nitrogen as compared to model cyanobacteria such as Nostoc PCC7120 and Nostoc punctiforme by uncoupling between nitrogen fixation and heterocyst differentiation. In order to assess whether or not the behaviour of N. spumigena strain AV1 is characteristic of N. spumigena populations, especially in the Baltic Sea, we have investigated the effect of nitrate and ammonium ions on growth, nitrogen fixation activity and presence of heterocysts in eight different Nodularia strains. Our results show that most of the strains retain heterocysts in the absence of nitrogenase activity indicating that uncoupling between nitrogen fixation and heterocyst differentiation is most likely a common behaviour among N. spumigena strains, especially in the Baltic Sea. In addition, there are variations between strains in regard to nitrate uptake.
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proteomic profiling of the baltic sea cyanobacterium Nodularia spumigena strain av1 during ammonium supplementation
Journal of Proteomics, 2010Co-Authors: Simina Vintila, Sara Jonasson, Henrik Wadensten, Anna Nilsson, Per E Andren, Rehab ElshehawyAbstract:The cyanobacterium Nodularia spumigena dominates the annual, toxic summer blooms in the Baltic Sea. Although Nodularia has been receiving attention due to its production of the hepatotoxin nodularin, molecular data regarding the regulation of nitrogen fixation is lacking. We have previously reported that N. spumigena strain AV1, unlike model filamentous cyanobacteria, differentiates heterocysts in the absence of detectable nitrogen fixation activity. To further analyze the uncoupling between these two linked processes, we assessed the impact of ammonium ions on the N. spumigena metabolism using a proteomic approach. Proteomic profiling was performed at three different times during ammonium supplementation using quantitative 2-dimensional gel electrophoresis followed by MS/MS analysis. Using this approach, we identified 34 proteins, 28 of which were unique proteins that changed successively in abundance during growth on ammonium. Our results indicate that N. spumigena generally exhibits lower energy production and carbon fixation in the presence of ammonium and seems to be inefficient in utilizing ammonium as an external nitrogen source. The possibility of ammonium toxicity due to PSII damage was investigated and the results are discussed. Our findings have implications in regard to the strategies considered to manage the cyanobacterial blooms in the Baltic Sea.
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expression of the nodularin synthetase genes in the baltic sea bloom former cyanobacterium Nodularia spumigena strain av1
FEMS Microbiology Ecology, 2008Co-Authors: Sara Jonasson, Kaarina Sivonen, Simina Vintila, Rehab ElshehawyAbstract: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.
Edna Graneli - One of the best experts on this subject based on the ideXlab platform.
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influence of acartia cf bifilosa copepoda on morphology and toxicity of Nodularia spumigena cyanophyceae
Harmful Algae, 2012Co-Authors: Veronica M Lundgren, Edna Graneli, Stephan PflugmacherAbstract:Nodularia spumigena was exposed directly and indirectly (grazer cages) to increasing densities of Acartia cf. bifilosa to investigate if the presence of copepods influenced the morphology and/or the toxicity of the cyanobacterium. Monocultures with only N. spumigena and mixed cultures, containing N. spumigena and the non-toxic Dunaliella tertiolecta, were included in each experiment. Following 6 days of incubation, the morphology and toxicity in grazer treatments were compared with grazer-free controls. We observed no effects of A. cf. bifilosa on either morphology or toxicity of N. spumigena. The lack of grazer induced nodularin production and morphological alterations suggest that these two potential defense strategies either has evolved as constitutive defenses or never evolved as grazer defenses. The mortality of copepods was higher in the monoculture than in the mixed culture treatments. Gut content observations indicated a low level of grazing in monoculture treatments and a higher level of grazing in mixed culture treatments. This higher level of grazing most likely occurred on the alternative food D. tertiolecta. Given the indications of low grazing and the concentrations of dissolved nodularin observed, we postulate that the higher mortality was not related to toxic effects, but to starvation. This in turn may have resulted from bad taste, production of unknown grazer deterrents or morphological constraints; although the size of the filaments would not have imposed an absolute limit for ingestion by A. cf. bifilosa. The higher copepod mortality observed on monocultures of N. spumigena may contribute to the success and maintenance of N. spumigena blooms.
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estimating the accumulation and transfer of Nodularia spumigena toxins by the blue mussel mytilus edulis an appraisal from culture and mesocosm experiments
Toxicon, 2006Co-Authors: Evangeli Strogyloudi, Catherine Legrand, Antonia Giannakourou, A Ruehl, Edna GraneliAbstract:Accumulation of Nodularia spumigena toxins by Mytilus edulis was studied during laboratory and mesocosm experiments in order to investigate the possible pathways of nodularin in mussels and calculate toxin budgets. Mussels were exposed to 0.2-15.6 microg nodularin l(-1), fed for up to 5 days with Nodularia cells from culture, or blooming in different nutrient-treated seawater. Toxin concentration was monitored with LC-ESI-MS. During different exposures, the amount of nodularin detected in mussels increased linearly with increasing toxin concentration in food and attained 0.28-13.8 microg of nodularin g dw(-1) of the mussel whole body tissue after 12 h. The digestive gland was found to be the tissue with the highest toxin concentration. Nodularin concentration in faeces was not proportional to faeces production or to toxin concentration in food; however, it seemed to be mostly related to food quality as well as to food availability. The percentage of nodularin taken up by the mussels, relative to the amount contained in the offered food, varied from 10% to 20%, depending on food quality. During a 5-day toxin accumulation experiment, the acute reduction of the toxin in mussel tissues the second day and the following stabilization, showed that probably mussels maintain low toxin levels via efficient elimination and/or toxin metabolism. After a 72 h depuration period, mussels showed 75% reduction in their toxin content.
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allelopathic effects of the baltic cyanobacteria Nodularia spumigena aphanizomenon flos aquae and anabaena lemmermannii on algal monocultures
Journal of Experimental Marine Biology and Ecology, 2004Co-Authors: Sanna Suikkanen, Giovana O Fistarol, Edna GraneliAbstract:Allelopathy, the release of extracellular compounds that inhibit the growth of other microorganisms, may be one factor contributing to the formation and/or maintenance of cyanobacterial blooms. We investigated the allelopathic effects of three cyanobacterial species (Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii) that frequently form mass-occurrences in the Baltic Sea. We exposed monocultures of three phytoplankton species (Thalassiosira weissflogii, Rhodomonas sp. and Prymnesium parvum) to cell-free filtrates of the three cyanobacteria, and quantified allelopathic effects with cell counts. We also investigated the role of the growth phase of cyanobacteria in their allelopathy, by comparing the effects of an exponential and a stationary phase culture of N. spumigena. All tested cyanobacteria inhibited the growth of Rhodomonas sp., but none of them affected P. parvum. The effects on T weissflogii were more variable, and they were amplified by repeated filtrate additions compared to a single filtrate addition. N. spumigena was more allelopathic in exponential than in stationary growth phase, whereas the culture filtrate was more hepatotoxic in stationary phase. Hepatotoxins were thus probably not involved in the allelopathic effects, which is also indicated by the allelopathic properties of the non-toxic A. flos-aquae and A. lemmermannii. The results demonstrate that the common Baltic cyanobacteria affect some coexisting phytoplankton species negatively. Allelopathy may therefore play a role in interspecific competition and contribute to cyanobacterial bloom maintenance. (Less)
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molecular identification of bacteria associated with filaments of Nodularia spumigena and their effect on the cyanobacterial growth
Harmful Algae, 2003Co-Authors: Paulo S Salomon, Sven Janson, Edna GraneliAbstract:Colonial and filamentous cyanobacteria frequently have bacteria associated with their extracellular mucus zone or more tightly attached to their cells surface. The toxin-producing cyanobacterium Nodularia spumigena is an important component of the Baltic Sea plankton community, and its filaments are likely to provide a microenvironment suitable for the development of a particular bacteria flora. In the present work, 13 bacterial strains associated with filaments of N. spumigena from the Baltic Sea were isolated and identified by sequencing the 16S rRNA gene. Different bacterial lineages were found associated with the cyanobacterial filaments, including the alpha, beta, and gamma subdivisions of the class Proteobacter and the division Firmicutes (Gram-positive bacteria). Several 16S rRNA gene sequences were not closely related to previously reported sequences of cultured bacteria from the Baltic Sea or to any other reported sequence. Conversely, sequences related to the gamma Proteobacter genus Shewanella, a group previously described in the Baltic Sea, were found among the isolates. The bacterial isolates were grown and added to cultures of exponentially growing N. spumigena. Five isolates, related to the alpha and gamma Proteobacter and Firmicutes, affected negatively the cyanobacterial growth, leading to a lower biomass yield up to 38% relative to controls with no bacteria addition. Five gamma Proteobacter-related strains had no effect on the cyanobacterial growth, while three strains related to Shewanella baltica had a positive effect. Although none of the bacterial isolates showed strong algicidal effect, the observed stimulatory and retarding effects on N. spumigena growth under culture conditions denotes the importance of the associated bacterial community for the dynamics of these cyanobacterial populations in nature. Moreover, several new taxa recovered in this study probably belong to species not yet described.
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modeling the increase of nodularin content in baltic sea Nodularia spumigena during stationary phase in phosphorus limited batch cultures
FEMS Microbiology Ecology, 2002Co-Authors: Willem Stolte, Chatarina Karlsson, Per Carlsson, Edna GraneliAbstract:Nodularin (Nod), produced by the brackish/marine cyanobacterium Nodularia spumigena, is a potent hepatotoxin, tumor promoter and is possibly carcinogenic to mammals. It is structurally and toxicologically related to the microcystins, produced by Microcystis aeruginosa in fresh water. A better understanding of the kinetics of Nod production might provide an insight into the physiological and ecological function of cyanobacterial hepatotoxins. The present study presents a simple model simulating the concentration of Nod in N. spumigena KAC66 during phosphorus-limited growth. The main assumption of the model is that the Nod production rate is proportional to the chlorophyll-a (Chla) concentration. The model was tuned to data from phosphorus-limited batch cultures of N. spumigena KAC66 at saturating light and was able to predict 96% or more of the variation in both Chla and Nod concentration. No significant effect of available nitrogen source was found on the Chla-specific Nod production rate although specific growth rates were higher in ammonium and nitrate grown cultures compared to cultures grown with N2 as the sole nitrogen source. Literature data on microcystin production by M. aeruginosa in phosphorus-limited chemostats fitted the model predictions well, except at very low dilution rates (0.1 day−1). The good fit with the proposed model to our own and literature data suggests that the production of hepatotoxic cyanotoxins is not regulated upon growth reduction due to phosphate limitation.
David P Fewer - One of the best experts on this subject based on the ideXlab platform.
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strains of the toxic and bloom forming Nodularia spumigena cyanobacteria can degrade methylphosphonate and release methane
The ISME Journal, 2018Co-Authors: Jonna E. Teikari, David P Fewer, Shengwei Hou, Wolfgang R. Hess, Rashmi Shrestha, Niina Leikoski, Minna Makela, Asko Simojoki, Kaarina SivonenAbstract:Nodularia spumigena is a nitrogen-fixing cyanobacterium that forms toxic blooms in the Baltic Sea each summer and the availability of phosphorous is an important factor limiting the formation of these blooms. Bioinformatic analysis identified a phosphonate degrading (phn) gene cluster in the genome of N. spumigena suggesting that this bacterium may use phosphonates as a phosphorus source. Our results show that strains of N. spumigena could grow in medium containing methylphosphonic acid (MPn) as the sole source of phosphorous and released methane when growing in medium containing MPn. We analyzed the total transcriptomes of N. spumigena UHCC 0039 grown using MPn and compared them with cultures growing in Pi-replete medium. The phnJ, phosphonate lyase gene, was upregulated when MPn was the sole source of phosphorus, suggesting that the expression of this gene could be used to indicate the presence of bioavailable phosphonates. Otherwise, growth on MPn resulted in only a minor reconstruction of the transcriptome and enabled good growth. However, N. spumigena strains were not able to utilize any of the anthropogenic phosphonates tested. The phosphonate utilizing pathway may offer N. spumigena a competitive advantage in the Pi-limited cyanobacterial blooms of the Baltic Sea.
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Insights into the Physiology and Ecology of the Brackish- Water-Adapted Cyanobacterium Nodularia spumigena CCY9414 Based on a Genome-Transcriptome Analysis
2016Co-Authors: Henk Bolhuis, Kaarina Sivonen, Birgitta Bergman, David P Fewer, Rehab El-shehawy, Matthias Kopf, Fabian Haas, Paul Hayes, Elke Dittmann, Dave J. ScanlanAbstract:Nodularia spumigena is a filamentous diazotrophic cyanobacterium that dominates the annual late summer cyanobacterial blooms in the Baltic Sea. But N. spumigena also is common in brackish water bodies worldwide, suggesting special adaptation allowing it to thrive at moderate salinities. A draft genome analysis of N. spumigena sp. CCY9414 yielded a single scaffold of 5,462,271 nucleotides in length on which genes for 5,294 proteins were annotated. A subsequent strand-specific transcriptome analysis identified more than 6,000 putative transcriptional start sites (TSS). Orphan TSSs located in intergenic regions led us to predict 764 non-coding RNAs, among them 70 copies of a possible retrotransposon and several potential RNA regulators, some of which are also present in other N2-fixing cyanobacteria. Approximately 4 % of the total coding capacity is devoted to the production of secondary metabolites, among them the potent hepatotoxin nodularin, the linear spumigin and the cyclic nodulapeptin. The transcriptional complexity associated with genes involved in nitrogen fixation and heterocyst differentiation is considerably smaller compared to other Nostocales. In contrast, sophisticated systems exis
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Pseudoaeruginosins, Nonribosomal Peptides in Nodularia spumigena
2015Co-Authors: Liwei Liu, David P Fewer, Matti Wahlsten, Adnan Budnjo, Jouni Jokela, Bengt Erik Haug, Leo Rouhiainen, Perttu Permi, Torgils Fossen, Kaarina SivonenAbstract:Nodularia spumigena is a filamentous cyanobacterium that forms toxic blooms in brackish waters around the world through the production of the pentapeptide toxin nodularin. This cyanobacterium also produces large amounts of protease inhibitors belonging to the aeruginosin and spumigin families. Here we report the discovery of previously unknown protease inhibitors, pseudoaeruginosins NS1 (1) and NS2 (2), from 33 strains of N. spumigena isolated from the Baltic Sea. Pseudoaeruginosin NS1 (1) and NS2 (2) contain hexanoic acid, tyrosine, 4-methylproline, and argininal/argininol. The chemical structure of the two pseudoaeruginosins was verified by thorough comparison of the liquid chromatography–mass spectrometry (LC–MS) analyses of the extracts from the N. spumigena strains with synthetic peptides. The structures of the synthetic pseudoaeruginosins were confirmed using nuclear magnetic resonance spectroscopy. Surprisingly, the structure of pseudoaeruginosin NS1 (1) and NS2 (2) combines features of both aeruginosins and spumigins, suggesting that they have been produced through the joint action of both the spumigin and aeruginosin biosynthesis pathways. We screened with polymerase chain reaction and LC–MS 68 N. spumigena strains from the Baltic Sea and Australia. Pseudoaeruginosins were present in half of the Baltic Sea strains but were not found from the Australian strains. The production of pseudoaeruginosin seems to be coupled to the production of aeruginosins and 4-methylproline-containing spumigins. Pseudoaeruginosin NS1 was found to be as potent trypsin inhibitor as the most potent aeruginosins and spumigins with an IC50 of 0.19 ± 0.04 μM. This finding suggests that cooperation between the spumigin and aeruginosin biosynthetic pathways results in hybrid pseudoaeruginosin peptides
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new structural variants of aeruginosin produced by the toxic bloom forming cyanobacterium Nodularia spumigena
PLOS ONE, 2013Co-Authors: David P Fewer, Matti Wahlsten, Jouni Jokela, Leo Rouhiainen, Perttu Permi, Eeva Paukku, Julia Osterholm, Olli Aitio, Gonzalo V Gomezsaez, Kaarina SivonenAbstract:Nodularia spumigena is a filamentous diazotrophic cyanobacterium that forms blooms in brackish water bodies. This cyanobacterium produces linear and cyclic peptide protease inhibitors which are thought to be part of a chemical defense against grazers. Here we show that N. spumigena produces structurally novel members of the aeruginosin family of serine protease inhibitors. Extensive chemical analyses including NMR demonstrated that the aeruginosins are comprised of an N-terminal short fatty acid chain, L-Tyr, L-Choi and L-argininal and in some cases pentose sugar. The genome of N. spumigena CCY9414 contains a compact 18-kb aeruginosin gene cluster encoding a peptide synthetase with a reductive release mechanism which offloads the aeruginosins as reactive peptide aldehydes. Analysis of the aeruginosin and spumigin gene clusters revealed two different strategies for the incorporation of N-terminal protecting carboxylic acids. These results demonstrate that strains of N. spumigena produce aeruginosins and spumigins, two families of structurally similar linear peptide aldehydes using separate peptide synthetases. The aeruginosins were chemically diverse and we found 11 structural variants in 16 strains from the Baltic Sea and Australia. Our findings broaden the known structural diversity of the aeruginosin peptide family to include peptides with rare N-terminal short chain (C2–C10) fatty acid moieties.
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insights into the physiology and ecology of the brackish water adapted cyanobacterium Nodularia spumigena ccy9414 based on a genome transcriptome analysis
PLOS ONE, 2013Co-Authors: Bjorn Vos, Birgitta Bergman, David P Fewer, Rehab Elshehawy, Henk Bolhuis, Matthias Kopf, Fred Moke, Fabian B Haas, P K Hayes, Kaarina SivonenAbstract:Nodularia spumigena is a filamentous diazotrophic cyanobacterium that dominates the annual late summer cyanobacterial blooms in the Baltic Sea. But N. spumigena also is common in brackish water bodies worldwide, suggesting special adaptation allowing it to thrive at moderate salinities. A draft genome analysis of N. spumigena sp. CCY9414 yielded a single scaffold of 5,462,271 nucleotides in length on which genes for 5,294 proteins were annotated. A subsequent strand-specific transcriptome analysis identified more than 6,000 putative transcriptional start sites (TSS). Orphan TSSs located in intergenic regions led us to predict 764 non-coding RNAs, among them 70 copies of a possible retrotransposon and several potential RNA regulators, some of which are also present in other N2-fixing cyanobacteria. Approximately 4% of the total coding capacity is devoted to the production of secondary metabolites, among them the potent hepatotoxin nodularin, the linear spumigin and the cyclic nodulapeptin. The transcriptional complexity associated with genes involved in nitrogen fixation and heterocyst differentiation is considerably smaller compared to other Nostocales. In contrast, sophisticated systems exist for the uptake and assimilation of iron and phosphorus compounds, for the synthesis of compatible solutes, and for the formation of gas vesicles, required for the active control of buoyancy. Hence, the annotation and interpretation of this sequence provides a vast array of clues into the genomic underpinnings of the physiology of this cyanobacterium and indicates in particular a competitive edge of N. spumigena in nutrient-limited brackish water ecosystems.
Hanna Mazurmarzec - One of the best experts on this subject based on the ideXlab platform.
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competitive interactions as a mechanism for chemical diversity maintenance in Nodularia spumigena
Scientific Reports, 2021Co-Authors: Sandra Lage, Hanna Mazurmarzec, Elena GorokhovaAbstract:Nodularia spumigena is a bloom-forming diazotrophic cyanobacterium inhabiting brackish waters worldwide. This species produces non-ribosomal peptides (NRPs), including the hepatotoxin nodularin, often referred to as cyanotoxin. Several known classes of NRPs have various biological activities, although their modes of action are poorly understood. In the Baltic N. spumigena, there is a high NRP chemodiversity among strains, allowing their grouping in specific chemotypes and subgroups. Therefore, it is relevant to ask whether the NRP production is affected by intraspecific interactions between the co-existing strains. Using a novel approach that combines culture technique and liquid chromatography-tandem mass spectrometry for the NRP analysis, we examined N. spumigena strains under mono- and co-culture conditions. The test strains were selected to represent N. spumigena belonging to the same or different chemotype subgroups. In this setup, we observed physiological and metabolic responses in the test strains grown without cell contact. The changes in NRP levels to co-culture conditions were conserved within a chemotype subgroup but different between the subgroups. Our results suggest that intraspecific interactions may promote a chemical diversity in N. spumigena population, with higher NRP production compared to a single-strain population. Studying allelochemical signalling in this cyanobacterium is crucial for understanding toxicity mechanisms and plankton community interactions in the Baltic Sea and other aquatic systems experiencing regular blooms.
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effect of crude extracts from Nodularia spumigena on round goby neogobius melanostomus
Marine Environmental Research, 2018Co-Authors: Ilona Zloch, Agnieszka Hebel, Hanna MazurmarzecAbstract:Abstract Nodularia spumigena is a nitrogen-fixing filamentous cyanobacteria in the Baltic Sea. Nodularin (NOD), the hepatotoxic peptide produced by this cyanobacterium, accumulates in the organisms from different trophic levels. In this paper, the effects of N. spumigena cell extract on the round goby (Neogobius melanostomus) was investigated under laboratory conditions. This benthic fish species feed on mussels in which nodularin accumulation was well documented. In current study a sharp increase in the NOD concentration in analyzed organs was observed after 24 h (PPIA) after 72 h of exposure (LC/MS). To determine the direction and strength of the changes induced in the fish by the toxin, several biochemical markers of exposure such as concentration of glutathione and activities of catalase, guaiacol peroxidase and glutathione S-transferase were used. In analyzed organs (liver, gills and muscle) of the round goby, the activity of these enzymes were suppressed. Higher GSH/protein amount and CAT and POD activity in gills than in liver reflects the importance of gills in NOD entering into analyzed fish body when exposed to toxin. The results indicate that the round goby (Neogobius melanostomus) exposed to extracts from N. spumigena cells triggered a defense system in a time-dependent manner. The obtained results contribute to a better understanding of fish response to the presence of compounds produced by N. spumigena.
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chemical and genetic diversity of Nodularia spumigena from the baltic sea
Marine Drugs, 2016Co-Authors: Hanna Mazurmarzec, Mireia Bertosfortis, Anna Torunskasitarz, Anna Fidor, Catherine LegrandAbstract:Nodularia spumigena is a toxic, filamentous cyanobacterium occurring in brackish waters worldwide, yet forms extensive recurrent blooms in the Baltic Sea. N. spumigena produces several classes of non-ribosomal peptides (NRPs) that are active against several key metabolic enzymes. Previously, strains from geographically distant regions showed distinct NRP metabolic profiles. In this work, conspecific diversity in N. spumigena was studied using chemical and genetic approaches. NRP profiles were determined in 25 N. spumigena strains isolated in different years and from different locations in the Baltic Sea using liquid chromatography-tandem mass spectrometry (LC-MS/MS). Genetic diversity was assessed by targeting the phycocyanin intergenic spacer and flanking regions (cpcBA-IGS). Overall, 14 spumigins, 5 aeruginosins, 2 pseudaeruginosins, 2 nodularins, 36 anabaenopeptins, and one new cyanopeptolin-like peptide were identified among the strains. Seven anabaenopeptins were new structures; one cyanopeptolin-like peptide was discovered in N. spumigena for the first time. Based on NRP profiles and cpcBA-IGS sequences, the strains were grouped into two main clusters without apparent influence of year and location, indicating persistent presence of these two subpopulations in the Baltic Sea. This study is a major step in using chemical profiling to explore conspecific diversity with a higher resolution than with a sole genetic approach.
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Nodularia spumigena peptides accumulation and effect on aquatic invertebrates
Toxins, 2015Co-Authors: Hanna Mazurmarzec, Katarzyna Sutryk, Agnieszka Hebel, Natalia Hohlfeld, Anna Pietrasik, Agata BlaszczykAbstract:Thus far, the negative effects of Nodularia spumigena blooms on aquatic organisms have been mainly attributed to the production of the hepatotoxic nodularin (NOD). In the current work, the accumulation of other N. spumigena metabolites in blue mussels and crustaceans, and their effect on Thamnocephalus platyurus and Artemia franciscana, were examined. The liquid chromatography-tandem mass spectrometry (LC-MS/MS) analyses provided evidence that both blue mussels collected after a cyanobacterial bloom in the Baltic Sea and the crustaceans exposed under laboratory conditions to N. spumigena extract accumulated the cyclic anabaenopeptins (APs). In the crustaceans, the linear peptides, spumigins (SPUs) and aeruginosins (AERs), were additionally detected. Exposure of T. platyurus and A. franciscana to N. spumigena extract confirmed the negative effect of nodularin on the organisms. However, high numbers of dead crustaceans were also recorded in the nodularin-free fraction, which contained protease inhibitors classified to spumigins and aeruginosins. These findings indicate that cyanobacterial toxicity to aquatic organisms is a complex phenomenon and the induced effects can be attributed to diverse metabolites, not only to the known hepatotoxins.
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diversity of peptides produced by Nodularia spumigena from various geographical regions
Marine Drugs, 2012Co-Authors: Hanna Mazurmarzec, Agata Blaszczyk, Monika J Kaczkowska, Reyhan Akcaalan, Lisa Spoof, Jussi MeriluotoAbstract:Cyanobacteria produce a great variety of non-ribosomal peptides. Among these compounds, both acute toxins and potential drug candidates have been reported. The profile of the peptides, as a stable and specific feature of an individual strain, can be used to discriminate cyanobacteria at sub-population levels. In our work, liquid chromatography-tandem mass spectrometry was used to elucidate the structures of non-ribosomal peptides produced by Nodularia spumigena from the Baltic Sea, the coastal waters of southern Australia and Lake Iznik in Turkey. In addition to known structures, 9 new congeners of spumigins, 4 aeruginosins and 12 anabaenopeptins (nodulapeptins) were identified. The production of aeruginosins by N. spumigena was revealed in this work for the first time. The isolates from the Baltic Sea appeared to be the richest source of the peptides; they also showed a higher diversity in peptide profiles. The Australian strains were characterized by similar peptide patterns, but distinct from those represented by the Baltic and Lake Iznik isolates. The results obtained with the application of the peptidomic approach were consistent with the published data on the genetic diversity of the Baltic and Australian populations.